Representation of visual stimuli in inferior temporal cortex.

In primates, inferior temporal (IT) cortex is crucial for the processing and storage of visual information about form and colour. This article reviews the properties of IT neurons and considers how these properties may underlie the perceptual and mnemonic functions of IT cortex. The available evidence suggests that the processing of the facial image by IT cortex is similar to its processing of other visual patterns. Faces and other complex visual stimuli appear to be represented by the pattern of responses over a population of IT neurons rather than by the responses of specific 'feature detectors' or 'grandmother' cells. IT neurons with adult-like stimulus properties are present in monkeys as young as six weeks old.     

Phase-of-firing coding of natural visual stimuli in primary visual cortex

We investigated the hypothesis that neurons encode rich naturalistic stimuli in terms of their spike times relative to the phase of ongoing network fluctuations rather than only in terms of their spike count. We recorded local field potentials (LFPs) and multiunit spikes from the primary visual cortex of anaesthetized macaques while binocularly presenting a color movie. We found that both the spike counts and the low-frequency LFP phase were reliably modulated by the movie and thus conveyed information about it. Moreover, movie periods eliciting higher firing rates also elicited a higher reliability of LFP phase across trials. To establish whether the LFP phase at which spikes were emitted conveyed visual information that could not be extracted by spike rates alone, we compared the Shannon information about the movie carried by spike counts to that carried by the phase of firing. We found that at low LFP frequencies, the phase of firing conveyed 54% additional information beyond that conveyed by spike counts. The extra information available in the phase of firing was crucial for the disambiguation between stimuli eliciting high spike rates of similar magnitude. Thus, phase coding may allow primary cortical neurons to represent several effective stimuli in an easily decodable format.     

Adaptation to contingencies in macaque primary visual cortex.

We tested the hypothesis that neurons in the primary visual cortex (V1) adapt selectively to contingencies in the attributes of visual stimuli. We recorded from single neurons in macaque V1 and measured the effects of adaptation either to the sum of two gratings (compound stimulus) or to the individual gratings. According to our hypothesis, there would be a component of adaptation that is specific to the compound stimulus. In a first series of experiments, the two gratings differed in orientation. One grating had optimal orientation and the other was orthogonal to it, and therefore did not activate the neuron under study. These experiments provided evidence in favour of our hypothesis. In most cells adaptation to the compound stimulus reduced responses to the compound stimulus more than it reduced responses to the optimal grating, and the responses to the compound stimulus were reduced more by adaptation to the compound stimulus than by adaptation to the individual gratings. This suggests that a component of adaptation was specific to (and caused by) the simultaneous presence of the two orientations in the compound stimulus. To test whether V1 neurons could adapt to other contingencies in the stimulus attributes, we performed a second series of experiments, in which the component gratings were parallel but differed in spatial frequency, and were both effective in activating the neuron under study. These experiments failed to reveal convincing contingent effects of adaptation, suggesting that neurons cannot adapt equally well to all types of contingency.     

Lateral connectivity and contextual interactions in macaque primary visual cortex

Two components of cortical circuits could mediate contour integration in primary visual cortex (V1): intrinsic horizontal connections and feedback from higher cortical areas. To distinguish between these, we combined functional mapping with a new technique for labeling axons, a recombinant adenovirus bearing the gene for green fluorescent protein (GFP), to determine the extent, density, and orientation specificity of V1 intrinsic connections and V2 to V1 feedback. Both connections cover portions of V1 representing regions of visual space up to eight times larger than receptive fields as classically defined, though the intrinsic connections are an order of magnitude denser than the feedback. Whereas the intrinsic connections link similarly oriented domains in V1, V2 to V1 feedback displays no such specificity. These findings suggest that V1 intrinsic horizontal connections provide a more likely substrate for contour integration.     

A neuronal basis of iconic memory in macaque primary visual cortex

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The representation of erroneously perceived stimuli in the primary visual cortex

In order to attain a correct interpretation of an ambiguous visual stimulus, the brain may have to elaborate on the sensory evidence. Are the neurons that carry the sensory evidence also involved in generating an interpretation? To address this question, we studied the activity of neurons in the primary visual cortex of macaque monkeys involved in a task in which they have to trace a curve mentally, without moving their eyes. On a percentage of trials, the monkeys made errors and traced the wrong curve. Here, we show that these errors are predicted by activity in area V1. Thus, neurons in the primary visual cortex do not only represent sensory events, but also the way in which they are interpreted by the monkey.     

Specialized color modules in macaque extrastriate cortex

Imaging studies are consistent with the existence of brain regions specialized for color, but electrophysiological studies have produced conflicting results. Here we address the neural basis for color, using targeted single-unit recording in alert macaque monkeys, guided by functional magnetic resonance imaging (fMRI) of the same subjects. Distributed within posterior inferior temporal cortex, a large region encompassing V4, PITd, and posterior TEO that some have proposed functions as a single visual complex, we found color-biased fMRI hotspots that we call "globs," each several millimeters wide. Almost all cells located in globs showed strong luminance-invariant color tuning and some shape selectivity. Cells in different globs represented distinct visual field locations, consistent with the coarse retinotopy of this brain region. Cells in "interglob" regions were not color tuned, but were more strongly shape selective. Neither population was direction selective. These results suggest that color perception is mediated by specialized neurons that are clustered within the extrastriate brain.     

Neural mechanisms for color perception in the primary visual cortex

New neurophysiological results show the existence of multiple transformations of color signals in the primary visual cortex (V1) in macaque monkey. These different color mechanisms may contribute separately to the perception of color boundaries and colored regions. Many cells in V1 respond to color and to black-white (luminance) patterns. These neurons are spatially selective and could provide signals about boundaries between differently colored regions. Other V1 neurons that prefer color over luminance respond without much spatial selectivity to colored stimuli, and could be the neural basis for the response to local color modulation within a region. How these different types of color cells combine inputs from cone photoreceptors is what gives them their different spatial selectivities for color.     

Attentional load modulates responses of human primary visual cortex to invisible stimuli

Visual neuroscience has long sought to determine the extent to which stimulus-evoked activity in visual cortex depends on attention and awareness. Some influential theories of consciousness maintain that the allocation of attention is restricted to conscious representations [1, 2]. However, in the load theory of attention [3], competition between task-relevant and task-irrelevant stimuli for limited-capacity attention does not depend on conscious perception of the irrelevant stimuli. The critical test is whether the level of attentional load in a relevant task would determine unconscious neural processing of invisible stimuli. Human participants were scanned with high-field fMRI while they performed a foveal task of low or high attentional load. Irrelevant, invisible monocular stimuli were simultaneously presented peripherally and were continuously suppressed by a flashing mask in the other eye [4]. Attentional load in the foveal task strongly modulated retinotopic activity evoked in primary visual cortex (V1) by the invisible stimuli. Contrary to traditional views [1, 2, 5, 6], we found that availability of attentional capacity determines neural representations related to unconscious processing of continuously suppressed stimuli in human primary visual cortex. Spillover of attention to cortical representations of invisible stimuli (under low load) cannot be a sufficient condition for their awareness.     

Representation of response categories in visual cortex

It is known that single neurons in visual area V4 are selective for visual features and that their responses are modulated by selective attention. Surprisingly, a new study by Mirabella et al. in this issue of Neuron found that V4 neurons also signal the behavioral response category of the attended feature.     

Varying response of caudate neurons to visual stimuli in awake cats

Activity in 62 caudate nucleus neurons produced during presentation of visual stimuli was recorded during experiments on awake cats. Response of a sensory pattern, associated with a photic stimulus falling within a certain section of the visual field was observed in 52% of the neurons tested as against only 11% manifesting motor response related to eye movement guided towards a target. About a quarter of the cells responded to biologically significant stimuli, producing a nonspecific response, i.e., not specifically related to the nature of the visual stimuli presented. Several different response patterns could be recorded from a single unit. A hypothesis that more than one parallel pathway for afferent visual inferences on the caudate nucleus may exist is presented on the basis of findings from this research.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 21, No. 3, May–June, pp. 372–378, 1989.     

Perceptual learning reduces interneuronal correlations in macaque visual cortex

Responses of neurons in early visual cortex change little with training and appear insufficient to account for perceptual learning. Behavioral performance, however, relies on population activity, and the accuracy of a population code is constrained by correlated noise among neurons. We tested whether training changes interneuronal correlations in the dorsal medial superior temporal area, which is involved in multisensory heading perception. Pairs of single units were recorded simultaneously in two groups of subjects: animals trained extensively in a heading discrimination task, and "naive" animals that performed a passive fixation task. Correlated noise was significantly weaker in trained versus naive animals, which might be expected to improve coding efficiency. However, we show that the observed uniform reduction in noise correlations leads to little change in population coding efficiency when all neurons are decoded. Thus, global changes in correlated noise among sensory neurons may be insufficient to account for perceptual learning.     

Spontaneous high-gamma band activity reflects functional organization of auditory cortex in the awake macaque

In the absence of sensory stimuli, spontaneous activity in the brain has been shown to exhibit organization at multiple spatiotemporal scales. In the macaque auditory cortex, responses to acoustic stimuli are tonotopically organized within multiple, adjacent frequency maps aligned in a caudorostral direction on the supratemporal plane (STP) of the lateral sulcus. Here, we used chronic microelectrocorticography to investigate the correspondence between sensory maps and spontaneous neural fluctuations in the auditory cortex. We first mapped tonotopic organization across 96 electrodes spanning approximately two centimeters along the primary and higher auditory cortex. In separate sessions, we then observed that spontaneous activity at the same sites exhibited spatial covariation that reflected the tonotopic map of the STP. This observation demonstrates a close relationship between functional organization and spontaneous neural activity in the sensory cortex of the awake monkey.     

Recognition of visual stimuli from multiple neuronal activity in monkey visual cortex

Response patterns recorded with 30 microelectrodes from area 17 of anaesthetized monkeys are analysed. A proportion of the patterns are used to define prototype response patterns. These in turn are used to recognize the stimulus from further non-averaged response patterns. In comparison, recognition by a feedforward neural network is much slower, and slightly inferior. The excitation time structure, with a resolution of about 20 ms, is found to contribute strongly to the recognition. There is some inter-ocular recognition for oriented moving bars, and for on and off phases of switched lights, but none for colours. Generalizations over some stimulus parameters (i.e. cases of confusion) are examined: If small jerking shapes are incorrectly recognized, in general the jerk direction often is the correct one. The onset of a response can most easily be found by determining the dissimilarity relative to spontaneous activity in a sliding window.     

Representation of three-dimensional visual space in the cerebral cortex

This article reviews two issues relevant to the topic of how three-dimensional space is represented in the cerebral cortex. The first is the question of how individual neurons encode information that might contribute to stereoscopic estimation of visual depth. Particular attention is given to the current understanding of the neural representation of motion through three-dimensional space and to the complexities that arise in interpreting neuronal responses to this complex stimulus parameter. The second issue considered is the disorderlines that exists in the retinotopic mapping of the visual field in some cortical visual areas. Several extrastriate areas have been found to contain maps of the contralateral visual hemifield that are disorderly in the sense that the representation of various parts of the visual field are often misplaced or grossly over-or under-represented. It is suggested that this disorderlines may in some cases represent adaptations to facilitate certain types of visual functions.     

Multisensory integration in macaque visual cortex depends on cue reliability

Responses of multisensory neurons to combinations of sensory cues are generally enhanced or depressed relative to single cues presented alone, but the rules that govern these interactions have remained unclear. We examined integration of visual and vestibular self-motion cues in macaque area MSTd in response to unimodal as well as congruent and conflicting bimodal stimuli in order to evaluate hypothetical combination rules employed by multisensory neurons. Bimodal responses were well fit by weighted linear sums of unimodal responses, with weights typically less than one (subadditive). Surprisingly, our results indicate that weights change with the relative reliabilities of the two cues: visual weights decrease and vestibular weights increase when visual stimuli are degraded. Moreover, both modulation depth and neuronal discrimination thresholds improve for matched bimodal compared to unimodal stimuli, which might allow for increased neural sensitivity during multisensory stimulation. These findings establish important new constraints for neural models of cue integration.     

Unit responses of the squirrel visual cortex to shaped visual stimuli

Visual cortical unit responses of the squirrelSciurus vulgaris to shaped visual stimuli (stationary and moving spots and bands) were studied. Neurons responding selectively to the direction of stimulus movement and orientation of lines and those not responding selectively to these features were distinguished. Many neurons, whether responding selectively or not to movement direction, were specifically sensitive to high speeds of movement, of the order of hundreds of degrees per second. This selectivity in neurons responding selectively to movement direction persisted at these high speeds, despite the short time taken by the stimulus to move across the receptive field. Neurons responding selectively to line orientation were sensitive to lower speeds of stimulus movement — from units to tens of degrees per second. Neuronal sensitivity to high speeds of stimulus movement is achieved through rapid summation of excitation from large areas of the receptive field crossed by the fast-moving stimulus. Selectivity of the response to movement direction is produced under these conditions with the aid of directed short-latency inhibition, inhibiting unit activity for stimulus movement in "zero" direction.     

Two-dimensional substructure of stereo and motion interactions in macaque visual cortex

The analysis of object motion and stereoscopic depth are important tasks that are begun at early stages of the primate visual system. Using sparse white noise, we mapped the receptive field substructure of motion and disparity interactions in neurons in V1 and MT of alert monkeys. Interactions in both regions revealed subunits similar in structure to V1 simple cells. For both motion and stereo, the scale and shape of the receptive field substructure could be predicted from conventional tuning for bars or dot-field stimuli, indicating that the small-scale interactions were repeated across the receptive fields. We also found neurons in V1 and in MT that were tuned to combinations of spatial and temporal binocular disparities, suggesting a possible neural substrate for the perceptual Pulfrich phenomenon. Our observations constrain computational and developmental models of motion-stereo integration.