75 results on '"Donner TH"'
Search Results
2. Temporal integration in visual motion detection with temporal uncertainty
- Author
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Pfeffer, T, Tsetsos, K, Jentgens, P, Knapen, T, Usher, M, and Donner, TH
- Published
- 2016
3. Task-irrelevant stimuli reliably boost phasic pupil-linked arousal but do not affect decision formation.
- Author
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Hebisch J, Ghassemieh AC, Zhecheva E, Brouwer M, van Gaal S, Schwabe L, Donner TH, and de Gee JW
- Subjects
- Humans, Male, Female, Adult, Young Adult, Cognition physiology, Reaction Time physiology, Locus Coeruleus physiology, Pupil physiology, Arousal physiology, Decision Making physiology, Acoustic Stimulation
- Abstract
The arousal systems of the brainstem, specifically the locus coeruleus-noradrenaline system, respond "phasically" during decisions. These central arousal transients are accompanied by dilations of the pupil. Mechanistic attempts to understand the impact of phasic arousal on cognition would benefit from temporally precise experimental manipulations. Here, we evaluated a non-invasive candidate approach to manipulate arousal in humans: presenting task-irrelevant auditory stimuli at different latencies during the execution of a challenging task. Task-irrelevant auditory stimuli drive responses of brainstem nuclei involved in the control of pupil size, but it is unknown whether such sound-evoked responses mimic the central arousal transients evoked during cognitive computations. A large body of evidence has implicated central arousal transients in reducing bias during challenging perceptual decisions. We thus used challenging visual decisions as a testbed, combining them with task-irrelevant sounds of varying onset latency or duration. Across three experiments, the sounds consistently elicited well-controlled pupil responses that superimposed onto task-evoked responses. While we replicated a negative correlation between task-evoked pupil responses and bias, the task-irrelevant sounds had no behavioral effect. This dissociation suggests that cognitive task engagement and task-irrelevant sounds may recruit distinct neural systems contributing to the control of pupil size., Competing Interests: Declarations Competing interests The authors declare no competing interests., (© 2024. The Author(s).)
- Published
- 2024
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4. Individual differences in belief updating and phasic arousal are related to psychosis proneness.
- Author
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Murphy PR, Krkovic K, Monov G, Kudlek N, Lincoln T, and Donner TH
- Abstract
Many decisions entail the updating of beliefs about the state of the environment by accumulating noisy sensory evidence. This form of probabilistic reasoning may go awry in psychosis. Computational theory shows that optimal belief updating in environments subject to hidden changes in their state requires a dynamic modulation of the evidence accumulation process. Recent empirical findings implicate transient responses of pupil-linked central arousal systems to individual evidence samples in this modulation. Here, we analyzed behavior and pupil responses during evidence accumulation in a changing environment in a community sample of human participants. We also assessed their subclinical psychotic experiences (psychosis proneness). Participants most prone to psychosis showed overall less flexible belief updating profiles, with diminished behavioral impact of evidence samples occurring late during decision formation. These same individuals also exhibited overall smaller pupil responses and less reliable pupil encoding of computational variables governing the dynamic belief updating. Our findings provide insights into the cognitive and physiological bases of psychosis proneness and open paths to unraveling the pathophysiology of psychotic disorders., (© 2024. The Author(s).)
- Published
- 2024
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5. Confirmation Bias through Selective Use of Evidence in Human Cortex.
- Author
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Park H, Arazi A, Talluri BC, Celotto M, Panzeri S, Stocker AA, and Donner TH
- Abstract
Decision-makers often process new evidence selectively, depending on their current beliefs about the world. We asked whether such confirmation biases result from biases in the encoding of sensory evidence in the brain, or alternatively in the utilization of encoded evidence for behavior. Human participants estimated the source of a sequence of visual-spatial evidence samples while we measured cortical population activity with magnetoencephalography (MEG). Halfway through the sequence, participants were prompted to judge the more likely source category. Their processing of subsequent evidence depended on its consistency with the previously chosen category, but the encoding of evidence in cortical activity did not. Instead, the encoded evidence in parietal and primary visual cortex contributed less to the estimation report when that evidence was inconsistent with the previous choice. We conclude that confirmation bias originates from the way in which decision-makers utilize information encoded in the brain. This provides room for deliberative control.
- Published
- 2024
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6. Linking Cognitive Integrity to Working Memory Dynamics in the Aging Human Brain.
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Monov G, Stein H, Klock L, Gallinat J, Kühn S, Lincoln T, Krkovic K, Murphy PR, and Donner TH
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- Humans, Male, Female, Aged, Adult, Middle Aged, Young Adult, Cognitive Dysfunction physiopathology, Cognitive Dysfunction psychology, Cognition physiology, Neuropsychological Tests, Aged, 80 and over, Models, Neurological, Memory, Short-Term physiology, Aging physiology, Aging psychology, Magnetoencephalography, Brain physiology
- Abstract
Aging is accompanied by a decline of working memory, an important cognitive capacity that involves stimulus-selective neural activity that persists after stimulus presentation. Here, we unraveled working memory dynamics in older human adults (male and female) including those diagnosed with mild cognitive impairment (MCI) using a combination of behavioral modeling, neuropsychological assessment, and MEG recordings of brain activity. Younger adults (male and female) were studied with behavioral modeling only. Participants performed a visuospatial delayed match-to-sample task under systematic manipulation of the delay and distance between sample and test stimuli. Their behavior (match/nonmatch decisions) was fit with a computational model permitting the dissociation of noise in the internal operations underlying the working memory performance from a strategic decision threshold. Task accuracy decreased with delay duration and sample/test proximity. When sample/test distances were small, older adults committed more false alarms than younger adults. The computational model explained the participants' behavior well. The model parameters reflecting internal noise (not decision threshold) correlated with the precision of stimulus-selective cortical activity measured with MEG during the delay interval. The model uncovered an increase specifically in working memory noise in older compared with younger participants. Furthermore, in the MCI group, but not in the older healthy controls, internal noise correlated with the participants' clinically assessed cognitive integrity. Our results are consistent with the idea that the stability of working memory contents deteriorates in aging, in a manner that is specifically linked to the overall cognitive integrity of individuals diagnosed with MCI., Competing Interests: The authors declare no competing financial interests., (Copyright © 2024 Monov et al.)
- Published
- 2024
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7. 40 Hz Steady-State Response in Human Auditory Cortex Is Shaped by Gabaergic Neuronal Inhibition.
- Author
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Toso A, Wermuth AP, Arazi A, Braun A, Jong TG, Uhlhaas PJ, and Donner TH
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- Humans, Male, Female, Adult, Young Adult, Neural Inhibition physiology, Neural Inhibition drug effects, Acoustic Stimulation, Auditory Cortex drug effects, Auditory Cortex physiology, Magnetoencephalography, Evoked Potentials, Auditory drug effects, Evoked Potentials, Auditory physiology, GABAergic Neurons physiology, GABAergic Neurons drug effects
- Abstract
The 40 Hz auditory steady-state response (ASSR), an oscillatory brain response to periodically modulated auditory stimuli, is a promising, noninvasive physiological biomarker for schizophrenia and related neuropsychiatric disorders. The 40 Hz ASSR might be amplified by synaptic interactions in cortical circuits, which are, in turn, disturbed in neuropsychiatric disorders. Here, we tested whether the 40 Hz ASSR in the human auditory cortex depends on two key synaptic components of neuronal interactions within cortical circuits: excitation via N-methyl-aspartate glutamate (NMDA) receptors and inhibition via gamma-amino-butyric acid (GABA) receptors. We combined magnetoencephalography (MEG) recordings with placebo-controlled, low-dose pharmacological interventions in the same healthy human participants (13 males, 7 females). All participants exhibited a robust 40 Hz ASSR in auditory cortices, especially in the right hemisphere, under a placebo. The GABA
A receptor-agonist lorazepam increased the amplitude of the 40 Hz ASSR, while no effect was detectable under the NMDA blocker memantine. Our findings indicate that the 40 Hz ASSR in the auditory cortex involves synaptic (and likely intracortical) inhibition via the GABAA receptor, thus highlighting its utility as a mechanistic signature of cortical circuit dysfunctions involving GABAergic inhibition., Competing Interests: The authors declare no competing financial interests., (Copyright © 2024 Toso et al.)- Published
- 2024
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8. Adaptive biasing of action-selective cortical build-up activity by stimulus history.
- Author
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Braun A and Donner TH
- Subjects
- Humans, Bias, Uncertainty, Magnetoencephalography, Motor Cortex
- Abstract
Decisions under uncertainty are often biased by the history of preceding sensory input, behavioral choices, or received outcomes. Behavioral studies of perceptual decisions suggest that such history-dependent biases affect the accumulation of evidence and can be adapted to the correlation structure of the sensory environment. Here, we systematically varied this correlation structure while human participants performed a canonical perceptual choice task. We tracked the trial-by-trial variations of history biases via behavioral modeling and of a neural signature of decision formation via magnetoencephalography (MEG). The history bias was flexibly adapted to the environment and exerted a selective effect on the build-up (not baseline level) of action-selective motor cortical activity during decision formation. This effect added to the impact of the current stimulus. We conclude that the build-up of action plans in human motor cortical circuits is shaped by dynamic prior expectations that result from an adaptive interaction with the environment., Competing Interests: AB, TD No competing interests declared, (© 2023, Braun and Donner.)
- Published
- 2023
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9. Brainstem fMRI signaling of surprise across different types of deviant stimuli.
- Author
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Mazancieux A, Mauconduit F, Amadon A, Willem de Gee J, Donner TH, and Meyniel F
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- Humans, Locus Coeruleus diagnostic imaging, Arousal, Pupil physiology, Magnetic Resonance Imaging methods, Brain Stem
- Abstract
Detection of deviant stimuli is crucial to orient and adapt our behavior. Previous work shows that deviant stimuli elicit phasic activation of the locus coeruleus (LC), which releases noradrenaline and controls central arousal. However, it is unclear whether the detection of behaviorally relevant deviant stimuli selectively triggers LC responses or other neuromodulatory systems (dopamine, serotonin, and acetylcholine). We combine human functional MRI (fMRI) recordings optimized for brainstem imaging with pupillometry to perform a mapping of deviant-related responses in subcortical structures. Participants have to detect deviant items in a "local-global" paradigm that distinguishes between deviance based on the stimulus probability and the sequence structure. fMRI responses to deviant stimuli are distributed in many cortical areas. Both types of deviance elicit responses in the pupil, LC, and other neuromodulatory systems. Our results reveal that the detection of task-relevant deviant items recruits the same multiple subcortical systems across computationally different types of deviance., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.)
- Published
- 2023
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10. An information-theoretic quantification of the content of communication between brain regions.
- Author
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Celotto M, Bím J, Tlaie A, De Feo V, Lemke S, Chicharro D, Nili H, Bieler M, Hanganu-Opatz IL, Donner TH, Brovelli A, and Panzeri S
- Abstract
Quantifying the amount, content and direction of communication between brain regions is key to understanding brain function. Traditional methods to analyze brain activity based on the Wiener-Granger causality principle quantify the overall information propagated by neural activity between simultaneously recorded brain regions, but do not reveal the information flow about specific features of interest (such as sensory stimuli). Here, we develop a new information theoretic measure termed Feature-specific Information Transfer (FIT), quantifying how much information about a specific feature flows between two regions. FIT merges the Wiener-Granger causality principle with information-content specificity. We first derive FIT and prove analytically its key properties. We then illustrate and test them with simulations of neural activity, demonstrating that FIT identifies, within the total information flowing between regions, the information that is transmitted about specific features. We then analyze three neural datasets obtained with different recording methods, magneto- and electro-encephalography, and spiking activity, to demonstrate the ability of FIT to uncover the content and direction of information flow between brain regions beyond what can be discerned with traditional anaytical methods. FIT can improve our understanding of how brain regions communicate by uncovering previously hidden feature-specific information flow.
- Published
- 2023
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11. Flexible sensory-motor mapping rules manifest in correlated variability of stimulus and action codes across the brain.
- Author
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van den Brink RL, Hagena K, Wilming N, Murphy PR, Büchel C, and Donner TH
- Subjects
- Humans, Cues, Judgment, Magnetic Resonance Imaging, Brain Mapping, Brain diagnostic imaging
- Abstract
Humans and non-human primates can flexibly switch between different arbitrary mappings from sensation to action to solve a cognitive task. It has remained unknown how the brain implements such flexible sensory-motor mapping rules. Here, we uncovered a dynamic reconfiguration of task-specific correlated variability between sensory and motor brain regions. Human participants switched between two rules for reporting visual orientation judgments during fMRI recordings. Rule switches were either signaled explicitly or inferred by the participants from ambiguous cues. We used behavioral modeling to reconstruct the time course of their belief about the active rule. In both contexts, the patterns of correlations between ongoing fluctuations in stimulus- and action-selective activity across visual- and action-related brain regions tracked participants' belief about the active rule. The rule-specific correlation patterns broke down around the time of behavioral errors. We conclude that internal beliefs about task state are instantiated in brain-wide, selective patterns of correlated variability., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.)
- Published
- 2023
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12. Persistent activity in human parietal cortex mediates perceptual choice repetition bias.
- Author
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Urai AE and Donner TH
- Subjects
- Animals, Choice Behavior, Humans, Magnetoencephalography, Parietal Lobe, Decision Making, Motor Cortex
- Abstract
Humans and other animals tend to repeat or alternate their previous choices, even when judging sensory stimuli presented in a random sequence. It is unclear if and how sensory, associative, and motor cortical circuits produce these idiosyncratic behavioral biases. Here, we combined behavioral modeling of a visual perceptual decision with magnetoencephalographic (MEG) analyses of neural dynamics, across multiple regions of the human cerebral cortex. We identified distinct history-dependent neural signals in motor and posterior parietal cortex. Gamma-band activity in parietal cortex tracked previous choices in a sustained fashion, and biased evidence accumulation toward choice repetition; sustained beta-band activity in motor cortex inversely reflected the previous motor action, and biased the accumulation starting point toward alternation. The parietal, not motor, signal mediated the impact of previous on current choice and reflected individual differences in choice repetition. In sum, parietal cortical signals seem to play a key role in shaping choice sequences., (© 2022. The Author(s).)
- Published
- 2022
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13. Time estimation and arousal responses in dopa-responsive dystonia.
- Author
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Becker LF, Tunc S, Murphy P, Bäumer T, Weissbach A, Pauly MG, Al-Shorafat DM, Saranza G, Lang AE, Beste C, Donner TH, Verrel J, and Münchau A
- Subjects
- Arousal, Case-Control Studies, GTP Cyclohydrolase genetics, Humans, Dystonic Disorders, Levodopa therapeutic use
- Abstract
Dopa-responsive dystonia (DRD) is caused by an impaired dopamine biosynthesis due to a GTP-cyclohydrolase-1 (GCH1) deficiency, resulting in a combination of dystonia and parkinsonism. However, the effect of GCH1 mutations and levodopa treatment on motor control beyond simple movements, such as timing, action preparation and feedback processing, have not been investigated so far. In an active time estimation task with trial-by-trial feedback, participants indicated a target interval (1200 ms) by a motor response. We compared 12 patients tested (in fixed order) under their current levodopa medication ("ON") and after levodopa withdrawal ("OFF") to matched healthy controls (HC), measured twice to control for repetition effects. We assessed time estimation accuracy, trial-to-trial adjustment, as well as task- and feedback-related pupil-linked arousal responses. Patients showed comparable time estimation accuracy ON medication as HC but reduced performance OFF medication. Task-related pupil responses showed the reverse pattern. Trial-to-trial adjustments of response times were reduced in DRD, particularly OFF medication. Our results indicate differential alterations of time estimation accuracy and task-related arousal dynamics in DRD patients as a function of dopaminergic medication state. A medication-independent alteration of task repetition effects in DRD cannot be ruled out with certainty but is discussed as less likely., (© 2022. The Author(s).)
- Published
- 2022
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14. Functional magnetic resonance imaging responses during perceptual decision-making at 3 and 7 T in human cortex, striatum, and brainstem.
- Author
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Colizoli O, de Gee JW, van der Zwaag W, and Donner TH
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- Adult, Female, Humans, Male, Young Adult, Brain Stem diagnostic imaging, Brain Stem physiology, Corpus Striatum diagnostic imaging, Corpus Striatum physiology, Decision Making physiology, Functional Neuroimaging, Magnetic Resonance Imaging, Motion Perception physiology, Reward, Visual Cortex diagnostic imaging, Visual Cortex physiology
- Abstract
While functional magnetic resonance imaging (fMRI) at ultra-high field (7 T) promises a general increase in sensitivity compared to lower field strengths, the benefits may be most pronounced for specific applications. The current study aimed to evaluate the relative benefit of 7 over 3 T fMRI for the assessment of responses evoked in different brain regions by a well-controlled cognitive task. At 3 and 7 T, the same participants made challenging perceptual decisions about visual motion combined with monetary rewards for correct choices. Previous work on this task has extensively characterized the underlying cognitive computations and single-cell responses in cortical and subcortical structures. We quantified the evoked fMRI responses in extrastriate visual cortical areas, the striatum, and the brainstem during the decision interval and the post-feedback interval of the task. The dependence of response amplitudes on field strength during the decision interval differed between cortical, striatal, and brainstem regions, with a generally bigger 7 versus 3 T benefit in subcortical structures. We also found stronger responses during relatively easier than harder decisions at 7 T for dopaminergic midbrain nuclei, in line with reward expectation. Our results demonstrate the potential of 7 T fMRI for illuminating the contribution of small brainstem nuclei to the orchestration of cognitive computations in the human brain., (© 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.)
- Published
- 2022
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15. Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing.
- Author
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Pfeffer T, Keitel C, Kluger DS, Keitel A, Russmann A, Thut G, Donner TH, and Gross J
- Subjects
- Adult, Brain diagnostic imaging, Cognition, Female, Humans, Male, Arousal physiology, Brain physiology, Cerebral Cortex diagnostic imaging, Cerebral Cortex physiology, Magnetoencephalography methods, Neurons physiology, Pupil physiology
- Abstract
Fluctuations in arousal, controlled by subcortical neuromodulatory systems, continuously shape cortical state, with profound consequences for information processing. Yet, how arousal signals influence cortical population activity in detail has so far only been characterized for a few selected brain regions. Traditional accounts conceptualize arousal as a homogeneous modulator of neural population activity across the cerebral cortex. Recent insights, however, point to a higher specificity of arousal effects on different components of neural activity and across cortical regions. Here, we provide a comprehensive account of the relationships between fluctuations in arousal and neuronal population activity across the human brain. Exploiting the established link between pupil size and central arousal systems, we performed concurrent magnetoencephalographic (MEG) and pupillographic recordings in a large number of participants, pooled across three laboratories. We found a cascade of effects relative to the peak timing of spontaneous pupil dilations: Decreases in low-frequency (2-8 Hz) activity in temporal and lateral frontal cortex, followed by increased high-frequency (>64 Hz) activity in mid-frontal regions, followed by monotonic and inverted U relationships with intermediate frequency-range activity (8-32 Hz) in occipito-parietal regions. Pupil-linked arousal also coincided with widespread changes in the structure of the aperiodic component of cortical population activity, indicative of changes in the excitation-inhibition balance in underlying microcircuits. Our results provide a novel basis for studying the arousal modulation of cognitive computations in cortical circuits., Competing Interests: TP, CK, DK, AK, AR, GT, JG No competing interests declared, TD Reviewing editor, eLife, (© 2022, Pfeffer et al.)
- Published
- 2022
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16. Circuit mechanisms for the chemical modulation of cortex-wide network interactions and behavioral variability.
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Pfeffer T, Ponce-Alvarez A, Tsetsos K, Meindertsma T, Gahnström CJ, van den Brink RL, Nolte G, Engel AK, Deco G, and Donner TH
- Abstract
Influential theories postulate distinct roles of catecholamines and acetylcholine in cognition and behavior. However, previous physiological work reported similar effects of these neuromodulators on the response properties (specifically, the gain) of individual cortical neurons. Here, we show a double dissociation between the effects of catecholamines and acetylcholine at the level of large-scale interactions between cortical areas in humans. A pharmacological boost of catecholamine levels increased cortex-wide interactions during a visual task, but not rest. An acetylcholine boost decreased interactions during rest, but not task. Cortical circuit modeling explained this dissociation by differential changes in two circuit properties: the local excitation-inhibition balance (more strongly increased by catecholamines) and intracortical transmission (more strongly reduced by acetylcholine). The inferred catecholaminergic mechanism also predicted noisier decision-making, which we confirmed for both perceptual and value-based choice behavior. Our work highlights specific circuit mechanisms for shaping cortical network interactions and behavioral variability by key neuromodulatory systems., (Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).)
- Published
- 2021
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17. Adaptive circuit dynamics across human cortex during evidence accumulation in changing environments.
- Author
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Murphy PR, Wilming N, Hernandez-Bocanegra DC, Prat-Ortega G, and Donner TH
- Subjects
- Adult, Female, Humans, Magnetoencephalography, Male, Models, Neurological, Cerebral Cortex physiology, Decision Making physiology
- Abstract
Many decisions under uncertainty entail the temporal accumulation of evidence that informs about the state of the environment. When environments are subject to hidden changes in their state, maximizing accuracy and reward requires non-linear accumulation of evidence. How this adaptive, non-linear computation is realized in the brain is unknown. We analyzed human behavior and cortical population activity (measured with magnetoencephalography) recorded during visual evidence accumulation in a changing environment. Behavior and decision-related activity in cortical regions involved in action planning exhibited hallmarks of adaptive evidence accumulation, which could also be implemented by a recurrent cortical microcircuit. Decision dynamics in action-encoding parietal and frontal regions were mirrored in a frequency-specific modulation of the state of the visual cortex that depended on pupil-linked arousal and the expected probability of change. These findings link normative decision computations to recurrent cortical circuit dynamics and highlight the adaptive nature of decision-related feedback to the sensory cortex.
- Published
- 2021
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18. Pupil Dilation and the Slow Wave ERP Reflect Surprise about Choice Outcome Resulting from Intrinsic Variability in Decision Confidence.
- Author
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de Gee JW, Correa CMC, Weaver M, Donner TH, and van Gaal S
- Subjects
- Adolescent, Electroencephalography, Female, Humans, Learning, Male, Pupil physiology, Uncertainty, Young Adult, Arousal physiology, Brain physiology, Decision Making physiology, Evoked Potentials physiology, Formative Feedback, Reflex, Pupillary physiology
- Abstract
Central to human and animal cognition is the ability to learn from feedback in order to optimize future rewards. Such a learning signal might be encoded and broadcasted by the brain's arousal systems, including the noradrenergic locus coeruleus. Pupil responses and the positive slow wave component of event-related potentials reflect rapid changes in the arousal level of the brain. Here, we ask whether and how these variables may reflect surprise: the mismatch between one's expectation about being correct and the outcome of a decision, when expectations fluctuate due to internal factors (e.g., engagement). We show that during an elementary decision task in the face of uncertainty both physiological markers of phasic arousal reflect surprise. We further show that pupil responses and slow wave event-related potential are unrelated to each other and that prediction error computations depend on feedback awareness. These results further advance our understanding of the role of central arousal systems in decision-making under uncertainty., (© The Author(s) 2021. Published by Oxford University Press.)
- Published
- 2021
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19. Choices change the temporal weighting of decision evidence.
- Author
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Talluri BC, Urai AE, Bronfman ZZ, Brezis N, Tsetsos K, Usher M, and Donner TH
- Subjects
- Adult, Humans, Pupil physiology, Young Adult, Decision Making physiology, Judgment physiology, Mathematical Concepts, Motion Perception physiology, Psychomotor Performance physiology, Psychophysics, Space Perception physiology
- Abstract
Many decisions result from the accumulation of decision-relevant information (evidence) over time. Even when maximizing decision accuracy requires weighting all the evidence equally, decision-makers often give stronger weight to evidence occurring early or late in the evidence stream. Here, we show changes in such temporal biases within participants as a function of intermittent judgments about parts of the evidence stream. Human participants performed a decision task that required a continuous estimation of the mean evidence at the end of the stream. The evidence was either perceptual (noisy random dot motion) or symbolic (variable sequences of numbers). Participants also reported a categorical judgment of the preceding evidence half-way through the stream in one condition or executed an evidence-independent motor response in another condition. The relative impact of early versus late evidence on the final estimation flipped between these two conditions. In particular, participants' sensitivity to late evidence after the intermittent judgment, but not the simple motor response, was decreased. Both the intermittent response as well as the final estimation reports were accompanied by nonluminance-mediated increases of pupil diameter. These pupil dilations were bigger during intermittent judgments than simple motor responses and bigger during estimation when the late evidence was consistent than inconsistent with the initial judgment. In sum, decisions activate pupil-linked arousal systems and alter the temporal weighting of decision evidence. Our results are consistent with the idea that categorical choices in the face of uncertainty induce a change in the state of the neural circuits underlying decision-making. NEW & NOTEWORTHY The psychology and neuroscience of decision-making have extensively studied the accumulation of decision-relevant information toward a categorical choice. Much fewer studies have assessed the impact of a choice on the processing of subsequent information. Here, we show that intermittent choices during a protracted stream of input reduce the sensitivity to subsequent decision information and transiently boost arousal. Choices might trigger a state change in the neural machinery for decision-making.
- Published
- 2021
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20. Decision making: How the past guides the future in frontal cortex.
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Talluri BC, Braun A, and Donner TH
- Subjects
- Frontal Lobe, Judgment, Uncertainty, Decision Making, Heuristics
- Abstract
Our judgments of our environment are often shaped by heuristics and prior experience. New research shows that the resulting biases are encoded, and combined with new sensory input, by groups of neurons in the frontal cortex during decisions under uncertainty., (Copyright © 2021 Elsevier Inc. All rights reserved.)
- Published
- 2021
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21. Dynamic expressions of confidence within an evidence accumulation framework.
- Author
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Desender K, Donner TH, and Verguts T
- Subjects
- Humans, Judgment, Probability, Choice Behavior, Decision Making
- Abstract
Human observers can reliably report their confidence in the choices they make. An influential framework conceptualizes decision confidence as the probability of a decision being correct, given the choice made and the evidence on which it was based. This framework accounts for three diagnostic signatures of human confidence reports, including an opposite dependence of confidence on evidence strength for correct and error trials. However, the framework does not account for the temporal evolution of these signatures, because it only describes the transformation of a static representation of evidence into choice and the associated confidence. Here, we combine this framework with another influential framework: dynamic accumulation of evidence over time, and build on the notion that confidence reflects the probability of being correct, given the choice and accumulated evidence up until that point. Critically, we show that such a dynamic model predicts that the diagnostic signatures of confidence depend on time; most critically, it predicts a stronger opposite dependence of confidence on evidence strength and choice correctness as a function of time. We tested, and confirmed, these predictions in human behaviour during random dot motion discrimination, in which confidence judgments were queried at different points in time. We conclude that human confidence reports reflect the dynamics of the probability of being correct given the accumulated evidence and choice., (Copyright © 2020 Elsevier B.V. All rights reserved.)
- Published
- 2021
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22. Large-scale dynamics of perceptual decision information across human cortex.
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Wilming N, Murphy PR, Meyniel F, and Donner TH
- Subjects
- Choice Behavior, Female, Humans, Male, Nontherapeutic Human Experimentation, Signal Processing, Computer-Assisted, Visual Cortex physiology, Cerebral Cortex physiology, Decision Making, Magnetoencephalography methods, Visual Perception physiology
- Abstract
Perceptual decisions entail the accumulation of sensory evidence for a particular choice towards an action plan. An influential framework holds that sensory cortical areas encode the instantaneous sensory evidence and downstream, action-related regions accumulate this evidence. The large-scale distribution of this computation across the cerebral cortex has remained largely elusive. Here, we develop a regionally-specific magnetoencephalography decoding approach to exhaustively map the dynamics of stimulus- and choice-specific signals across the human cortical surface during a visual decision. Comparison with the evidence accumulation dynamics inferred from behavior disentangles stimulus-dependent and endogenous components of choice-predictive activity across the visual cortical hierarchy. We find such an endogenous component in early visual cortex (including V1), which is expressed in a low (<20 Hz) frequency band and tracks, with delay, the build-up of choice-predictive activity in (pre-) motor regions. Our results are consistent with choice- and frequency-specific cortical feedback signaling during decision formation.
- Published
- 2020
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23. Pupil-linked phasic arousal predicts a reduction of choice bias across species and decision domains.
- Author
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de Gee JW, Tsetsos K, Schwabe L, Urai AE, McCormick D, McGinley MJ, and Donner TH
- Subjects
- Adult, Animals, Female, Humans, Male, Mice, Species Specificity, Young Adult, Arousal physiology, Choice Behavior physiology, Pupil physiology
- Abstract
Decisions are often made by accumulating ambiguous evidence over time. The brain's arousal systems are activated during such decisions. In previous work in humans, we found that evoked responses of arousal systems during decisions are reported by rapid dilations of the pupil and track a suppression of biases in the accumulation of decision-relevant evidence (de Gee et al., 2017). Here, we show that this arousal-related suppression in decision bias acts on both conservative and liberal biases, and generalizes from humans to mice, and from perceptual to memory-based decisions. In challenging sound-detection tasks, the impact of spontaneous or experimentally induced choice biases was reduced under high phasic arousal. Similar bias suppression occurred when evidence was drawn from memory. All of these behavioral effects were explained by reduced evidence accumulation biases. Our results point to a general principle of interplay between phasic arousal and decision-making., Competing Interests: Jd, KT, LS, AU, DM, MM No competing interests declared, TD Reviewing editor, eLife, (© 2020, de Gee et al.)
- Published
- 2020
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24. Reinforcement biases subsequent perceptual decisions when confidence is low, a widespread behavioral phenomenon.
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Lak A, Hueske E, Hirokawa J, Masset P, Ott T, Urai AE, Donner TH, Carandini M, Tonegawa S, Uchida N, and Kepecs A
- Subjects
- Animals, Choice Behavior, Hearing, Humans, Mice, Rats, Smell, Vision, Ocular, Bias, Decision Making physiology, Reinforcement, Psychology
- Abstract
Learning from successes and failures often improves the quality of subsequent decisions. Past outcomes, however, should not influence purely perceptual decisions after task acquisition is complete since these are designed so that only sensory evidence determines the correct choice. Yet, numerous studies report that outcomes can bias perceptual decisions, causing spurious changes in choice behavior without improving accuracy. Here we show that the effects of reward on perceptual decisions are principled: past rewards bias future choices specifically when previous choice was difficult and hence decision confidence was low. We identified this phenomenon in six datasets from four laboratories, across mice, rats, and humans, and sensory modalities from olfaction and audition to vision. We show that this choice-updating strategy can be explained by reinforcement learning models incorporating statistical decision confidence into their teaching signals. Thus, reinforcement learning mechanisms are continually engaged to produce systematic adjustments of choices even in well-learned perceptual decisions in order to optimize behavior in an uncertain world., Competing Interests: AL, EH, JH, PM, TO, AU, MC, ST, AK No competing interests declared, TD, NU Reviewing editor, eLife, (© 2020, Lak et al.)
- Published
- 2020
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25. Post-training Load-Related Changes of Auditory Working Memory - An EEG Study.
- Author
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Gudi-Mindermann H, Rimmele JM, Bruns P, Kloosterman NA, Donner TH, Engel AK, and Röder B
- Abstract
Working memory (WM) refers to the temporary retention and manipulation of information, and its capacity is highly susceptible to training. Yet, the neural mechanisms that allow for increased performance under demanding conditions are not fully understood. We expected that post-training efficiency in WM performance modulates neural processing during high load tasks. We tested this hypothesis, using electroencephalography (EEG) ( N = 39), by comparing source space spectral power of healthy adults performing low and high load auditory WM tasks. Prior to the assessment, participants either underwent a modality-specific auditory WM training, or a modality-irrelevant tactile WM training, or were not trained (active control). After a modality-specific training participants showed higher behavioral performance, compared to the control. EEG data analysis revealed general effects of WM load, across all training groups, in the theta-, alpha-, and beta-frequency bands. With increased load theta-band power increased over frontal, and decreased over parietal areas. Centro-parietal alpha-band power and central beta-band power decreased with load. Interestingly, in the high load condition a tendency toward reduced beta-band power in the right medial temporal lobe was observed in the modality-specific WM training group compared to the modality-irrelevant and active control groups. Our finding that WM processing during the high load condition changed after modality-specific WM training, showing reduced beta-band activity in voice-selective regions, possibly indicates a more efficient maintenance of task-relevant stimuli. The general load effects suggest that WM performance at high load demands involves complementary mechanisms, combining a strengthening of task-relevant and a suppression of task-irrelevant processing., (Copyright © 2020 Gudi-Mindermann, Rimmele, Bruns, Kloosterman, Donner, Engel and Röder.)
- Published
- 2020
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26. Author Correction: Thalamus exhibits less sensory variability quenching than cortex.
- Author
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Poland E, Donner TH, Müller KM, Leopold DA, and Wilke M
- Abstract
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
- Published
- 2020
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27. The Relationship between Trial-by-Trial Variability and Oscillations of Cortical Population Activity.
- Author
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Daniel E, Meindertsma T, Arazi A, Donner TH, and Dinstein I
- Subjects
- Adult, Electroencephalography methods, Female, Head physiology, Humans, Male, Middle Aged, Motion, Photic Stimulation, Single-Case Studies as Topic statistics & numerical data, Young Adult, Biological Clocks physiology, Biological Variation, Individual, Cerebral Cortex physiology, Magnetoencephalography methods, Magnetoencephalography standards, Magnetoencephalography statistics & numerical data, Visual Perception physiology
- Abstract
Neural activity fluctuates over time, creating considerable variability across trials. This trial-by-trial neural variability is dramatically reduced ("quenched") after the presentation of sensory stimuli. Likewise, the power of neural oscillations, primarily in the alpha-beta band, is also reduced after stimulus onset. Despite their similarity, these phenomena have so far been studied and discussed independently. We hypothesized that the two phenomena are tightly coupled in electrophysiological recordings of large cortical neural populations. To test this, we examined magnetoencephalography (MEG) recordings of healthy subjects viewing repeated presentations of a visual stimulus. The timing, amplitude, and spatial topography of variability-quenching and power-suppression were remarkably similar. Neural variability quenching was eliminated by excluding the alpha-beta band from the recordings, but not by excluding other frequency-bands. Moreover, individual magnitudes of alpha-beta band-power explained 86% of between-subject differences in variability quenching. An alternative mechanism that may generate variability quenching is increased phase alignment across trials. However, changes in inter-trial-phase-coherence (ITPC) exhibited distinct timing and no correlations with the magnitude of variability quenching in individual participants. These results reveal that neural variability quenching is tightly coupled with stimulus-induced changes in the power of alpha-beta band oscillations, associating two phenomena that have so far been studied in isolation.
- Published
- 2019
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28. Brainstem Modulation of Large-Scale Intrinsic Cortical Activity Correlations.
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van den Brink RL, Pfeffer T, and Donner TH
- Abstract
Brain activity fluctuates continuously, even in the absence of changes in sensory input or motor output. These intrinsic activity fluctuations are correlated across brain regions and are spatially organized in macroscale networks. Variations in the strength, topography, and topology of correlated activity occur over time, and unfold upon a backbone of long-range anatomical connections. Subcortical neuromodulatory systems send widespread ascending projections to the cortex, and are thus ideally situated to shape the temporal and spatial structure of intrinsic correlations. These systems are also the targets of the pharmacological treatment of major neurological and psychiatric disorders, such as Parkinson's disease, depression, and schizophrenia. Here, we review recent work that has investigated how neuromodulatory systems shape correlations of intrinsic fluctuations of large-scale cortical activity. We discuss studies in the human, monkey, and rodent brain, with a focus on non-invasive recordings of human brain activity. We provide a structured but selective overview of this work and distil a number of emerging principles. Future efforts to chart the effect of specific neuromodulators and, in particular, specific receptors, on intrinsic correlations may help identify shared or antagonistic principles between different neuromodulatory systems. Such principles can inform models of healthy brain function and may provide an important reference for understanding altered cortical dynamics that are evident in neurological and psychiatric disorders, potentially paving the way for mechanistically inspired biomarkers and individualized treatments of these disorders., (Copyright © 2019 van den Brink, Pfeffer and Donner.)
- Published
- 2019
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29. Confidence predicts speed-accuracy tradeoff for subsequent decisions.
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Desender K, Boldt A, Verguts T, and Donner TH
- Subjects
- Adolescent, Adult, Female, Humans, Male, Models, Neurological, Young Adult, Behavior, Decision Making, Self Concept, Time
- Abstract
When external feedback about decision outcomes is lacking, agents need to adapt their decision policies based on an internal estimate of the correctness of their choices (i.e., decision confidence). We hypothesized that agents use confidence to continuously update the tradeoff between the speed and accuracy of their decisions: When confidence is low in one decision, the agent needs more evidence before committing to a choice in the next decision, leading to slower but more accurate decisions. We tested this hypothesis by fitting a bounded accumulation decision model to behavioral data from three different perceptual choice tasks. Decision bounds indeed depended on the reported confidence on the previous trial, independent of objective accuracy. This increase in decision bound was predicted by a centro-parietal EEG component sensitive to confidence. We conclude that internally computed neural signals of confidence predict the ongoing adjustment of decision policies., Competing Interests: KD, AB, TV No competing interests declared, TD Reviewing editor, eLife, (© 2019, Desender et al.)
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- 2019
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30. Choice history biases subsequent evidence accumulation.
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Urai AE, de Gee JW, Tsetsos K, and Donner TH
- Subjects
- Adolescent, Adult, Behavior, Computer Simulation, Decision Making, Female, Humans, Male, Models, Theoretical, Task Performance and Analysis, Young Adult, Bias, Choice Behavior
- Abstract
Perceptual choices depend not only on the current sensory input but also on the behavioral context, such as the history of one's own choices. Yet, it remains unknown how such history signals shape the dynamics of later decision formation. In models of decision formation, it is commonly assumed that choice history shifts the starting point of accumulation toward the bound reflecting the previous choice. We here present results that challenge this idea. We fit bounded-accumulation decision models to human perceptual choice data, and estimated bias parameters that depended on observers' previous choices. Across multiple task protocols and sensory modalities, individual history biases in overt behavior were consistently explained by a history-dependent change in the evidence accumulation, rather than in its starting point. Choice history signals thus seem to bias the interpretation of current sensory input, akin to shifting endogenous attention toward (or away from) the previously selected interpretation., Competing Interests: AU, Jd, KT, TD No competing interests declared, (© 2019, Urai et al.)
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- 2019
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31. Thalamus exhibits less sensory variability quenching than cortex.
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Poland E, Donner TH, Müller KM, Leopold DA, and Wilke M
- Subjects
- Animals, Macaca mulatta, Photic Stimulation, Visual Pathways physiology, Thalamus physiology, Visual Cortex physiology, Visual Perception
- Abstract
Spiking activity exhibits a large degree of variability across identical trials, which has been shown to be significantly reduced by stimulus onset in a wide range of cortical areas. Whether similar dynamics apply to the thalamus and in particular to the pulvinar is largely unknown. Here, we examined electrophysiological recordings from two adult rhesus macaques performing a perceptual task and comparatively investigated trial-to-trial variability in higher-order thalamus (ventral and dorsal pulvinar), the lateral geniculate nucleus (LGN) and visual cortex (area V4) prior to and following the presentation of a visual stimulus. We found spiking variability during stable fixation prior to stimulus onset to be considerably lower in both pulvinar and the LGN as compared to area V4. In contrast to the prominent variability reduction in V4 upon stimulus onset, variability in the thalamic nuclei was largely unaffected by visual stimulation. There was a small but significant variability decrease in the dorsal pulvinar, but not in the ventral portion of the pulvinar, which is closely connected to visual cortices and would thus have been expected to reflect cortical response properties. This dissociation did not stem from differences in response strength or mean firing rates and indicates fundamental differences in variability quenching between thalamus and cortex.
- Published
- 2019
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32. Author Correction: Task-evoked pupil responses reflect internal belief states.
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Colizoli O, de Gee JW, Urai AE, and Donner TH
- Abstract
A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.
- Published
- 2018
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33. Confirmation Bias through Selective Overweighting of Choice-Consistent Evidence.
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Talluri BC, Urai AE, Tsetsos K, Usher M, and Donner TH
- Subjects
- Adolescent, Adult, Attention physiology, Bias, Brain physiology, Computer Simulation, Female, Humans, Male, Psychometrics methods, Psychophysics, Visual Perception physiology, Young Adult, Choice Behavior physiology, Decision Making physiology, Motion Perception physiology
- Abstract
People's assessments of the state of the world often deviate systematically from the information available to them [1]. Such biases can originate from people's own decisions: committing to a categorical proposition, or a course of action, biases subsequent judgment and decision-making. This phenomenon, called confirmation bias [2], has been explained as suppression of post-decisional dissonance [3, 4]. Here, we provide insights into the underlying mechanism. It is commonly held that decisions result from the accumulation of samples of evidence informing about the state of the world [5-8]. We hypothesized that choices bias the accumulation process by selectively altering the weighting (gain) of subsequent evidence, akin to selective attention. We developed a novel psychophysical task to test this idea. Participants viewed two successive random dot motion stimuli and made two motion-direction judgments: a categorical discrimination after the first stimulus and a continuous estimation of the overall direction across both stimuli after the second stimulus. Participants' sensitivity for the second stimulus was selectively enhanced when that stimulus was consistent with the initial choice (compared to both, first stimuli and choice-inconsistent second stimuli). A model entailing choice-dependent selective gain modulation explained this effect better than several alternative mechanisms. Choice-dependent gain modulation was also established in another task entailing averaging of numerical values instead of motion directions. We conclude that intermittent choices direct selective attention during the evaluation of subsequent evidence, possibly due to decision-related feedback in the brain [9]. Our results point to a recurrent interplay between decision-making and selective attention., (Copyright © 2018 The Authors. Published by Elsevier Ltd.. All rights reserved.)
- Published
- 2018
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34. Task-evoked pupil responses reflect internal belief states.
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Colizoli O, de Gee JW, Urai AE, and Donner TH
- Abstract
Perceptual decisions about the state of the environment are often made in the face of uncertain evidence. Internal uncertainty signals are considered important regulators of learning and decision-making. A growing body of work has implicated the brain's arousal systems in uncertainty signaling. Here, we found that two specific computational variables, postulated by recent theoretical work, evoke boosts of arousal at different times during a perceptual decision: decision confidence (the observer's internally estimated probability that a choice was correct given the evidence) before feedback, and prediction errors (deviations from expected reward) after feedback. We monitored pupil diameter, a peripheral marker of central arousal state, while subjects performed a challenging perceptual choice task with a delayed monetary reward. We quantified evoked pupil responses during decision formation and after reward-linked feedback. During both intervals, decision difficulty and accuracy had interacting effects on pupil responses. Pupil responses negatively scaled with decision confidence prior to feedback and scaled with uncertainty-dependent prediction errors after feedback. This pattern of pupil responses during both intervals was in line with a model using the observer's graded belief about choice accuracy to anticipate rewards and compute prediction errors. We conclude that pupil-linked arousal systems are modulated by internal belief states.
- Published
- 2018
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35. Surprise About Sensory Event Timing Drives Cortical Transients in the Beta Frequency Band.
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Meindertsma T, Kloosterman NA, Engel AK, Wagenmakers EJ, and Donner TH
- Subjects
- Adult, Bayes Theorem, Cerebral Cortex physiology, Female, Humans, Magnetoencephalography, Male, Middle Aged, Visual Perception physiology, Young Adult, Anticipation, Psychological physiology, Beta Rhythm physiology, Models, Neurological, Models, Psychological, Time Perception physiology
- Abstract
Learning the statistical structure of the environment is crucial for adaptive behavior. Humans and nonhuman decision-makers seem to track such structure through a process of probabilistic inference, which enables predictions about behaviorally relevant events. Deviations from such predictions cause surprise, which in turn helps improve inference. Surprise about the timing of behaviorally relevant sensory events drives phasic responses of neuromodulatory brainstem systems, which project to the cerebral cortex. Here, we developed a computational model-based magnetoencephalography (MEG) approach for mapping the resulting cortical transients across space, time, and frequency, in the human brain ( N = 28, 17 female). We used a Bayesian ideal observer model to learn the statistics of the timing of changes in a simple visual detection task. This model yielded quantitative trial-by-trial estimates of temporal surprise. The model-based surprise variable predicted trial-by-trial variations in reaction time more strongly than the externally observable interval timings alone. Trial-by-trial variations in surprise were negatively correlated with the power of cortical population activity measured with MEG. This surprise-related power suppression occurred transiently around the behavioral response, specifically in the beta frequency band. It peaked in parietal and prefrontal cortices, remote from the motor cortical suppression of beta power related to overt report (button press) of change detection. Our results indicate that surprise about sensory event timing transiently suppresses ongoing beta-band oscillations in association cortex. This transient suppression of frontal beta-band oscillations might reflect an active reset triggered by surprise, and is in line with the idea that beta-oscillations help maintain cognitive sets. SIGNIFICANCE STATEMENT The brain continuously tracks the statistical structure of the environment to anticipate behaviorally relevant events. Deviations from such predictions cause surprise, which in turn drives neural activity in subcortical brain regions that project to the cerebral cortex. We used magnetoencephalography in humans to map out surprise-related modulations of cortical population activity across space, time, and frequency. Surprise was elicited by variable timing of visual stimulus changes requiring a behavioral response. Surprise was quantified by means of an ideal observer model. Surprise predicted behavior as well as a transient suppression of beta frequency-band oscillations in frontal cortical regions. Our results are in line with conceptual accounts that have linked neural oscillations in the beta-band to the maintenance of cognitive sets., (Copyright © 2018 the authors 0270-6474/18/387600-11$15.00/0.)
- Published
- 2018
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36. Amplification and Suppression of Distinct Brainwide Activity Patterns by Catecholamines.
- Author
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van den Brink RL, Nieuwenhuis S, and Donner TH
- Subjects
- Adrenergic Uptake Inhibitors pharmacology, Atomoxetine Hydrochloride pharmacology, Brain Chemistry, Cross-Over Studies, Datasets as Topic, Double-Blind Method, Female, Functional Neuroimaging, Humans, Magnetic Resonance Imaging, Male, Nerve Tissue Proteins analysis, Nerve Tissue Proteins genetics, Receptors, Catecholamine analysis, Receptors, Catecholamine genetics, Rest, Brain physiology, Catecholamines physiology, Connectome
- Abstract
The widely projecting catecholaminergic (norepinephrine and dopamine) neurotransmitter systems profoundly shape the state of neuronal networks in the forebrain. Current models posit that the effects of catecholaminergic modulation on network dynamics are homogeneous across the brain. However, the brain is equipped with a variety of catecholamine receptors with distinct functional effects and heterogeneous density across brain regions. Consequently, catecholaminergic effects on brainwide network dynamics might be more spatially specific than assumed. We tested this idea through the analysis of fMRI measurements performed in humans (19 females, 5 males) at "rest" under pharmacological (atomoxetine-induced) elevation of catecholamine levels. We used a linear decomposition technique to identify spatial patterns of correlated fMRI signal fluctuations that were either increased or decreased by atomoxetine. This yielded two distinct spatial patterns, each expressing reliable and specific drug effects. The spatial structure of both fluctuation patterns resembled the spatial distribution of the expression of catecholamine receptor genes: α
1 norepinephrine receptors (for the fluctuation pattern: placebo > atomoxetine), D2 -like dopamine receptors (pattern: atomoxetine > placebo), and β norepinephrine receptors (for both patterns, with correlations of opposite sign). We conclude that catecholaminergic effects on the forebrain are spatially more structured than traditionally assumed and at least in part explained by the heterogeneous distribution of various catecholamine receptors. Our findings link catecholaminergic effects on large-scale brain networks to low-level characteristics of the underlying neurotransmitter systems. They also provide key constraints for the development of realistic models of neuromodulatory effects on large-scale brain network dynamics. SIGNIFICANCE STATEMENT The catecholamines norepinephrine and dopamine are an important class of modulatory neurotransmitters. Because of the widespread and diffuse release of these neuromodulators, it has commonly been assumed that their effects on neural interactions are homogeneous across the brain. Here, we present results from the human brain that challenge this view. We pharmacologically increased catecholamine levels and imaged the effects on the spontaneous covariations between brainwide fMRI signals at "rest." We identified two distinct spatial patterns of covariations: one that was amplified and another that was suppressed by catecholamines. Each pattern was associated with the heterogeneous spatial distribution of the expression of distinct catecholamine receptor genes. Our results provide novel insights into the catecholaminergic modulation of large-scale human brain dynamics., (Copyright © 2018 van den Brink et al.)- Published
- 2018
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37. Reading memory formation from the eyes.
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Bergt A, Urai AE, Donner TH, and Schwabe L
- Subjects
- Adolescent, Adult, Female, Humans, Male, Young Adult, Arousal physiology, Emotions physiology, Memory, Long-Term physiology, Memory, Short-Term physiology, Mental Recall physiology, Pattern Recognition, Visual physiology, Pupil physiology, Speech Perception physiology
- Abstract
At any time, we are processing thousands of stimuli, but only few of them will be remembered hours or days later. Is there any way to predict which ones? Here, we tested whether the pupil response to ongoing stimuli, an indicator of physiological arousal known to be relevant for memory formation, is a reliable predictor of long-term memory for these stimuli, over at least 1 day. Pupil dilation was tracked while participants performed visual and auditory encoding tasks. Memory was tested immediately after encoding and 24 hr later. Irrespective of the encoding modality, trial-by-trial variations in pupil dilation predicted reliably which stimuli were recalled in the immediate and 24 hr-delayed tests, in particular for emotionally arousing stimuli. These results show that our eyes may provide a window into the formation of long-term memories. Furthermore, our findings underline the important role of central arousal systems in the rapid formation of memories in the brain, possibly by gating synaptic plasticity mechanisms in the neocortex., (© 2018 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)
- Published
- 2018
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38. Adaptive History Biases Result from Confidence-Weighted Accumulation of past Choices.
- Author
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Braun A, Urai AE, and Donner TH
- Subjects
- Adult, Discrimination, Psychological physiology, Environment, Feedback, Psychological, Female, Humans, Male, Motion Perception physiology, Observation, Psychomotor Performance physiology, Reaction Time physiology, Uncertainty, Young Adult, Adaptation, Psychological physiology, Choice Behavior physiology, Decision Making physiology
- Abstract
Perceptual decision-making is biased by previous events, including the history of preceding choices: observers tend to repeat (or alternate) their judgments of the sensory environment more often than expected by chance. Computational models postulate that these so-called choice history biases result from the accumulation of internal decision signals across trials. Here, we provide psychophysical evidence for such a mechanism and its adaptive utility. Male and female human observers performed different variants of a challenging visual motion discrimination task near psychophysical threshold. In a first experiment, we decoupled categorical perceptual choices and motor responses on a trial-by-trial basis. Choice history bias was explained by previous perceptual choices, not motor responses, highlighting the importance of internal decision signals in action-independent formats. In a second experiment, observers performed the task in stimulus environments containing different levels of autocorrelation and providing no external feedback about choice correctness. Despite performing under overall high levels of uncertainty, observers adjusted both the strength and the sign of their choice history biases to these environments. When stimulus sequences were dominated by either repetitions or alternations, the individual degree of this adjustment of history bias was about as good a predictor of individual performance as individual perceptual sensitivity. The history bias adjustment scaled with two proxies for observers' confidence about their previous choices (accuracy and reaction time). Together, our results are consistent with the idea that action-independent, confidence-modulated decision variables are accumulated across choices in a flexible manner that depends on decision-makers' model of their environment. SIGNIFICANCE STATEMENT Decisions based on sensory input are often influenced by the history of one's preceding choices, manifesting as a bias to systematically repeat (or alternate) choices. We here provide support for the idea that such choice history biases arise from the context-dependent accumulation of a quantity referred to as the decision variable: the variable's sign dictates the choice and its magnitude the confidence about choice correctness. We show that choices are accumulated in an action-independent format and a context-dependent manner, weighted by the confidence about their correctness. This confidence-weighted accumulation of choices enables decision-makers to flexibly adjust their behavior to different sensory environments. The bias adjustment can be as important for optimizing performance as one's sensitivity to the momentary sensory input., (Copyright © 2018 Braun et al.)
- Published
- 2018
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39. Catecholamines alter the intrinsic variability of cortical population activity and perception.
- Author
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Pfeffer T, Avramiea AE, Nolte G, Engel AK, Linkenkaer-Hansen K, and Donner TH
- Subjects
- Adrenergic Uptake Inhibitors pharmacology, Atomoxetine Hydrochloride pharmacology, Brain Mapping, Cerebral Cortex drug effects, Humans, Magnetoencephalography methods, Models, Neurological, Photic Stimulation, Placebos, Psychophysics, Catecholamines physiology, Cerebral Cortex physiology, Visual Perception physiology
- Abstract
The ascending modulatory systems of the brain stem are powerful regulators of global brain state. Disturbances of these systems are implicated in several major neuropsychiatric disorders. Yet, how these systems interact with specific neural computations in the cerebral cortex to shape perception, cognition, and behavior remains poorly understood. Here, we probed into the effect of two such systems, the catecholaminergic (dopaminergic and noradrenergic) and cholinergic systems, on an important aspect of cortical computation: its intrinsic variability. To this end, we combined placebo-controlled pharmacological intervention in humans, recordings of cortical population activity using magnetoencephalography (MEG), and psychophysical measurements of the perception of ambiguous visual input. A low-dose catecholaminergic, but not cholinergic, manipulation altered the rate of spontaneous perceptual fluctuations as well as the temporal structure of "scale-free" population activity of large swaths of the visual and parietal cortices. Computational analyses indicate that both effects were consistent with an increase in excitatory relative to inhibitory activity in the cortical areas underlying visual perceptual inference. We propose that catecholamines regulate the variability of perception and cognition through dynamically changing the cortical excitation-inhibition ratio. The combined readout of fluctuations in perception and cortical activity we established here may prove useful as an efficient and easily accessible marker of altered cortical computation in neuropsychiatric disorders.
- Published
- 2018
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40. Multiple Transient Signals in Human Visual Cortex Associated with an Elementary Decision.
- Author
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Meindertsma T, Kloosterman NA, Nolte G, Engel AK, and Donner TH
- Subjects
- Adult, Eye Movements physiology, Female, Fixation, Ocular physiology, Humans, Male, Middle Aged, Arousal physiology, Beta Rhythm physiology, Decision Making physiology, Nerve Net physiology, Visual Cortex physiology, Visual Perception physiology
- Abstract
The cerebral cortex continuously undergoes changes in its state, which are manifested in transient modulations of the cortical power spectrum. Cortical state changes also occur at full wakefulness and during rapid cognitive acts, such as perceptual decisions. Previous studies found a global modulation of beta-band (12-30 Hz) activity in human and monkey visual cortex during an elementary visual decision: reporting the appearance or disappearance of salient visual targets surrounded by a distractor. The previous studies disentangled neither the motor action associated with behavioral report nor other secondary processes, such as arousal, from perceptual decision processing per se. Here, we used magnetoencephalography in humans to pinpoint the factors underlying the beta-band modulation. We found that disappearances of a salient target were associated with beta-band suppression, and target reappearances with beta-band enhancement. This was true for both overt behavioral reports (immediate button presses) and silent counting of the perceptual events. This finding indicates that the beta-band modulation was unrelated to the execution of the motor act associated with a behavioral report of the perceptual decision. Further, changes in pupil-linked arousal, fixational eye movements, or gamma-band responses were not necessary for the beta-band modulation. Together, our results suggest that the beta-band modulation was a top-down signal associated with the process of converting graded perceptual signals into a categorical format underlying flexible behavior. This signal may have been fed back from brain regions involved in decision processing to visual cortex, thus enforcing a "decision-consistent" cortical state. SIGNIFICANCE STATEMENT Elementary visual decisions are associated with a rapid state change in visual cortex, indexed by a modulation of neural activity in the beta-frequency range. Such decisions are also followed by other events that might affect the state of visual cortex, including the motor command associated with the report of the decision, an increase in pupil-linked arousal, fixational eye movements, and fluctuations in bottom-up sensory processing. Here, we ruled out the necessity of these events for the beta-band modulation of visual cortex. We propose that the modulation reflects a decision-related state change, which is induced by the conversion of graded perceptual signals into a categorical format underlying behavior. The resulting decision signal may be fed back to visual cortex., (Copyright © 2017 Meindertsma et al.)
- Published
- 2017
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41. Dynamic modulation of decision biases by brainstem arousal systems.
- Author
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de Gee JW, Colizoli O, Kloosterman NA, Knapen T, Nieuwenhuis S, and Donner TH
- Subjects
- Adult, Brain Stem diagnostic imaging, Female, Healthy Volunteers, Humans, Magnetic Resonance Imaging, Male, Models, Neurological, Young Adult, Arousal, Brain Stem physiology, Decision Making
- Abstract
Decision-makers often arrive at different choices when faced with repeated presentations of the same evidence. Variability of behavior is commonly attributed to noise in the brain's decision-making machinery. We hypothesized that phasic responses of brainstem arousal systems are a significant source of this variability. We tracked pupil responses (a proxy of phasic arousal) during sensory-motor decisions in humans, across different sensory modalities and task protocols. Large pupil responses generally predicted a reduction in decision bias. Using fMRI, we showed that the pupil-linked bias reduction was (i) accompanied by a modulation of choice-encoding pattern signals in parietal and prefrontal cortex and (ii) predicted by phasic, pupil-linked responses of a number of neuromodulatory brainstem centers involved in the control of cortical arousal state, including the noradrenergic locus coeruleus. We conclude that phasic arousal suppresses decision bias on a trial-by-trial basis, thus accounting for a significant component of the variability of choice behavior.
- Published
- 2017
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42. Pupil-linked arousal is driven by decision uncertainty and alters serial choice bias.
- Author
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Urai AE, Braun A, and Donner TH
- Subjects
- Adult, Feedback, Physiological physiology, Female, Healthy Volunteers, Humans, Male, Models, Biological, Psychomotor Performance physiology, Reaction Time, Young Adult, Arousal physiology, Choice Behavior physiology, Pupil physiology, Uncertainty
- Abstract
While judging their sensory environments, decision-makers seem to use the uncertainty about their choices to guide adjustments of their subsequent behaviour. One possible source of these behavioural adjustments is arousal: decision uncertainty might drive the brain's arousal systems, which control global brain state and might thereby shape subsequent decision-making. Here, we measure pupil diameter, a proxy for central arousal state, in human observers performing a perceptual choice task of varying difficulty. Pupil dilation, after choice but before external feedback, reflects three hallmark signatures of decision uncertainty derived from a computational model. This increase in pupil-linked arousal boosts observers' tendency to alternate their choice on the subsequent trial. We conclude that decision uncertainty drives rapid changes in pupil-linked arousal state, which shape the serial correlation structure of ongoing choice behaviour.
- Published
- 2017
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43. Catecholaminergic Neuromodulation Shapes Intrinsic MRI Functional Connectivity in the Human Brain.
- Author
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van den Brink RL, Pfeffer T, Warren CM, Murphy PR, Tona KD, van der Wee NJ, Giltay E, van Noorden MS, Rombouts SA, Donner TH, and Nieuwenhuis S
- Subjects
- Adult, Double-Blind Method, Humans, Magnetic Resonance Imaging methods, Male, Neural Pathways physiology, Placebo Effect, Rest physiology, Young Adult, Adrenergic Neurons physiology, Catecholamines metabolism, Cerebral Cortex physiology, Connectome methods, Dopaminergic Neurons physiology, Nerve Net physiology
- Abstract
Unlabelled: The brain commonly exhibits spontaneous (i.e., in the absence of a task) fluctuations in neural activity that are correlated across brain regions. It has been established that the spatial structure, or topography, of these intrinsic correlations is in part determined by the fixed anatomical connectivity between regions. However, it remains unclear which factors dynamically sculpt this topography as a function of brain state. Potential candidate factors are subcortical catecholaminergic neuromodulatory systems, such as the locus ceruleus-norepinephrine system, which send diffuse projections to most parts of the forebrain. Here, we systematically characterized the effects of endogenous central neuromodulation on correlated fluctuations during rest in the human brain. Using a double-blind placebo-controlled crossover design, we pharmacologically increased synaptic catecholamine levels by administering atomoxetine, an NE transporter blocker, and examined the effects on the strength and spatial structure of resting-state MRI functional connectivity. First, atomoxetine reduced the strength of inter-regional correlations across three levels of spatial organization, indicating that catecholamines reduce the strength of functional interactions during rest. Second, this modulatory effect on intrinsic correlations exhibited a substantial degree of spatial specificity: the decrease in functional connectivity showed an anterior-posterior gradient in the cortex, depended on the strength of baseline functional connectivity, and was strongest for connections between regions belonging to distinct resting-state networks. Thus, catecholamines reduce intrinsic correlations in a spatially heterogeneous fashion. We conclude that neuromodulation is an important factor shaping the topography of intrinsic functional connectivity., Significance Statement: The human brain shows spontaneous activity that is strongly correlated across brain regions. The factors that dynamically sculpt these inter-regional correlation patterns are poorly understood. Here, we test the hypothesis that they are shaped by the catecholaminergic neuromodulators norepinephrine and dopamine. We pharmacologically increased synaptic catecholamine levels and measured the resulting changes in intrinsic fMRI functional connectivity. At odds with common understanding of catecholamine function, we found (1) overall reduced inter-regional correlations across several levels of spatial organization; and (2) a remarkable spatial specificity of this modulatory effect. Our results identify norepinephrine and dopamine as important factors shaping intrinsic functional connectivity and advance our understanding of catecholamine function in the central nervous system., (Copyright © 2016 the authors 0270-6474/16/367866-12$15.00/0.)
- Published
- 2016
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44. The Relationship between Perceptual Decision Variables and Confidence in the Human Brain.
- Author
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Hebart MN, Schriever Y, Donner TH, and Haynes JD
- Subjects
- Adolescent, Adult, Brain Mapping, Cerebral Cortex physiology, Female, Humans, Male, Prefrontal Cortex physiology, Young Adult, Choice Behavior physiology, Decision Making physiology, Emotions physiology, Motion Perception physiology, Perception physiology, Visual Perception physiology
- Abstract
Perceptual confidence refers to the degree to which we believe in the accuracy of our percepts. Signal detection theory suggests that perceptual confidence is computed from an internal "decision variable," which reflects the amount of available information in favor of one or another perceptual interpretation of the sensory input. The neural processes underlying these computations have, however, remained elusive. Here, we used fMRI and multivariate decoding techniques to identify regions of the human brain that encode this decision variable and confidence during a visual motion discrimination task. We used observers' binary perceptual choices and confidence ratings to reconstruct the internal decision variable that governed the subjects' behavior. A number of areas in prefrontal and posterior parietal association cortex encoded this decision variable, and activity in the ventral striatum reflected the degree of perceptual confidence. Using a multivariate connectivity analysis, we demonstrate that patterns of brain activity in the right ventrolateral prefrontal cortex reflecting the decision variable were linked to brain signals in the ventral striatum reflecting confidence. Our results suggest that the representation of perceptual confidence in the ventral striatum is derived from a transformation of the continuous decision variable encoded in the cerebral cortex., (© The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.)
- Published
- 2016
- Full Text
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45. Correction: Action Planning and the Timescale of Evidence Accumulation.
- Author
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Tsetsos K, Pfeffer T, Jentgens P, and Donner TH
- Published
- 2015
- Full Text
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46. Perceptual choice boosts network stability: effect of neuromodulation?
- Author
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Warren CM, Nieuwenhuis S, and Donner TH
- Subjects
- Female, Humans, Male, Cerebral Cortex physiopathology, Consciousness physiology, Sensation physiology
- Abstract
A recent paper demonstrates that conscious perceptual decisions are characterized by a hallmark of attractor states in recurrent cortical networks: increased stability of cortex-wide activity patterns. We propose that this global cortical state change may be caused by a transient gain modulation through ascending brainstem systems., (Copyright © 2015 Elsevier Ltd. All rights reserved.)
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- 2015
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47. Action Planning and the Timescale of Evidence Accumulation.
- Author
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Tsetsos K, Pfeffer T, Jentgens P, and Donner TH
- Subjects
- Adult, Brain physiology, Brain Mapping, Female, Humans, Male, Decision Making, Psychomotor Performance
- Abstract
Perceptual decisions are based on the temporal integration of sensory evidence for different states of the outside world. The timescale of this integration process varies widely across behavioral contexts and individuals, and it is diagnostic for the underlying neural mechanisms. In many situations, the decision-maker knows the required mapping between perceptual evidence and motor response (henceforth termed "sensory-motor contingency") before decision formation. Here, the integrated evidence can be directly translated into a motor plan and, indeed, neural signatures of the integration process are evident as build-up activity in premotor brain regions. In other situations, however, the sensory-motor contingencies are unknown at the time of decision formation. We used behavioral psychophysics and computational modeling to test if knowledge about sensory-motor contingencies affects the timescale of perceptual evidence integration. We asked human observers to perform the same motion discrimination task, with or without trial-to-trial variations of the mapping between perceptual choice and motor response. When the mapping varied, it was either instructed before or after the stimulus presentation. We quantified the timescale of evidence integration under these different sensory-motor mapping conditions by means of two approaches. First, we analyzed subjects' discrimination threshold as a function of stimulus duration. Second, we fitted a dynamical decision-making model to subjects' choice behavior. The results from both approaches indicated that observers (i) integrated motion information for several hundred ms, (ii) used a shorter than optimal integration timescale, and (iii) used the same integration timescale under all sensory-motor mappings. We conclude that the mechanisms limiting the timescale of perceptual decisions are largely independent from long-term learning (under fixed mapping) or rapid acquisition (under variable mapping) of sensory-motor contingencies. This conclusion has implications for neurophysiological and neuroimaging studies of perceptual decision-making.
- Published
- 2015
- Full Text
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48. Pupil size tracks perceptual content and surprise.
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Kloosterman NA, Meindertsma T, van Loon AM, Lamme VA, Bonneh YS, and Donner TH
- Subjects
- Adult, Female, Humans, Male, Middle Aged, Young Adult, Motion Perception physiology, Pupil physiology, Visual Perception physiology
- Abstract
Changes in pupil size at constant light levels reflect the activity of neuromodulatory brainstem centers that control global brain state. These endogenously driven pupil dynamics can be synchronized with cognitive acts. For example, the pupil dilates during the spontaneous switches of perception of a constant sensory input in bistable perceptual illusions. It is unknown whether this pupil dilation only indicates the occurrence of perceptual switches, or also their content. Here, we measured pupil diameter in human subjects reporting the subjective disappearance and re-appearance of a physically constant visual target surrounded by a moving pattern ('motion-induced blindness' illusion). We show that the pupil dilates during the perceptual switches in the illusion and a stimulus-evoked 'replay' of that illusion. Critically, the switch-related pupil dilation encodes perceptual content, with larger amplitude for disappearance than re-appearance. This difference in pupil response amplitude enables prediction of the type of report (disappearance vs. re-appearance) on individual switches (receiver-operating characteristic: 61%). The amplitude difference is independent of the relative durations of target-visible and target-invisible intervals and subjects' overt behavioral report of the perceptual switches. Further, we show that pupil dilation during the replay also scales with the level of surprise about the timing of switches, but there is no evidence for an interaction between the effects of surprise and perceptual content on the pupil response. Taken together, our results suggest that pupil-linked brain systems track both the content of, and surprise about, perceptual events., (© 2015 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.)
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- 2015
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49. Top-down modulation in human visual cortex predicts the stability of a perceptual illusion.
- Author
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Kloosterman NA, Meindertsma T, Hillebrand A, van Dijk BW, Lamme VA, and Donner TH
- Subjects
- Adult, Beta Rhythm, Female, Humans, Male, Optical Illusions, Visual Cortex physiology
- Abstract
Conscious perception sometimes fluctuates strongly, even when the sensory input is constant. For example, in motion-induced blindness (MIB), a salient visual target surrounded by a moving pattern suddenly disappears from perception, only to reappear after some variable time. Whereas such changes of perception result from fluctuations of neural activity, mounting evidence suggests that the perceptual changes, in turn, may also cause modulations of activity in several brain areas, including visual cortex. In this study, we asked whether these latter modulations might affect the subsequent dynamics of perception. We used magnetoencephalography (MEG) to measure modulations in cortical population activity during MIB. We observed a transient, retinotopically widespread modulation of beta (12-30 Hz)-frequency power over visual cortex that was closely linked to the time of subjects' behavioral report of the target disappearance. This beta modulation was a top-down signal, decoupled from both the physical stimulus properties and the motor response but contingent on the behavioral relevance of the perceptual change. Critically, the modulation amplitude predicted the duration of the subsequent target disappearance. We propose that the transformation of the perceptual change into a report triggers a top-down mechanism that stabilizes the newly selected perceptual interpretation., (Copyright © 2015 the American Physiological Society.)
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- 2015
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50. Motion-induced blindness and Troxler fading: common and different mechanisms.
- Author
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Bonneh YS, Donner TH, Cooperman A, Heeger DJ, and Sagi D
- Subjects
- Adult, Female, Humans, Male, Middle Aged, Photic Stimulation, Reaction Time, Perceptual Masking physiology
- Abstract
Extended stabilization of gaze leads to disappearance of dim visual targets presented peripherally. This phenomenon, known as Troxler fading, is thought to result from neuronal adaptation. Intense targets also disappear intermittently when surrounded by a moving pattern (the "mask"), a phenomenon known as motion-induced blindness (MIB). The similar phenomenology and dynamics of these disappearances may suggest that also MIB is, likewise, solely due to adaptation, which may be amplified by the presence of the mask. Here we directly compared the dependence of both phenomena on target contrast. Observers reported the disappearance and reappearance of a target of varying intensity (contrast levels: 8%-80%). MIB was induced by adding a mask that moved at one of various different speeds. The results revealed a lawful effect of contrast in both MIB and Troxler fading, but with opposite trends. Increasing target contrast increased (doubled) the rate of disappearance events for MIB, but decreased the disappearance rate to half in Troxler fading. The target mean invisible period decreased equally strongly with target contrast in MIB and in Troxler fading. The results suggest that both MIB and Troxler are equally affected by contrast adaptation, but that the rate of MIB is governed by an additional mechanism, possibly involving antagonistic processes between neuronal populations processing target and mask. Our results link MIB to other bi-stable visual phenomena that involve neuronal competition (such as binocular rivalry), which exhibit an analogous dependency on the strength of the competing stimulus components.
- Published
- 2014
- Full Text
- View/download PDF
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