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The vestibular system detects head motion to coordinate vital reflexes and provide our sense of balance and spatial orientation. A long-standing hypothesis has been that projections from the central vestibular system back to the vestibular sensory organs (i.e., the efferent vestibular system) mediate adaptive sensory coding during voluntary locomotion. However, direct proof for this idea has been lacking. Here we recorded from individual semicircular canal and otolith afferents during walking and running in monkeys. Using a combination of mathematical modeling and nonlinear analysis, we show that afferent encoding is actually identical across passive and active conditions, irrespective of context. Thus, taken together our results are instead consistent with the view that the vestibular periphery relays robust information to the brain during primate locomotion, suggesting that context-dependent modulation instead occurs centrally to ensure that coding is consistent with behavioral goals during locomotion., Using experimental and computational approaches the authors show that the vestibular efferent system does not modulate peripheral coding during locomotion. Instead, vestibular afferents unambiguously convey information in a context independent manner.

Object-vector (OV) cells are cells in the medial entorhinal cortex (MEC) that track an animal’s distance and direction to objects in the environment. Their firing fields are defined by vectorial relationships to free-standing 3-dimensional (3D) objects of a variety of identities and shapes. However, the natural world contains a panorama of objects, ranging from discrete 3D items to flat two-dimensional (2D) surfaces, and it remains unclear what are the most fundamental features of objects that drive vectorial responses. Here we address this question by systematically changing features of experimental objects. Using an algorithm that robustly identifies OV firing fields, we show that the cells respond to a variety of 2D surfaces, with visual contrast as the most basic visual feature to elicit neural responses. The findings suggest that OV cells use plain visual features as vectorial anchoring points, allowing vector-guided navigation to proceed in environments with few free-standing landmarks., In order to understand more about which object features are the most influential when driving vectorial responses, Andersson et al. use an algorithm to reliably examine object-vector (OV) cells in mice. Their findings suggest that OV cells use visual features as anchoring points, allowing vector-guided navigation to proceed with reference to a wide range of visual landmarks.

Many sensory-driven behaviors rely on predictions about future states of the environment. Visual input typically evolves along complex temporal trajectories that are difficult to extrapolate. We test the hypothesis that spatial processing mechanisms in the early visual system facilitate prediction by constructing neural representations that follow straighter temporal trajectories. We recorded V1 population activity in anesthetized macaques while presenting static frames taken from brief video clips, and developed a procedure to measure the curvature of the associated neural population trajectory. We found that V1 populations straighten naturally occurring image sequences, but entangle artificial sequences that contain unnatural temporal transformations. We show that these effects arise in part from computational mechanisms that underlie the stimulus selectivity of V1 cells. Together, our findings reveal that the early visual system uses a set of specialized computations to build representations that can support prediction in the natural environment., Many behaviours depend on predictions about the environment. Here the authors find neural populations in primary visual cortex to straighten the temporal trajectories of natural video clips, facilitating the extrapolation of past observations.

Visual cortical responses are known to be highly variable across trials within an experimental session. However, the long-term stability of visual cortical responses is poorly understood. Here using chronic imaging of V1 in mice we show that neural responses to repeated natural movie clips are unstable across weeks. Individual neuronal responses consist of sparse episodic activity which are stable in time but unstable in gain across weeks. Further, we find that the individual episode, instead of neuron, serves as the basic unit of the week-to-week fluctuation. To investigate how population activity encodes the stimulus, we extract a stable one-dimensional representation of the time in the natural movie, using an unsupervised method. Most week-to-week fluctuation is perpendicular to the stimulus encoding direction, thus leaving the stimulus representation largely unaffected. We propose that precise episodic activity with coordinated gain changes are keys to maintain a stable stimulus representation in V1., Here the authors show that individual neural responses in mouse V1 to a repeated natural movie clip consist of episodic activity which is unstable in gain across weeks. Despite of the gain variability, time in the natural movie is stably represented by population activity in V1.

Feedback in the brain is thought to convey contextual information that underlies our flexibility to perform different tasks. Empirical and computational work on the visual system suggests this is achieved by targeting task-relevant neuronal subpopulations. We combine two tasks, each resulting in selective modulation by feedback, to test whether the feedback reflected the combination of both selectivities. We used visual feature-discrimination specified at one of two possible locations and uncoupled the decision formation from motor plans to report it, while recording in macaque mid-level visual areas. Here we show that although the behavior is spatially selective, using only task-relevant information, modulation by decision-related feedback is spatially unselective. Population responses reveal similar stimulus-choice alignments irrespective of stimulus relevance. The results suggest a common mechanism across tasks, independent of the spatial selectivity these tasks demand. This may reflect biological constraints and facilitate generalization across tasks. Our findings also support a previously hypothesized link between feature-based attention and decision-related activity., Feedback modulates visual neurons, thought to help achieve flexible task performance. Here, the authors show decision-related feedback is not only relayed to task-relevant neurons, suggesting a broader mechanism and supporting a previously hypothesized link to feature-based attention.

Cortical representations of brief, static stimuli become more invariant to identity-preserving transformations along the ventral stream. Likewise, increased invariance along the visual hierarchy should imply greater temporal persistence of temporally structured dynamic stimuli, possibly complemented by temporal broadening of neuronal receptive fields. However, such stimuli could engage adaptive and predictive processes, whose impact on neural coding dynamics is unknown. By probing the rat analog of the ventral stream with movies, we uncovered a hierarchy of temporal scales, with deeper areas encoding visual information more persistently. Furthermore, the impact of intrinsic dynamics on the stability of stimulus representations grew gradually along the hierarchy. A database of recordings from mouse showed similar trends, additionally revealing dependencies on the behavioral state. Overall, these findings show that visual representations become progressively more stable along rodent visual processing hierarchies, with an important contribution provided by intrinsic processing., Understanding stability of representation in the visual system can benefit by use of non-static, naturalistic stimuli. Here the authors examine stability of neural representations along the rat ventral stream while viewing naturalistic and synthetic movies.

Neuronal activity in sensory cortex fluctuates over time and across repetitions of the same input. This variability is often considered detrimental to neural coding. The theory of neural sampling proposes instead that variability encodes the uncertainty of perceptual inferences. In primary visual cortex (V1), modulation of variability by sensory and non-sensory factors supports this view. However, it is unknown whether V1 variability reflects the statistical structure of visual inputs, as would be required for inferences correctly tuned to the statistics of the natural environment. Here we combine analysis of image statistics and recordings in macaque V1 to show that probabilistic inference tuned to natural image statistics explains the widely observed dependence between spike count variance and mean, and the modulation of V1 activity and variability by spatial context in images. Our results show that the properties of a basic aspect of cortical responses—their variability—can be explained by a probabilistic representation tuned to naturalistic inputs., The neural sampling theory suggests that neuronal variability encodes the uncertainty of probabilistic inferences. This paper shows that response variability in primary visual cortex reflects the statistical structure of visual inputs, as required for inferences correctly tuned to the statistics of the natural environment.

Nicolelis wrote in his 2003 review on brain-machine interfaces (BMIs) that the design of a successful BMI relies on general physiological principles describing how neuronal signals are encoded. Our study explored whether neural information exchanged between brains of different species is possible, similar to the information exchange between computers. We show for the first time that single words processed by the guinea pig auditory system are intelligible to humans who receive the processed information via a cochlear implant. We recorded the neural response patterns to single-spoken words with multi-channel electrodes from the guinea inferior colliculus. The recordings served as a blueprint for trains of biphasic, charge-balanced electrical pulses, which a cochlear implant delivered to the cochlear implant user’s ear. Study participants completed a four-word forced-choice test and identified the correct word in 34.8% of trials. The participants' recognition, defined by the ability to choose the same word twice, whether right or wrong, was 53.6%. For all sessions, the participants received no training and no feedback. The results show that lexical information can be transmitted from an animal to a human auditory system. In the discussion, we will contemplate how learning from the animals might help developing novel coding strategies.

Motor function depends on neural dynamics spanning multiple spatiotemporal scales of population activity, from spiking of neurons to larger-scale local field potentials (LFP). How multiple scales of low-dimensional population dynamics are related in control of movements remains unknown. Multiscale neural dynamics are especially important to study in naturalistic reach-and-grasp movements, which are relatively under-explored. We learn novel multiscale dynamical models for spike-LFP network activity in monkeys performing naturalistic reach-and-grasps. We show low-dimensional dynamics of spiking and LFP activity exhibited several principal modes, each with a unique decay-frequency characteristic. One principal mode dominantly predicted movements. Despite distinct principal modes existing at the two scales, this predictive mode was multiscale and shared between scales, and was shared across sessions and monkeys, yet did not simply replicate behavioral modes. Further, this multiscale mode’s decay-frequency explained behavior. We propose that multiscale, low-dimensional motor cortical state dynamics reflect the neural control of naturalistic reach-and-grasp behaviors., Motor control involves neural dynamics at multiple spatiotemporal scales. Here the authors show that a multiscale, low-dimensional dynamical structure that is shared between scales and subjects reflects naturalistic reach-and-grasp movements in macaques.

When measuring sparseness in neural populations as an indicator of efficient coding, an implicit assumption is that each stimulus activates a different random set of neurons. In other words, population responses to different stimuli are, on average, uncorrelated. Here we examine neurophysiological data from four lobes of macaque monkey cortex, including V1, V2, MT, anterior inferotemporal cortex, lateral intraparietal cortex, the frontal eye fields, and perirhinal cortex, to determine how correlated population responses are. We call the mean correlation the pseudosparseness index, because high pseudosparseness can mimic statistical properties of sparseness without being authentically sparse. In every data set we find high levels of pseudosparseness ranging from 0.59–0.98, substantially greater than the value of 0.00 for authentic sparseness. This was true for synthetic and natural stimuli, as well as for single-electrode and multielectrode data. A model indicates that a key variable producing high pseudosparseness is the standard deviation of spontaneous activity across the population. Consistently high values of pseudosparseness in the data demand reconsideration of the sparse coding literature as well as consideration of the degree to which authentic sparseness provides a useful framework for understanding neural coding in the cortex., Sidney R. Lehky et al. examined neurophysiological data from a wide variety of macaque cortices and find highly correlated population responses to both synthetic and natural stimuli. This high correlation, termed the pseudosparseness index, mimics statistical properties of sparseness without being authentically sparse, highlighting need for more in-depth assessment of the cortical sparse coding literature.

Value-based decision-making requires different variables—including offer value, choice, expected outcome, and recent history—at different times in the decision process. Orbitofrontal cortex (OFC) is implicated in value-based decision-making, but it is unclear how downstream circuits read out complex OFC responses into separate representations of the relevant variables to support distinct functions at specific times. We recorded from single OFC neurons while macaque monkeys made cost-benefit decisions. Using a novel analysis, we find separable neural dimensions that selectively represent the value, choice, and expected reward of the present and previous offers. The representations are generally stable during periods of behavioral relevance, then transition abruptly at key task events and between trials. Applying new statistical methods, we show that the sensitivity, specificity and stability of the representations are greater than expected from the population’s low-level features—dimensionality and temporal smoothness—alone. The separability and stability suggest a mechanism—linear summation over static synaptic weights—by which downstream circuits can select for specific variables at specific times., In value-based decision-making, single prefrontal neurons represent multiple variables at different times in the decision process. Here, the authors show these representations to be separable and stable at the population level, allowing read out of specific variables at behaviorally relevant times.

Humans observe a wide range of actions in their surroundings. How is the visual cortex organized to process this diverse input? Using functional neuroimaging, we measured brain responses while participants viewed short videos of everyday actions, then probed the structure in these responses using voxel-wise encoding modeling. Responses are well fit by feature spaces that capture the body parts involved in an action and the action’s targets (i.e. whether the action was directed at an object, another person, the actor, and space). Clustering analyses reveal five large-scale networks that summarize the voxel tuning: one related to social aspects of an action, and four related to the scale of the interaction envelope, ranging from fine-scale manipulations directed at objects, to large-scale whole-body movements directed at distant locations. We propose that these networks reveal the major representational joints in how actions are processed by visual regions of the brain., How is action perception organized in the brain? Here, the authors report evidence for five networks tuned to actions’ social content and the scale of their effect on the world and propose that sociality and interaction envelope are organizing dimensions of visual action representation.

Much of our world changes smoothly in time, yet the allocation of attention is typically studied with sudden changes – transients. A sizeable lag in selecting feature information is seen when stimuli change smoothly. Yet this lag is not seen with temporally uncorrelated rapid serial visual presentation (RSVP) stimuli. This suggests that temporal autocorrelation of a feature paradoxically increases the latency at which information is sampled. To test this, participants are asked to report the color of a disk when a cue was presented. There is an increase in selection latency when the disk’s color changed smoothly compared to randomly. This increase is due to the smooth color change presented after the cue rather than extrapolated predictions based on the color changes presented before. These results support an attentional drag theory, whereby attentional engagement is prolonged when features change smoothly. A computational model provides insights into the potential underlying neural mechanisms., When a cue is provided, people can rapidly attend to a changing scene and remember how it looked right after the cue appeared, but if the scene changes gradually, there is a delay in what we remember. Here the authors model these effects as prolonged attentional engagement.

Clustering of functionally similar synapses in dendrites is thought to affect neuronal input-output transformation by triggering local nonlinearities. However, neither the in vivo impact of synaptic clusters on somatic membrane potential (sVm), nor the rules of cluster formation are elucidated. We develop a computational approach to measure the effect of functional synaptic clusters on sVm response of biophysical model CA1 and L2/3 pyramidal neurons to in vivo-like inputs. We demonstrate that small synaptic clusters appearing with random connectivity do not influence sVm. With structured connectivity, ~10–20 synapses/cluster are optimal for clustering-based tuning via state-dependent mechanisms, but larger selectivity is achieved by 2-fold potentiation of the same synapses. We further show that without nonlinear amplification of the effect of random clusters, action potential-based, global plasticity rules cannot generate functional clustering. Our results suggest that clusters likely form via local synaptic interactions, and have to be moderately large to impact sVm responses., The formation of functional synaptic clusters (FSCs) and their impact on somatic membrane potential (sVm) in vivo are poorly understood. Here, the authors develop a computational approach to show that FSCs have to form via local rather than global plasticity and be moderately large to impact sVm.

Hippocampal pyramidal neurons are endowed with signature excitability characteristics, exhibit theta-frequency selectivity — manifesting as impedance resonance and as a band-pass structure in the spike-triggered average (STA) — and coincidence detection tuned for gamma-frequency inputs. Are there specific constraints on molecular-scale (ion channel) properties in the concomitant emergence of cellular-scale encoding (feature detection and selectivity) and excitability characteristics? Here, we employed a biophysically-constrained unbiased stochastic search strategy involving thousands of conductance-based models, spanning 11 active ion channels, to assess the concomitant emergence of 14 different electrophysiological measurements. Despite the strong biophysical and physiological constraints, we found models that were similar in terms of their spectral selectivity, operating mode along the integrator-coincidence detection continuum and intrinsic excitability characteristics. The parametric combinations that resulted in these functionally similar models were non-unique with weak pair-wise correlations. Employing virtual knockout of individual ion channels in these functionally similar models, we found a many-to-many relationship between channels and physiological characteristics to mediate this degeneracy, and predicted a dominant role for HCN and transient potassium channels in regulating hippocampal neuronal STA. Our analyses reveals the expression of degeneracy, that results from synergistic interactions among disparate channel components, in the concomitant emergence of neuronal excitability and encoding characteristics.

The methods for electrophysiology in neuroscience have evolved tremendously over the recent years with a growing emphasis on dense-array signal recordings. Such increased complexity and augmented wealth in the volume of data recorded, have not been accompanied by efforts to streamline and facilitate access to processing methods, which too are susceptible to grow in sophistication. Moreover, unsuccessful attempts to reproduce peer-reviewed publications indicate a problem of transparency in science. This growing problem could be tackled by unrestricted access to methods that promote research transparency and data sharing, ensuring the reproducibility of published results.Here, we provide a free, extensive, open-source software that provides data-analysis, data-management and multi-modality integration solutions for invasive neurophysiology. Users can perform their entire analysis through a user-friendly environment without the need of programming skills, in a tractable (logged) way. This work contributes to open-science, analysis standardization, transparency and reproducibility in invasive neurophysiology.