Michele A Cox

Receptive field focus of visual area V4 neurons determines responses to illusory surfaces

Significance Visual information is often fragmented, such as when objects block each other from view, and our brain must actively deduce missing parts of an image to perceive key features of the world. This study asks whether neurons in cortical area V4 can infer the presence of an object’s surface when visual clues are limited. Indeed, our experiments reveal that certain V4 neurons enhance their responses to an array of stimuli only when they are configured to give rise to an illusory surface. Intriguingly, this effect exhibited unexpected spatial precision relative to the inducing components of the illusion. These findings provide important clues about how the brain overcomes a fundamental challenge of vision. Illusory figures demonstrate the visual system’s ability to infer surfaces under conditions of fragmented sensory input. To investigate the role of midlevel visual area V4 in visual surface completion, we used multielectrode arrays to measure spiking responses to two types of visual stimuli: Kanizsa patterns that induce the perception of an illusory surface and physically similar control stimuli that do not. Neurons in V4 exhibited stronger and sometimes rhythmic spiking responses for the illusion-promoting configurations compared with controls. Moreover, this elevated response depended on the precise alignment of the neuron’s peak visual field sensitivity (receptive field focus) with the illusory surface itself. Neurons whose receptive field focus was over adjacent inducing elements, less than 1.5° away, did not show response enhancement to the illusion. Neither receptive field sizes nor fixational eye movements could account for this effect, which was present in both single-unit signals and multiunit activity. These results suggest that the active perceptual completion of surfaces and shapes, which is a fundamental problem in natural visual experience, draws upon the selective enhancement of activity within a distinct subpopulation of neurons in cortical area V4.

Ongoing Alpha Activity in V1 Regulates Visually Driven Spiking Responses

Abstract The interlaminar connections in the primate primary visual cortex (V1) are well described, as is the presence of ongoing alpha‐range (7‐14 Hz) fluctuations in this area. Less well understood is how these interlaminar connections and ongoing fluctuations contribute to the regulation of visual spiking responses. Here, we investigate the relationship between alpha fluctuations and spiking responses to visual stimuli across cortical layers. Using laminar probes in macaque V1, we show that neural firing couples with the phase of alpha fluctuations, and that magnitude of this coupling is particularly pronounced during visual stimulation. The strongest modulation of spiking activity was observed in layers 2/3. Alpha‐spike coupling and current source density analysis pointed to an infragranular origin of the alpha fluctuations. Taken together, these results indicate that ongoing infragranular alpha‐range fluctuations in V1 play a role in regulating columnar visual activity.

Sustained perceptual invisibility of solid shapes following contour adaptation to partial outlines

Contour adaptation (CA) is a recently described paradigm that renders otherwise salient visual stimuli temporarily perceptually invisible. Here we investigate whether this illusion can be exploited to study visual awareness. We found that CA can induce seconds of sustained invisibility following similarly long periods of uninterrupted adaptation. Furthermore, even fragmented adaptors are capable of producing CA, with the strength of CA increasing monotonically as the adaptors encompass a greater fraction of the stimulus outline. However, different types of adaptor patterns, such as distinctive shapes or illusory contours, produce equivalent levels of CA suggesting that the main determinants of CA are low-level stimulus characteristics, with minimal modulation by higher-order visual processes. Taken together, our results indicate that CA has desirable properties for studying visual awareness, including the production of prolonged periods of perceptual dissociation from stimulation as well as parametric dependencies of that dissociation on a host of stimulus parameters.

Serial versus parallel processing in mid-level vision: filling-in the details of spatial interpolation

Abstract The relationship between boundary completion and surface filling-in, two core mechanisms of mid-level vision, remains unclear. Here, we integrate recent empirical findings to shine new light onto the neural mechanisms of boundary completion and surface filling-in as well as their relation to each other. Specifically, we discuss several psychophysical and neurophysiological studies that, when taken together, support a model where object boundaries and visual surfaces are interpolated in parallel, with one process impacting the other. We suggest that visual boundary completion and surface filling-in are two interacting processes that are supported by neural processes that are distributed throughout several areas of the early visual system.

Anisotropy of ongoing neural activity in the primate visual cortex

The mammalian neocortex features distinct anatomical variation in its tangential and radial extents. This review consolidates previously published findings from our group in order to compare and contrast the spatial profile of neural activity coherence across these distinct cortical dimensions. We focus on studies of ongoing local field potential (LFP) data obtained simultaneously from multiple sites in the primary visual cortex in two types of experiments in which electrode contacts were spaced either along the cortical surface or at different laminar positions. These studies demonstrate that across both dimensions the coherence of ongoing LFP fluctuations diminishes as a function of interelectrode distance, although the nature and spatial scale of this falloff is very different. Along the cortical surface, the overall LFP coherence declines gradually and continuously away from a given position. In contrast, across the cortical layers, LFP coherence is discontinuous and compartmentalized as a function of depth. Specifically, regions of high LFP coherence fall into discrete superficial and deep laminar zones, with an abrupt discontinuity between the granular and infragranular layers. This spatial pattern of ongoing LFP coherence is similar when animals are at rest and when they are engaged in a behavioral task. These results point to the existence of partially segregated laminar zones of cortical processing that extend tangentially within the laminar compartments and are thus oriented orthogonal to the cortical columns. We interpret these electrophysiological observations in light of the known anatomical organization of the cortical microcircuit.

Adaptation of Intracortical Signaling Concurs with Enhanced Encoding Efficiency

Stimulus repetitions improve performance despite decreased brain responses, suggesting that the brain is more efficient when processing familiar stimuli. Previous work demonstrated that stimulus repetition enhances encoding efficiency in primary visual cortex (V1) by increasing synchrony and sharpening the orientation tuning of neurons. Here we show that these adaptive changes are supported by an altered flow of sensory activation across the V1 laminar microcircuit. Using a repeating stimulus sequence, we recorded laminar responses in V1 of two fixating monkeys. We found repetition-related response reductions that were most pronounced outside V1 layers that receive the main retinogeniculate input. This repetition-induced suppression was robust to alternating stimuli between the eyes, in line with the notion that repetition suppression is predominantly of cortical origin. Congruent with earlier reports, we found that V1 adaptation to repeating stimuli is accompanied by sharpened neural tuning as well as increased neural synchrony. Current source density (CSD) analysis, which provides an estimate of net synaptic activation, revealed that the responses to repeated stimuli were most profoundly affected within layers that harbor the bulk of cortico-cortical connections. Together, these results suggest that stimulus repetition induces an altered state of intracortical processing resulting in enhanced encoding efficiency of sensory stimuli.

Binocular Integration Manifests as a Transient Spiking Increase Followed by Selective Suppression in Primary Visual Cortex

Research throughout the past decades revealed that neurons in primate primary visual cortex (V1) rapidly integrate the two eyes’ separate signals into a combined binocular response. The exact mechanisms giving underlying this binocular integration remain elusive. One open question is whether binocular integration occurs at a single stage of sensory processing or in a sequence of computational steps. To address this question, we examined the temporal dynamics of binocular integration across V1’s laminar microcircuit of awake behaving monkeys. We find that V1 processes binocular stimuli in a dynamic sequence that comprises at least two distinct phases: A transient phase, lasting 50-150ms from stimulus onset, in which neuronal population responses are significantly enhanced for binocular stimulation compared to monocular stimulation, followed by a sustained phase characterized by widespread suppression in which feature-specific computations emerge. In the sustained phase, incongruent binocular stimulation resulted in response reduction relative to monocular stimulation across the V1 population. By contrast, sustained responses for binocular congruent stimulation were either reduced or enhanced relative to monocular responses depending on the neurons’ selectivity for one or both eyes (i.e., ocularity). These results suggest that binocular integration in V1 occurs in at least two sequential steps, with an initial additive combination of the two eyes’ signals followed by the establishment of interocular concordance and discordance. Significance Statement Our two eyes provide two separate streams of visual information that are merged in the primary visual cortex (V1). Previous work showed that stimulating both eyes rather than one eye may either increase or decrease activity in V1, depending on the nature of the stimuli. Here we show that V1 binocular responses change over time, with an early phase of general excitation and followed by stimulus-dependent response suppression. These results provide important new insights into the neural machinery that supports the combination of the two eye’s perspectives into a single coherent view.

Binocular modulation of monocular V1 neurons

Our brains combine the separate streams of sensory signals from the two eyes into a singular view. Where the separate streams from the two eyes first converge in the primary visual pathway is unclear. At the initial stage of visual processing following transduction in the retina, neurons in the lateral geniculate nucleus of the thalamus (LGN) are deemed monocular because they are excited by stimulation of one eye and not the other. At the next stage of visual processing, in the primary visual cortex (V1), there are many neurons that are deemed binocular because they are excited by stimulation of either eye, signifying that binocular convergence has happened by that stage. Visual stimulation evokes a specific sequence of activation across the laminar microcircuit of V1. During which part of this sequence binocular convergence occurs is unresolved. Here we investigate where binocular convergence occurs in the V1 laminar microcircuit by examining the extent to which macaque V1 neurons in all layers are sensitive to both eyes. We found that more than 94% of V1 neurons across all layers were binocular in the sense that they were driven by stimulation of either eye. As expected, monocular neurons were largely located in the primary geniculate input layer of V1. Interestingly, these monocular neurons showed systematic firing rate differences between stimulation of their driving eye alone compared to stimulation of both eyes, revealing that these so-called monocular neurons actually encode what is shown to both eyes. This finding suggests that, while geniculate inputs to V1 are largely segregated by eye, the outputs of their V1 target neurons are sensitive to what both eyes view, marking this processing stage as the primary point of binocular convergence in the primate visual system.

Spiking Suppression Precedes Cued Attentional Enhancement of Neural Responses in Primary Visual Cortex

Attending to a visual stimulus increases its detectability, even if gaze is directed elsewhere. This covert attentional selection is known to enhance spiking across many brain areas, including the primary visual cortex (V1). Here we investigate the temporal dynamics of attention-related spiking changes in V1 of macaques performing a task that separates attentional selection from the onset of visual stimulation. We found that preceding attentional enhancement there was a sharp, transient decline in spiking following presentation of an attention-guiding cue. This disruption of V1 spiking was not observed in a task-naïve subject that passively observed the same stimulus sequence, suggesting that sensory activation is insufficient to cause suppression. Following this suppression, attended stimuli evoked more spiking than unattended stimuli, matching previous reports of attention-related activity in V1. Laminar analyses revealed a distinct pattern of activation in feedback-associated layers during both the cue-induced suppression and subsequent attentional enhancement. These findings suggest that top-down modulation of V1 spiking can be bidirectional and result in either suppression or enhancement of spiking responses.

Visual spiking responses in V1 couple to alpha fluctuations in deep layers.

Alpha-range (8-12 Hz) neural rhythms, prominent over occipital cortex, can serve as a predictor of performance on visual tasks. Specifically, visual performance and attentional selection have been shown to co-vary with the ongoing alpha cycle recorded on the scalp. Despite their impact on visual performance, little is known about the intracortical origins of alpha rhythms and how alpha cycles impact visual processing. Here, we study laminar neural activity in primate visual cortex in order to determine a mechanistic link between alpha cycles and visually evoked spiking responses. Two macaque monkeys (Macaca radiata) fixated while static grating stimuli were presented inside of the receptive field under study. During this time, we recorded alpha-range local field potentials and multiunit spiking activity from all layers of V1 simultaneously. We found that throughout several hundred milliseconds of visual stimulation, spiking activity in all layers was strongly decreased at the time of alpha troughs recorded in the deep, feedback-recipient cortical layers compared to the level of columnar spiking at alpha peaks. Specifically, the magnitude of population spiking activity at the time of alpha troughs was nearly half that at alpha peaks, suggesting that alpha induces pulsed inhibition of visual responses at the earliest stages of cortical processing. Lastly in order to probe the potential role of feedback afferences, we will present a comparison of intracolumnar coupling between alpha and visual spiking responses between the two attentional states. Meeting abstract presented at VSS 2015.