Neurons In Early Visual Cortex Research Articles

Brief Stimuli Cast a Persistent Long-Term Trace in Visual Cortex.

Visual processing is strongly influenced by recent stimulus history, a phenomenon termed adaptation. Prominent theories cast adaptation as a consequence of optimized encoding of visual information by exploiting the temporal statistics of the world. However, this would require the visual system to track the history of individual briefly experienced events, within a stream of visual input, to build up statistical representations over longer timescales. Here, using an openly available dataset from the Allen Brain Observatory, we show that neurons in the early visual cortex of the mouse indeed maintain long-term traces of individual past stimuli that persist despite the presentation of several intervening stimuli, leading to long-term and stimulus-specific adaptation over dozens of seconds. Long-term adaptation was selectively expressed in cortical, but not in thalamic, neurons, which only showed short-term adaptation. Early visual cortex thus maintains concurrent stimulus-specific memory traces of past input, enabling the visual system to build up a statistical representation of the world to optimize the encoding of new information in a changing environment.SIGNIFICANCE STATEMENT In the natural world, previous sensory input is predictive of current input over multisecond timescales. The visual system could exploit these predictabilities by adapting current visual processing to the long-term history of visual input. However, it is unclear whether the visual system can track the history of individual briefly experienced images, within a stream of input, to build up statistical representations over such long timescales. Here, we show that neurons in early visual cortex of the mouse brain exhibit remarkably long-term adaptation to brief stimuli, persisting over dozens of seconds, and despite the presentation of several intervening stimuli. The visual cortex thus maintains long-term traces of individual briefly experienced past images, enabling the formation of statistical representations over extended timescales.

Amodal completion instead of predictive coding can explain activity suppression of early visual cortex during illusory shape perception

A set of recent neuroimaging studies observed that the perception of an illusory shape can elicit both positive and negative feedback modulations in different parts of the early visual cortex. When three Pac-Men shapes were aligned in such a way that they created an illusory triangle (i.e., the Kanizsa illusion), neural activity in early visual cortex was enhanced in those neurons that had receptive fields that overlapped with the illusory shape but suppressed in neurons whose receptive field overlapped with the Pac-Men inducers. These results were interpreted as congruent with the predictive coding framework, in which neurons in early visual cortex enhance or suppress their activity depending on whether the top-down predictions match the bottom-up sensory inputs. However, there are several plausible alternative explanations for the activity modulations. Here we tested a recent proposal (Moors, 2015) that the activity suppression in early visual cortex during illusory shape perception reflects neural adaptation to perceptually stable input. Namely, the inducers appear perceptually stable during the illusory shape condition (discs on which a triangle is superimposed), but not during the control condition (discs that change into Pac-Men). We examined this hypothesis by manipulating the perceptual stability of inducers. When the inducers could be perceptually interpreted as persistent circles, we replicated the up- and downregulation pattern shown in previous studies. However, when the inducers could not be perceived as persistent circles, we still observed enhanced activity in neurons representing the illusory shape but the suppression of activity in neurons representing the inducers was absent. Thus our results support the hypothesis that the activity suppression in neurons representing the inducers during the Kanizsa illusion is better explained by neural adaptation to perceptually stable input than by reduced prediction error.

Visual Cortex: Binocular Matchmaking

Most binocular neurons in the mammalian visual cortex show matched selectivity for light stimuli presented through either eye. A recent study tracked the responses of individual neurons in early visual cortex over time, revealing that matched binocular selectivity develops through major rearrangements of binocular visual circuits.

Steady-state visual evoked potentials reveal enhanced neural responses to illusory surfaces during a concurrent visual attention task

Under natural viewing conditions, visual stimuli are often obscured by occluding surfaces. To aid object recognition, the visual system actively reconstructs the missing information, as exemplified in the classic Kanizsa illusion, a phenomenon termed “modal completion”. Single-cell recordings in monkeys have shown that neurons in early visual cortex respond to illusory contours, but it has proven difficult to measure the neural correlates of modal completion in humans. We used electroencephalography (EEG) to measure steady-state visual-evoked potentials (SSVEPs) from disks with quarter segments removed to induce an illusory shape (or rotated to eliminate the illusory square in control trials). Opposing pairs of inducers were tagged with one of two flicker frequencies (2.5 or 4 Hz). During stimulus presentations, participants performed an attention task at fixation that required them to judge the orientation of a briefly flashed central bar while ignoring congruent (same orientation) or incongruent (different orientation) flanker bars that appeared on or off the illusory surface. Importantly, the occurrence of any illusory shape was never task relevant. Frequency-based analyses revealed that SSVEP amplitudes were reliably enhanced for trials in which an illusory square appeared, relative to control trials, at 4, 5 and 8 Hz and at an intermodulation frequency of 13 Hz. Participants' reaction times in the flanker task were significantly slower for incongruent versus congruent trials, and this distractor interference effect occurred only in the presence of an illusory surface and not in the control condition. Our results reveal a robust neural correlate of modal completion in the human visual system and provide evidence that visual completion can affect attentional control processes as deployed in a flanker task.

Nonlinear Y-Like Receptive Fields in the Early Visual Cortex: An Intermediate Stage for Building Cue-Invariant Receptive Fields from Subcortical Y Cells.

A significant fraction of neurons in early visual cortex have specialized receptive fields that allow them to selectively respond to the orientation of boundaries that are invariant to the cue (luminance, contrast, texture, motion) that defines them. However, the neural mechanism to construct such versatile receptive fields remains unclear. Using multielectrode recording, we found a large fraction of neurons in early visual cortex with receptive fields not selective for orientation that have spatial nonlinearities like those of subcortical Y cells. These are strong candidates for building cue-invariant orientation-selective neurons; we present a neural circuit model that pools such neurons in an imbalanced "push-pull" manner, to generate orientation-selective cue-invariant receptive fields.

The efficiency of second order orientation coherence detection

Neurons in early visual cortex respond to both luminance- (1st order) and contrast-modulated (2nd order) local features in the visual field. In later extra-striate areas neurons with larger receptive fields integrate information across the visual field. For example, local luminance-defined features can be integrated into contours and shapes. Evidence for the global integration of features defined by contrast-modulation is less well established. While good performance in some shape tasks has been demonstrated with 2nd order stimuli, the integration of contours fails with 2nd order elements. Recently we developed a global orientation coherence task that is more basic than contour integration, bearing similarity to the well-established global motion coherence task. Similar to our previous 1st order result for this task, we find 2nd order coherence detection to be scale-invariant. There was a small but significant threshold elevation for 2nd order relative to 1st order. We used a noise masking approach to compare the efficiency of orientation integration for the 1st and 2nd order. We find a significant deficit for 2nd order detection at both the local and global level, however the small size of this effect stands in stark contrast against previous results from contour-integration experiments, which are almost impossible with 2nd order stimuli.

Contrast-dependent phase sensitivity in V1 but not V2 of macaque visual cortex.

Some neurons in early visual cortex are highly selective for the position of oriented edges in their receptive fields (simple cells), whereas others are largely position insensitive (complex cells). These characteristics are reflected in their sensitivity to the spatial phase of moving sine-wave gratings: simple cell responses oscillate at the fundamental frequency of the stimulus, whereas this is less so for complex cells. In primates, when assessed at high stimulus contrast, simple cells and complex cells are roughly equally represented in the first visual cortical area, V1, whereas in the second visual area, V2, the majority of cells are complex. Recent evidence has shown that phase sensitivity of complex cells is contrast dependent. This has led to speculation that reduced contrast may lead to changes in the spatial structure of receptive fields, perhaps due to changes in how feedforward and recurrent signals interact. Given the substantial interconnections between V1 and V2 and recent evidence for the emergence of unique functional capacity in V2, we assess the relationship between contrast and phase sensitivity in the two brain regions. We show that a substantial proportion of complex cells in macaque V1 exhibit significant increases in phase sensitivity at low contrast, whereas this is rarely observed in V2. Our results support a degree of hierarchical processing from V1 to V2 with the differences possibly relating to the fact that V1 combines both subcortical and cortical input, whereas V2 receives input purely from cortical circuits.

Long-range, pattern-dependent contextual effects in early human visual cortex

The standard view of neurons in early visual cortex is that they behave like localized feature detectors. We will discuss recent results that demonstrate that neurons in early visual areas go beyond localized feature detection and are sensitive to part-whole relationships in images. We measured neural responses to a grating stimulus (“target”) embedded in various visual patterns as defined by the relative orientation of flanking stimuli. We varied whether or not the target was part of a predictable sequence by changing the orientation of distant gratings while maintaining the same local stimulus arrangement. For example, a vertically oriented target grating that is flanked locally with horizontal flankers (HVH) can be made to be part of a predictable sequence by adding vertical distant flankers (VHVHV). We found that even when the local configuration (e.g. HVH) around the target was kept the same there was a smaller neural response when the target was part of a predictable sequence (VHVHV). Furthermore, when making an orientation judgment of a “noise” stimulus that contains no specific orientation information, observers were biased to “see” the orientation that deviates from the predictable orientation, consistent with computational models of primate cortical processing that incorporate efficient coding principles. Our results suggest that early visual cortex is sensitive to global patterns in images in a way that is markedly different from the predictions of standard models of cortical visual processing and indicate an important role in coding part-whole relationships in images. Meeting abstract presented at VSS 2012

Functional Organization of Envelope-Responsive Neurons in Early Visual Cortex: Organization of Carrier Tuning Properties

It is well established that visual cortex neurons having similar selectivity for orientation, direction of motion, ocular dominance, and other properties of first-order (luminance-defined) stimuli are clustered into a columnar organization. However, the cortical architecture of neuronal responses to second-order (contrast/texture-defined) stimuli is poorly understood. A useful second-order stimulus is a contrast envelope, consisting of a finely detailed pattern (carrier) whose contrast varies on a coarse spatial scale (envelope). In this study, we analyzed the cortical organization of carrier tuning properties of neurons, which responded to contrast-modulated stimuli. We examined whether neurons tuned to similar carrier properties are clustered spatially and whether such spatial clusters are arranged in columns. To address these questions, we recorded single-unit activity, multiunit activity, and local field potentials simultaneously from area 18 of anesthetized cats, using single-channel microelectrodes and multielectrode arrays. Our data showed that neurons tuned to similar carrier spatial frequency are distributed in a highly clustered manner; neurons tuned to similar carrier orientation are also significantly clustered. Neurons along linear arrays perpendicular to the brain surface always exhibited similar optimal carrier spatial frequency, indicating a columnar organization. Multi-pronged tetrode recordings indicated that the diameter of these columns is ≥450 μm. Optimal carrier orientation was also significantly clustered but with finer-grain organization and greater scatter. These results indicate a fine anatomical structure of cortical organization of second-order information processing and suggest that there are probably more maps in cat area 18 than previously believed.

Long-Range, Pattern-Dependent Contextual Effects in Early Human Visual Cortex

The standard view of neurons in early visual cortex is that they behave like localized feature detectors. Here we demonstrate that processing in early visual areas goes beyond feature detection by showing that neural responses are greater when a feature deviates from its context compared to when it does not deviate from its context. Using psychophysics, fMRI, and electroencephalography methodologies, we measured neural responses to an oriented Gabor ("target") embedded in various visual patterns as defined by the relative orientation of flanking stimuli. We first show using psychophysical contrast adaptation and fMRI that a target that differs from its context results in more neural activity compared to a target that is contained within an alternating sequence, suggesting that neurons in early visual cortex are sensitive to large-scale orientation patterns. Next, we use event-related potentials to show that orientation deviations affect the earliest sensory components of the target response. Finally, we use forced-choice classification of "noise" stimuli to show that we are more likely to "see" orientations that deviate from the context. Our results suggest that early visual cortex is sensitive to global patterns in images in a way that is markedly different from the predictions of standard models of cortical visual processing.

Long-range, pattern-dependent contextual effects in early visual cortex

Summary The standard view of neurons in early visual cortex is that they behave like localized feature detectors [1–7]. Here we demonstrate that processing in early visual areas goes beyond feature detection by showing that neural responses are greater when a feature deviates from its context compared to when it does not deviate from its context. Using psychophysics, fMRI, and electroencephalography methodologies, we measured neural responses to an oriented Gabor (target) embedded in various visual patterns as defined by the relative orientation of flanking stimuli. We first show using psychophysical contrast adaptation and fMRI that a target that differs from its context results in more neural activity compared to a target that is contained within an alternating sequence, suggesting that neurons in early visual cortex are sensitive to large-scale orientation patterns. Next, we use event-related potentials to show that orientation deviations affect the earliest sensory components of the target response. Finally, we use forced-choice classification of noise stimuli to show that we are more likely to see orientations that deviate from the context. Our results suggest that early visual cortex is sensitive to global patterns in images in a way that is markedly different from the predictions of standard models of cortical visual processing.

Binding and selective attention increase coherence between distant sites in early visual cortex

We have proposed that the border ownership selectivity that is observed in many neurons in early visual cortex is the result of specific network connectivity (Craft et. al., J. Neurophysiol. 97:4310–26, 2007). According to our model, border ownership cells (B-cells) have reciprocal connections with grouping cells (G-cells) in another level of cortex. A G-cell integrates inputs from B-cells and modulates their firing rates. When a pair of neurons is activated by edges that are part of one figure (the contours are bound), the neurons receive reentrant inputs from the same G-cell. When the contours are part of separate figures, the inputs come from different G-cells. Thus the model predicts that coherence will increase between pairs with bound edges in their receptive fields. Specifically, because pairs that both prefer the bound configuration are connected to the same G-cell, they should display enhanced coherence with binding compared to other pairs. In the model, attention is inserted at a G-cell and propagates back to the B-cells, modulating their firing rates for further processing. Thus as with binding, the model predicts that coherence will increase with attention, especially for pairs that both prefer the bound configuration. We tested these predictions by recording local field potentials and single-unit spiking activity from two electrodes separated by long distances (3–10 mm) in macaque areas V1 and V2. We found that binding increases coherence at around 20 Hz, especially for pairs that both prefer the bound configuration. Selective attention also increases coherence in the same range, though the effect is more subtle. As with binding, the increase in coherence with attention is more pronounced for pairs that both prefer the bound configuration. These results support the network connectivity proposed by the model. The coherence difference (although not gamma) may play a role in coding binding and selective attention.

Chromatic tuning of binocular neurons in early visual cortex

Chromatic tuning of binocular neurons in early visual cortex

Effects of Orientation-Specific Visual Deprivation Induced with Altered Reality

What happens to neurons in visual cortex when they are deprived of their preferred stimuli? Long-term deprivation during development, spanning weeks, reduces the number of neurons selective for the deprived orientation [1-4]. In contrast, short-term deprivation in adults, for periods of seconds, can increase neural sensitivity relative to a stimulated baseline [5]. Effects over intermediate timescales remain largely unexplored, however. Here we introduce a new method for manipulating the visual environment of adult humans and report effects of four hours of orientation-specific deprivation. Subjects wore a head-mounted video camera that fed into a laptop computer that drove a head-mounted display. Software filtered the video stream in real time, allowing subjects to interact with the world while being deprived of visual input at a specified orientation. Four hours in this environment increased sensitivity to the deprived orientation, which likely reflected an increase in responsiveness of neurons in early visual cortex. Our results help distinguish between two theories of neural adaptation: the response increase optimized the responses of individual neurons, rather than increasing the efficiency of the population code. Our method should be able to produce a wide range of environmental manipulations useful for studying many topics in perception.

Dissociation of Neural Mechanisms Underlying Orientation Processing in Humans

Orientation selectivity is a fundamental, emergent property of neurons in early visual cortex, and the discovery of that property has dramatically shaped how we conceptualize visual processing. However, much remains unknown about the neural substrates of this basic building block of perception, and what is known primarily stems from animal physiology studies. To probe the neural concomitants of orientation processing in humans, we employed repetitive transcranial magnetic stimulation (rTMS), which can significantly attenuate neuronal spiking activity, hemodynamic responses, and local field potentials within a focused cortical region. Using rTMS to suppress neural responses evoked by stimuli falling within a local region of the visual field, we were able to dissociate two distinct components of the neural circuitry underlying orientation processing: selectivity and contextual effects. Orientation selectivity gauged by masking was unchanged by rTMS, whereas an otherwise robust orientation repulsion illusion was weakened after rTMS. This dissociation implies that orientation processing in humans relies on distinct mechanisms, only one of which was impacted by rTMS. These results are consistent with models positing that orientation selectivity is governed by patterns of convergence of thalamic afferents onto cortical neurons, with intracortical activity then shaping population responses amongst those cortical neurons.

Neuronal response to texture- and contrast-defined boundaries in early visual cortex

Natural scenes contain a variety of visual cues that facilitate boundary perception (e.g., luminance, contrast, and texture). Here we explore whether single neurons in early visual cortex can process both contrast and texture cues. We recorded neural responses in cat A18 to both illusory contours formed by abutting gratings (ICs, texture-defined) and contrast-modulated gratings (CMs, contrast-defined). We found that if a neuron responded to one of the two stimuli, it also responded to the other. These neurons signaled similar contour orientation, spatial frequency, and movement direction of the two stimuli. A given neuron also exhibited similar selectivity for spatial frequency of the fine, stationary grating components (carriers) of the stimuli. These results suggest that the cue-invariance of early cortical neurons extends to different kinds of texture or contrast cues, and might arise from a common nonlinear mechanism.