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Decisions about where to move the eyes depend on neurons in frontal eye field (FEF). Movement neurons in FEF accumulate salience evidence derived from FEF visual neurons to select the location of a saccade target among distractors. How visual neurons achieve this salience representation is unknown. We present a neuro-computational model of target selection called salience by competitive and recurrent interactions (SCRI), based on the competitive interaction model of attentional selection and decision-making (SmithSewell, 2013). SCRI selects targets by synthesizing localization and identification information to yield a dynamically evolving representation of salience across the visual field. SCRI accounts for neural spiking of individual FEF visual neurons, explaining idiosyncratic differences in neural dynamics with specific parameters. Many visual neurons resolve the competition between search items through feedforward inhibition between signals representing different search items, some also require lateral inhibition, and many act as recurrent gates to modulate the incoming flow of information about stimulus identity. SCRI was tested further by using simulated spiking representations of visual salience as input to the gated accumulator model of FEF movement neurons (Purcell et al., 2010, 2012). Predicted saccade response times fit those observed for search arrays of different set sizes and different target-distractor similarities, and accumulator trajectories replicated movement neuron discharge rates. These findings offer new insights into visual decision-making through converging neuro-computational constraints and provide a novel computational account of the diversity of FEF visual neurons. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Neuronal spiking was sampled from the frontal eye field (FEF) and from the rostral part of area 6 that reaches to the superior limb of the arcuate sulcus, dorsal to the arcuate spur when present (F2vr) in macaque monkeys performing memory-guided saccades and visually guided saccades for visual search. Neuronal spiking modulation in F2vr resembled that in FEF in many but not all respects. A new consensus clustering algorithm of neuronal modulation patterns revealed that F2vr and FEF contain a greater variety of modulation patterns than previously reported. The areas differ in the proportions of visuomotor neuron types, the proportions of neurons discriminating a target from distractors during visual search, and the consistency of modulation patterns across tasks. However, between F2vr and FEF we found no difference in the magnitude of delay period activity, the timing of the peak discharge rate relative to saccades, or the time of search target selection. The observed similarities and differences between the 2 cortical regions contribute to other work establishing the organization of eye fields in the frontal lobe and may help explain why FEF in monkeys is identified within granular prefrontal area 8 but in humans is identified within agranular premotor area 6.

International audience; The article ‘In vitro neurons learn and exhibit sentience when embodied in a simulated game-world’ by Kagan et al. triggered a wave of positive mainstream and scientific media coverage as well as a widespread negative reaction from the scientific community. Here, we discuss why this negative reaction is legitimate and must be taken seriously. We raise concerns about the key claim of the article: that it demonstrates that “a single layer of in vitro cortical neurons can self-organize activity to display intelligent and sentient behavior when embodied in a simulated game-world”.

EEG β-bursts observed over the medial frontal cortex are claimed to mediate response inhibition despite their infrequent occurrence. The weak association with stopping behavior is supposed to be a by-product of the low signal-to-noise ratio of EEG recordings. We tested the premise that β-bursts are more common within the cerebral cortex and more directly associated with response inhibition. We sampled simultaneously EEG and intracortical local field potentials (LFP) within the medial frontal cortex (MFC) of two macaque monkeys performing a response inhibition task. Intracortical β-bursts were just as infrequent as those in EEG and did not parallel the likelihood of canceling a planned response. Cortical β-bursts were more prevalent in upper layers but were not synchronized across a cortical column or with EEG β-bursts. These findings contradict claims for a causal contribution of β-bursts during response inhibition, provide important constraints for biophysical and cortical circuit models, and invite further considerations of β-burst function in cognitive control.

Salient objects stand out (pop-out) from their surroundings, grabbing our attention. Whether this phenomenon is a consequence of bottom-up sensory processing or predicated on top-down influence is debated. We show that the neural computation of attentional pop-out is embedded in the earliest cortical sensory response, seemingly void of feedback from higher-level areas. We measured synaptic and spiking activity across cortical columns in mid-level area V4 of monkeys searching for an attention-grabbing stimulus. Indexed by reaction times and behavioral accuracy, attention was captured at variable times. This moment of attentional capture occurred within the earliest feedforward response, both in terms of timing and spatial location. Moreover, the magnitude of the earliest sensory response predicted reaction times. Crucially, errant attentional selection and consequent behavior was associated with errant selection in sensory cortex. Together, these findings demonstrate a dominant role for feedforward activation of sensory cortex for dictating attentional priority and subsequent behavior.In briefWhy do certain objects stand out from their surroundings and seemingly grab our attention? In this study, Westerberg et al. determine that attentional selection for salient objects in our environment is computed in sensory cortex as soon as sensory information arrives.HighlightsEarly sensory responses in V4 predict attentional selection and behavioral responsesErrant attentional selection in sensory cortex precedes errant behaviorTonic modulation of sensory cortex can regulate attentional selection

Express saccades are rapid saccadic eye movements that can accurately redirect gaze to behaviorally relevant stimuli in the visual environment. This behavior can be commonly observed when the fixation spot disappears at a consistent, short interval before a target spot appears at a repeated location. While seemingly automatic, whether cognitive control can govern express saccade production has not been investigated. Here we report the production and manipulation of express saccades under unfavorable conditions in a saccade countermanding task necessitating cognitive control. To perform this task, we trained two monkeys to fixate a central spot and, following a variable amount of time, saccade to a target stimulus at one of two fixed locations (no-stop trials) presented simultaneously with the disappearance of the fixation dot. On a minority of trials, the fixation point reappeared instructing the monkeys to cancel their planned saccade to the peripheral target (stop-signal trials). Monkeys earned fluid reward for generating saccades to targets on no-stop trials and for maintaining fixation on stop-signal trials. Monkeys and humans adapt to the stop-signal trials by increasing saccade latencies. However, in two macaque monkeys we observed a significant fraction of trials with saccade latencies < 100 ms, resulting in a bimodal distribution of saccadic latencies. Target timing derived from regularities of the fixation interval (foreperiod) was used by some monkeys in some sessions to adapt regular but not express saccade latencies. Furthermore, simulations revealed by varying express saccade production, monkeys could maximize the opportunity for reward. To determine whether monkeys exploited this opportunity, reward contingencies for express saccade were changed. When unrewarded, significantly fewer express saccades were produced. This was confirmed in two other monkeys. This study highlights an unexpected manifestation of cognitive control through release of very short latency responses.

Cognitive operations are widely studied by measuring electric fields through EEG and ECoG. However, despite their widespread use, the component neural circuitry giving rise to these signals remains unknown. Specifically, the functional architecture of cortical columns which results in attention-associated electric fields has not been explored. Here we detail the laminar cortical circuitry underlying an attention-associated electric field often measured over posterior regions of the brain in humans and monkeys. First, we identified visual cortical area V4 as one plausible contributor to this attention-associated electric field through inverse modeling of cranial EEG in macaque monkeys performing a visual attention task. Next, we performed laminar neurophysiological recordings on the prelunate gyrus and identified the electric-field-producing dipoles as synaptic activity in distinct cortical layers of area V4. Specifically, activation in the extragranular layers of cortex resulted in the generation of the attention-associated dipole. Feature selectivity of a given cortical column determined the overall contribution to this electric field. Columns selective for the attended feature contributed more to the electric field than columns selective for a different feature. Lastly, the laminar profile of synaptic activity generated by V4 was sufficient to produce an attention-associated signal measurable outside of the column. These findings suggest that the top-down recipient cortical layers produce an attention-associated electric field capable of being measured extracranially and the relative contribution of each column depends upon the underlying functional architecture.

Visual search is a workhorse for investigating how attention interacts with processing of sensory information. Attentional selection has been linked to altered cortical sensory responses and feature preferences (i.e., tuning). However, attentional modulation of feature selectivity during search is largely unexplored. Here we map the spatiotemporal profile of feature selectivity during singleton search. Monkeys performed a search where a pop-out feature determined the target of attention. We recorded laminar neural responses from visual area V4. We first identified "feature columns" which showed preference for individual colors. In the unattended condition, feature columns were significantly more selective in superficial relative to middle and deep layers. Attending a stimulus increased selectivity in all layers but not equally. Feature selectivity increased most in the deep layers, leading to higher selectivity in extragranular layers as compared to the middle layer. This attention-induced enhancement was rhythmically gated in phase with the beta-band local field potential. Beta power dominated both extragranular laminar compartments, but current source density analysis pointed to an origin in superficial layers, specifically. While beta-band power was present regardless of attentional state, feature selectivity was only gated by beta in the attended condition. Neither the beta oscillation nor its gating of feature selectivity varied with microsaccade production. Importantly, beta modulation of neural activity predicted response times, suggesting a direct link between attentional gating and behavioral output. Together, these findings suggest beta-range synaptic activation in V4's superficial layers rhythmically gates attentional enhancement of feature tuning in a way that affects the speed of attentional selection.

Medial frontal cortex enables executive control by monitoring relevant information and using it to adapt behavior. In macaques performing a saccade countermanding (stop-signal) task, we recorded EEG over and neural spiking across all layers of the supplementary eye field (SEF). We report the laminar organization of concurrently activated neurons monitoring the conflict between incompatible responses and the timing of events serving goal maintenance and executive control. We also show their relation to coincident event-related potentials (ERP). Neurons signaling response conflict were largely broad-spiking found across all layers. Neurons signaling the interval until specific task events were largely broad-spiking neurons concentrated in L3 and L5. Neurons predicting the duration of control and sustaining the task goal until the release of operant control were a mix of narrow- and broad-spiking neurons confined to L2/3. We complement these results with the first report of a monkey homologue of the N2/P3 ERP complex associated with response inhibition. N2 polarization varied with error likelihood and P3 polarization varied with the duration of expected control. The amplitude of the N2 and P3 were predicted by the spike rate of different classes of neurons located in L2/3 but not L5/6. These findings reveal important, new features of the cortical microcircuitry supporting executive control and producing associated ERP.

Evidence accumulation is a computational framework that accounts for behavior as well as the dynamics of individual neurons involved in decision making. Linking these two levels of description reveals a scaling paradox: How do choices and response times (RT) explained by models assuming single accumulators arise from a large ensemble of idiosyncratic accumulator neurons? We created a simulation model that makes decisions by aggregating across ensembles of accumulators, thereby instantiating the essential structure of neural ensembles that make decisions. Across different levels of simulated choice difficulty and speed-accuracy emphasis, choice proportions and RT distributions simulated by the ensembles are invariant to ensemble size and the accumulated evidence at RT is invariant across RT when the accumulators are at least moderately correlated in either baseline evidence or rates of accumulation and when RT is not governed by the most extreme accumulators. To explore the relationship between the low-level ensemble accumulators and high-level cognitive models, we fit simulated ensemble behavior with a standard LBA model. The standard LBA model generally recovered the core accumulator parameters (particularly drift rates and residual time) of individual ensemble accumulators with high accuracy, with variability parameters of the standard LBA modulating as a function of various ensemble parameters. Ensembles of accumulators also provide an alternative conception of speed-accuracy tradeoff without relying on varying thresholds of individual accumulators, instead by adjusting how ensembles of accumulators are aggregated or by how accumulators are correlated within ensembles. These results clarify relationships between neural and computational accounts of decision making.

We discuss the problem of elucidating mechanisms of visual search. We begin by considering the history, logic, and methods of relating behavioral or cognitive processes with neural processes. We then survey briefly the cognitive neurophysiology of visual search and essential aspects of the neural circuitry supporting this capacity. We introduce conceptually and empirically a powerful but underutilized experimental approach to dissect the cognitive processes supporting performance of a visual search task with factorial manipulations of singleton-distractor identifiability and stimulus-response cue discriminability. We show that systems factorial technology can distinguish processing architectures from the performance of macaque monkeys. This demonstration offers new opportunities to distinguish neural mechanisms through selective manipulation of visual encoding, search selection, rule encoding, and stimulus-response mapping.

Selective attention affords scrutinizing items in our environment. However, attentional selection changes over time and across space. Empirically, repetition of visual search conditions changes attentional processing. Priming of pop-out is a vivid example. Repeatedly searching for the same pop-out search feature is accomplished with faster response times and fewer errors. We will review the psychophysical background of priming of pop-out, focusing on the hypothesis that it arises through changes in visual selective attention. We then describe research done with macaque monkeys to understand the neural mechanisms supporting visual selective attention and priming of pop-out. Next, we will survey research on priming of pop-out using noninvasive brain measures with humans. We will conclude by hypothesizing three alternative neural mechanisms and highlighting open questions.

The neural mechanisms of executive and motor control concern both basic researchers and clinicians. In human studies, preparation and cancellation of movements are accompanied by changes in the β-frequency band (15–29 Hz) of electroencephalogram (EEG). Previous studies with human participants performing stop signal (countermanding) tasks have described reduced frequency of transient β-bursts over sensorimotor cortical areas before movement initiation and increased β-bursting over medial frontal areas with movement cancellation. This modulation has been interpreted as contributing to the trial-by-trial control of behavior. We performed identical analyses of EEG recorded over the frontal lobe of macaque monkeys (one male, one female) performing a saccade countermanding task. While we replicate the occurrence and modulation of β-bursts associated with initiation and cancellation of saccades, we found that β-bursts occur too infrequently to account for the observed stopping behavior. We also found β-bursts were more common after errors, but their incidence was unrelated to response time (RT) adaptation. These results demonstrate the homology of this EEG signature between humans and macaques but raise questions about the current interpretation of β band functional significance.SIGNIFICANCE STATEMENTThe finding of increased β-bursting over medial frontal cortex with movement cancellation in humans is difficult to reconcile with the finding of modulation too late to contribute to movement cancellation in medial frontal cortex of macaque monkeys. To obtain comparable measurement scales, we recorded electroencephalogram (EEG) over medial frontal cortex of macaques performing a stop signal (countermanding) task. We replicated the occurrence and modulation of β-bursts associated with the cancellation of movements, but we found that β-bursts occur too infrequently to account for observed stopping behavior. Unfortunately, this finding raises doubts whether β-bursts can be a causal mechanism of response inhibition, which impacts future applications in devices such as brain-machine interfaces.

The goal of this short review is to call attention to a yawning gap of knowledge that separates two processes essential for saccade production. On the one hand, knowledge about the saccade generation circuitry within the brainstem is detailed and precise - push-pull interactions between gaze-shifting and gaze-holding processes control the time of saccade initiation, which begins when omnipause neurons are inhibited and brainstem burst neurons are excited. On the other hand, knowledge about the cortical and subcortical premotor circuitry accomplishing saccade initiation has crystalized around the concept of stochastic accumulation - the accumulating activity of saccade neurons reaching a fixed value triggers a saccade. Here is the gap: we do not know how the reaching of a threshold by premotor neurons causes the critical pause and burst of brainstem neurons that initiates saccades. Why this problem matters and how it can be addressed will be discussed. Closing the gap would unify two rich but curiously disconnected empirical and theoretical domains.

Balancing the speed-accuracy tradeoff (SAT) is necessary for successful behavior. Using a visual search task with interleaved cues emphasizing speed or accuracy, we recently reported diverse contributions of frontal eye field (FEF) neurons instantiating salience evidence and response preparation. Here, we report replication of visual search SAT performance in two macaque monkeys, new information about variation of saccade dynamics with SAT, extension of the neurophysiological investigation to describe processes in the superior colliculus (SC), and a description of the origin of search errors in this task. Saccade vigor varied idiosyncratically across SAT conditions and monkeys but tended to decrease with response time. As observed in the FEF, speed-accuracy tradeoff was accomplished through several distinct adjustments in the superior colliculus. In “Accurate” relative to “Fast” trials, visually responsive neurons in SC as in FEF had lower baseline firing rates and later target selection. The magnitude of these adjustments in SC was indistinguishable from that in FEF. Search errors occurred when visual salience neurons in the FEF and the SC treated distractors as targets, even in the Accurate condition. Unlike FEF, the magnitude of visual responses in the SC did not vary across SAT conditions. Also unlike FEF, the activity of SC movement neurons when saccades were initiated was equivalent in Fast and Accurate trials. Saccade-related neural activity in SC, but not FEF, varied with saccade peak velocity. These results extend our understanding of the cortical and subcortical contributions to SAT. NEW & NOTEWORTHY Neurophysiological mechanisms of speed-accuracy tradeoff (SAT) have only recently been investigated. This article reports the first replication of SAT performance in nonhuman primates, the first report of variation of saccade dynamics with SAT, the first description of superior colliculus contributions to SAT, and the first description of the origin of errors during SAT. These results inform and constrain new models of distributed decision making.

Ca2+spikes initiated in the distal trunk of layer 5 pyramidal cells (PCs) underlie nonlinear dynamic changes in the gain of cellular response, critical for top-down control of cortical processing. Detailed models with many compartments and dozens of ionic channels can account for this Ca2+spike-dependent gain and associated critical frequency. However, current models do not account for all known Ca2+-dependent features. Previous attempts to include more features have required increasing complexity, limiting their interpretability and utility for studying large population dynamics. We overcome these limitations in a minimal two-compartment biophysical model. In our model, a basal-dendrites/somatic compartment included fast-inactivating Na+and delayed-rectifier K+conductances, while an apical-dendrites/trunk compartment included persistent Na+, hyperpolarization-activated cation (Ih), slow-inactivating K+, muscarinic K+, and Ca2+L-type. The model replicated the Ca2+spike morphology and its critical frequency plus three other defining features of layer 5 PC synaptic integration: linear frequency-current relationships, back-propagation-activated Ca2+spike firing, and a shift in the critical frequency by blocking Ih. Simulating 1000 synchronized layer 5 PCs, we reproduced the current source density patterns evoked by Ca2+spikes and describe resulting medial-frontal EEG on a male macaque monkey. We reproduced changes in the current source density when Ihwas blocked. Thus, a two-compartment model with five crucial ionic currents in the apical dendrites reproduces all features of these neurons. We discuss the utility of this minimal model to study the microcircuitry of agranular areas of the frontal lobe involved in cognitive control and responsible for event-related potentials, such as the error-related negativity.SIGNIFICANCE STATEMENTA minimal model of layer 5 pyramidal cells replicates all known features crucial for distal synaptic integration in these neurons. By redistributing voltage-gated and returning transmembrane currents in the model, we establish a theoretical framework for the investigation of cortical microcircuit contribution to intracranial local field potentials and EEG. This tractable model will enable biophysical evaluation of multiscale electrophysiological signatures and computational investigation of cortical processing.

Patients with Parkinson’s disease (PD) often experience reductions in the proficiency to inhibit actions. The motor symptoms of PD can be effectively treated with deep brain stimulation (DBS) of the subthalamic nucleus (STN), a key structure in the frontal–striatal network that may be directly involved in regulating inhibitory control. However, the precise role of the STN in stopping control is unclear. The STN consists of functional subterritories linked to dissociable cortical networks, although the boundaries of the subregions are still under debate. We investigated whether stimulating the dorsal and ventral subregions of the STN would show dissociable effects on ability to stop. We studied 12 PD patients with STN DBS. Patients with two adjacent contacts positioned within the bounds of the dorsal and ventral STN completed two testing sessions (OFF medication) with low amplitude stimulation (0.4 mA) at either the dorsal or ventral contacts bilaterally, while performing the stop task. Ventral, but not dorsal, DBS improved stopping latencies. Go reactions were similar between dorsal and ventral DBS STN. Stimulation in the ventral, but not dorsal, subregion of the STN improved stopping speed, confirming the involvement of the STN in stopping control and supporting the STN functional subregions.

SummaryModels of the cerebral cortex propose a canonical columnar architecture preserved across the brain. Evidence for this model primarily stems from observations in primary sensory areas, such as the visual cortex, where neurons in an anatomical column respond preferentially to the same stimulus features. Similar columnar feature selectivity has been described for visual area V2, visual area V3 [9, 10], the middle temporal visual area (area V5), and inferotemporal cortex. The fourth visual area (V4) features color selective neurons, organized in clusters across its surface. However, whether these color-sensitive neurons are organized in a columnar fashion is debated and uncertain due to technical limitations. Here, we utilize laminar multielectrode recordings along V4 columns to resolve rival hypotheses. Linear electrode arrays were introduced orthogonally into area V4, spanning all cortical layers. Monkeys viewed color stimuli presented to the visual receptive field of the column of neurons. We found that preference for a specific color was conserved along depth but varied across columns. Interestingly, while color preference (e.g. red or green) was consistent along depth, color selectivity was significantly greater in upper layers relative to the input layer and was weakest in the lower layers. These findings demonstrate that area V4 is organized in functional columns like other visual areas.

Summary We investigated whether a task requiring concurrent perceptual decision-making and response control can be performed concurrently, whether evidence accumulation and response control are accomplished by the same neurons, and whether perceptual decision-making and countermanding can be unified computationally. Based on neural recordings in a prefrontal area of macaque monkeys, we present behavioral, neural, and computational results demonstrating that perceptual decision-making of varying difficulty can be countermanded efficiently, that single prefrontal neurons instantiate both evidence accumulation and response control, and that an interactive race between stochastic GO evidence accumulators for each alternative and a distinct STOP accumulator fits countermanding choice behavior and replicates neural trajectories. Thus, perceptual decision-making and response control, previously regarded as distinct mechanisms, are actually aspects of a common neuro-computational mechanism supporting flexible behavior., Graphical Abstract, Highlights • Monkeys can perform combined perceptual decision-making and countermanding • Prefrontal neurons accumulate evidence, but this accumulation can be interrupted • Interactive race of response accumulators and a stop accumulator explains findings • Results clarify the circuit logic of brain regions involved in decision-making, Biological Sciences; Neuroscience; Behavioral Neuroscience; Sensory Neuroscience; Cognitive Neuroscience

What are the neural correlates that distinguish goal-directed (G) from non-goal-directed movements (nG)? We investigated this question in the monkey frontal eye field, which is implicated in voluntary control of saccades. We found that only for G-saccades, the variability in spike rate across trials decreased, the regularity of spike timings within trials increased, the neural activity increased earlier from baseline and had a concurrent reduction of LFP beta band power.

SUMMARYThe balance of speed with accuracy requires error detection and performance adaptation. To date, neural concomitants of these processes have been investigated only with noninvasive measures. To provide the first neurophysiological description, macaque monkeys performed visual search under cued speed accuracy tradeoff (SAT). Monkeys changed SAT emphasis immediately after a cued switch while neuron discharges were sampled in medial frontal cortex area supplementary eye field (SEF). A multiplicity of SEF neurons signaled production of choice errors and timing errors. Modulation of SEF activity after choice errors predicted production of un-rewarded corrective saccades. Modulation of activity after timing errors signaled reward prediction error. Adaptation of performance during SAT of visual search was accomplished through pronounced changes in neural state from before search array presentation until after reward delivery. These results contextualize previous findings using noninvasive measures, complement neurophysiological findings in visuomotor structures, endorse the role of medial frontal cortex as a critic relative to the actor instantiated in visuomotor structures, and extend our understanding of the distributed neural mechanisms of SAT.HIGHLIGHTSMedial frontal cortex enables post-error adjustment during SATChoice and timing errors were signaled by partially overlapping neural poolsMedial frontal cortex can proactively modulate visuomotor processesMedial frontal cortex is to visuomotor circuits as critic to actor

Neurons in macaque frontal eye field contribute to spatial but typically not feature selection during visual search. Using an innovative visual search task, we report a serendipitous discovery that some frontal eye field neurons can develop rapid selectivity for stimulus orientation that is used to guide gaze during a visual search task with pro-saccade and anti-saccade responses. This feature selectivity occurs simultaneously at multiple locations for all objects sharing that feature and coincides with when neurons select the singleton of a search array. This feature selectivity also reveals the distinct, subsequent operation of selecting the endpoint of the saccade in pro-saccade as well as anti-saccade trials. These results demonstrate that target selection preceding saccade preparation is composed of multiple operations. We conjecture that singleton selection indexes the allocation of attention, which can be divided, to conspicuous items. Consequently, endpoint selection indexes the focused allocation of attention to the endpoint of the saccade. These results demonstrate that saccade target selection is not a unitary process.SIGNIFICANCE STATEMENTFrontal eye field is well known to contribute to spatial selection for attention and eye movements. We discovered that some frontal eye field neurons can acquire selectivity for stimulus orientation when it guides visual search. The chronometry of neurons with and without feature selectivity reveal distinct operations accomplishing visual search.

The marriage of cognitive neurophysiology and mathematical psychology to understand decision-making has been exceptionally productive. This interdisciplinary area is based on the proposition that particular neurons or circuits instantiate the accumulation of evidence specified by mathematical models of sequential sampling and stochastic accumulation. This linking proposition has earned widespread endorsement. Here, a brief survey of the history of the proposition precedes a review of multiple conundrums and paradoxes concerning the accuracy, precision, and transparency of that linking proposition. Correctly establishing how abstract models of decision-making are instantiated by particular neural circuits would represent a remarkable accomplishment in mapping mind to brain. Failing would reveal challenging limits for cognitive neuroscience. This is such a vigorous area of research because so much is at stake.

Stochastic accumulator models account for response times and errors in perceptual decision making by assuming a noisy accumulation of perceptual evidence to a threshold. Previously, we explained saccade visual search decision making by macaque monkeys with a stochastic multiaccumulator model in which accumulation was driven by a gated feed-forward integration to threshold of spike trains from visually responsive neurons in frontal eye field that signal stimulus salience. This neurally constrained model quantitatively accounted for response times and errors in visual search for a target among varying numbers of distractors and replicated the dynamics of presaccadic movement neurons hypothesized to instantiate evidence accumulation. This modeling framework suggested strategic control over gate or over threshold as two potential mechanisms to accomplish speed-accuracy tradeoff (SAT). Here, we show that our gated accumulator model framework can account for visual search performance under SAT instructions observed in a milestone neurophysiological study of frontal eye field. This framework captured key elements of saccade search performance, through observed modulations of neural input, as well as flexible combinations of gate and threshold parameters necessary to explain differences in SAT strategy across monkeys. However, the trajectories of the model accumulators deviated from the dynamics of most presaccadic movement neurons. These findings demonstrate that traditional theoretical accounts of SAT are incomplete descriptions of the underlying neural adjustments that accomplish SAT, offer a novel mechanistic account of decision-making mechanisms during speed-accuracy tradeoff, and highlight questions regarding the identity of model and neural accumulators. NEW & NOTEWORTHY A gated accumulator model is used to elucidate neurocomputational mechanisms of speed-accuracy tradeoff. Whereas canonical stochastic accumulators adjust strategy only through variation of an accumulation threshold, we demonstrate that strategic adjustments are accomplished by flexible combinations of both modulation of the evidence representation and adaptation of accumulator gate and threshold. The results indicate how model-based cognitive neuroscience can translate between abstract cognitive models of performance and neural mechanisms of speed-accuracy tradeoff.

We investigated the chronometry of neural processes in frontal eye fields of macaques performing double-step saccade visual search in which a conspicuous target changes location in the array on a random fraction of trials. Durations of computational processes producing a saccade to original and final target locations (GO1 and GO2, respectively) are derived from response times (RT) on different types of trials. In these data, GO2 tended to be faster than GO1, demonstrating that inhibition of the initial saccade did not delay production of the compensated saccade. Here, we measured the dynamics of visual, visuomovement, and movement neuron activity in relation to these processes by examining trials when neurons instantiated either process. First, we verified that saccades were initiated when the discharge rate of movement neurons reached a threshold that was invariant across RT and trial type. Second, the time when visual and visuomovement neurons selected the target and when movement neuron activity began to accumulate were not significantly different across trial type. Third, the interval from the beginning of accumulation to threshold of movement-related activity was significantly shorter when instantiating the GO2 relative to the GO1 process. Differences observed between monkeys are discussed. Fourth, random variation of RT was accounted for to some extent by random variation in both the onset and duration of selective activity of each neuron type but mostly by variation of movement neuron accumulation duration. These findings offer new insights into the sources of control of target selection and saccade production in dynamic environments.