Cortical synchronization suggests neural principles of visual feature grouping

Compositions of visual scenes are related here to neural signals in visual cortex and to cortical circuit models to understand neural mechanisms of perceptual feature grouping. Starting from the hypothesis that synchronization and decoupling of cortical gamma-activities (35-90 Hz) define the relations among visual objects, we concentrate on synchronization related to (1) static retinal stimulation during ocular fixation, and (2) transient stimulation by sudden shifts in object position. The synchronization hypothesis has been tested by analyzing signal correlations in visual cortex of monkeys with the following results: Static retinal stimuli induce loosely phase-coupled gamma-activities among neurons of an object's cortical representation. Patches of gamma-synchronization become decoupled across the representation of an object's contour, and thereby can code figure-ground segregation. Transient stimuli evoke synchronized volleys of stimulus-locked activities that are typically non-rhythmic and include low frequency components in addition to those in the gamma-range. It is argued that stimulus-induced and stimulus-locked synchronizations may play different roles in perceptual feature grouping.     

Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance

Short-term memory requires communication between multiple brain regions that collectively mediate the encoding and maintenance of sensory information. It has been suggested that oscillatory synchronization underlies intercortical communication. Yet, whether and how distant cortical areas cooperate during visual memory remains elusive. We examined neural interactions between visual area V4 and the lateral prefrontal cortex using simultaneous local field potential (LFP) recordings and single-unit activity (SUA) in monkeys performing a visual short-term memory task. During the memory period, we observed enhanced between-area phase synchronization in theta frequencies (3-9 Hz) of LFPs together with elevated phase locking of SUA to theta oscillations across regions. In addition, we found that the strength of intercortical locking was predictive of the animals' behavioral performance. This suggests that theta-band synchronization coordinates action potential communication between V4 and prefrontal cortex that may contribute to the maintenance of visual short-term memories.     

Suppressive effects of receptive field surround on neuronal activity in the cat primary visual cortex

Effects of sinusoidal grating stimulus presented outside the classical receptive field (CRF) on neuronal responses were studied in the primary visual cortex of anaesthetized cats. Among 101 cells electrophysiologically recorded, the predominant effect of the stimulus in the receptive field surround (SRF) was the suppression of responses to the CRF stimulation, and the SRF grating suppressed them up to 56% of the responses (44% suppression) to the CRF stimulus alone. The strong suppression was observed more often in layer II/III cells than in other layers and in complex cells more often than in simple cells. The modulatory effects by SRF stimulus might be enhanced by the cortical recurrent excitation particularly in the superficial layers. We also examined whether the modulation by the surround grating exhibits a differential effect according to the presence or absence of figure-ground segregation in the stimulus configuration. For this purpose, effects of stimulus configuration with orientation-, direction-contrast or relative spatial phase difference between CRF and SRF stimuli (figure-ground segregated configuration) were compared with those of uniform configuration of stimulus (non-segregated configuration). There was a population of cells, which exhibited significantly stronger suppression with non-segregated configuration than with figure-ground segregated configuration. Such differential modulation of response by the SRF stimulus in the primary visual cortex is a possible basis of perceptual figure-ground segregation.     

Neural coding of temporal information in auditory thalamus and cortex

How the brain processes temporal information embedded in sounds is a core question in auditory research. This article synthesizes recent studies from our laboratory regarding neural representations of time-varying signals in auditory cortex and thalamus in awake marmoset monkeys. Findings from these studies show that 1) the primary auditory cortex (A1) uses a temporal representation to encode slowly varying acoustic signals and a firing rate-based representation to encode rapidly changing acoustic signals, 2) the dual temporal-rate representations in A1 represent a progressive transformation from the auditory thalamus, 3) firing rate-based representations in the form of monotonic rate-code are also found to encode slow temporal repetitions in the range of acoustic flutter in A1 and more prevalently in the cortical fields rostral to A1 in the core region of marmoset auditory cortex, suggesting further temporal-to-rate transformations in higher cortical areas. These findings indicate that the auditory cortex forms internal representations of temporal characteristics of sounds that are no longer faithful replicas of their acoustic structures. We suggest that such transformations are necessary for the auditory cortex to perform a wide range of functions including sound segmentation, object processing and multi-sensory integration.     

Neural coding of temporal information in auditory thalamus and cortex

How the brain processes temporal information embedded in sounds is a core question in auditory research. This article synthesizes recent studies from our laboratory regarding neural representations of time-varying signals in auditory cortex and thalamus in awake marmoset monkeys. Findings from these studies show that 1) the primary auditory cortex (A1) uses a temporal representation to encode slowly varying acoustic signals and a firing rate–based representation to encode rapidly changing acoustic signals, 2) the dual temporal-rate representations in A1 represent a progressive transformation from the auditory thalamus, 3) firing rate–based representations in the form of a monotonic rate-code are also found to encode slow temporal repetitions in the range of acoustic flutter in A1 and more prevalently in the cortical fields rostral to A1 in the core region of marmoset auditory cortex, suggesting further temporal-to-rate transformations in higher cortical areas. These findings indicate that the auditory cortex forms internal representations of temporal characteristics of sounds that are no longer faithful replicas of their acoustic structures. We suggest that such transformations are necessary for the auditory cortex to perform a wide range of functions including sound segmentation, object processing and multi-sensory integration.     

Privileged coding of convex shapes in human object-selective cortex

What is the neural code for object shape? Despite intensive research, the precise nature of object representations in high-level visual cortex remains elusive. Here we use functional magnetic resonance imaging (fMRI) to show that convex shapes are encoded in a privileged fashion by human lateral occipital complex (LOC), a region that has been implicated in object recognition. On each trial, two convex or two concave shapes that were either identical or different were presented sequentially. Critically, the convex and concave stimuli were the same except for a binocular disparity change that reversed the figure-ground assignment. The fMRI response in LOC for convex stimuli was higher for different than that for identical shape pairs, indicating sensitivity to differences in convex shape. However, when the same stimuli were seen as concave, the response for different and identical pairs was the same, indicating lower sensitivity to changes in concave shape than convex shape. This pattern was more pronounced in the anterior than that in the posterior portion of LOC. These results suggest that convex contours could be important elements in cortical object representations.     

Neuronal responses from beyond the classic receptive field in V1 of alert monkeys

Responses of primary visual cortex (V1) neurons to stimuli inside the classic receptive field (CRF) can be modulated by stimuli outside the CRF. We recently reported that responses of most V1 neurons to a line in the CRF center are inhibited by large surround-stimuli and that this modulation is stimulus selective. Here we report that a significant proportion of V1 neurons in alert monkeys respond directly to stimuli outside the CRF with very long latency and much reduced selectivity. When surround stimuli are presented alone, three response patterns can be distinguished in 153 single- or multiunits tested: (1) 31.4% have no significant response; (2) 50.3% show excitatory responses that are significantly higher than spontaneous activity. The average latency of these responses is about 145 ms, 2–3 times longer than center responses; (3) 18.3% show suppressed spontaneous activity after stimulus onset. The direct surround responses are found to be only weakly selective for the orientation of contextual lines, and not selective for other contextual patterns tested. While the outburst of responses to stimuli within the CRF is not affected by reducing stimulus duration from 500 ms to 50 ms, late excitatory surround responses are virtually eliminated. We propose that the late excitatory surround responses to extra-CRF stimulation alone are the reflection of feedback from higher cortical areas and may contribute to reduced contextual inhibition of cells in V1. This could play a role in figure-ground segregation. Electronic Publication     

A neural model of figure-ground organization

Psychophysical studies suggest that figure-ground organization is a largely autonomous process that guides--and thus precedes--allocation of attention and object recognition. The discovery of border-ownership representation in single neurons of early visual cortex has confirmed this view. Recent theoretical studies have demonstrated that border-ownership assignment can be modeled as a process of self-organization by lateral interactions within V2 cortex. However, the mechanism proposed relies on propagation of signals through horizontal fibers, which would result in increasing delays of the border-ownership signal with increasing size of the visual stimulus, in contradiction with experimental findings. It also remains unclear how the resulting border-ownership representation would interact with attention mechanisms to guide further processing. Here we present a model of border-ownership coding based on dedicated neural circuits for contour grouping that produce border-ownership assignment and also provide handles for mechanisms of selective attention. The results are consistent with neurophysiological and psychophysical findings. The model makes predictions about the hypothetical grouping circuits and the role of feedback between cortical areas.     

Working memory for visual objects: complementary roles of inferior temporal, medial temporal, and prefrontal cortex

Humans have an extraordinary ability to maintain and manipulate visual image information in the absence of perceptual stimulation. The neural substrates of visual working memory have been extensively researched, but there have been few attempts to integrate these findings into a model of how different cortical areas interact to form and maintain visual memories. In this paper, I review findings from neurophysiological, neuropsychological, and neuroimaging studies of visual working memory in human and nonhuman primates. These data support a model in which visual working memory operations rely on activation of object representations in inferior temporal cortex, via top-down feedback from neocortical areas in the prefrontal and medial temporal cortex, and also from the hippocampus.     

Dissociation of spatial-, object-, and sound-coding neurons in the mediodorsal nucleus of the primate thalamus

The mediodorsal nucleus (MD) is the thalamic gateway to the prefrontal cortex, an area of the brain associated with spatial and object working memory functions. We have recorded single-neuron activities from the MD nucleus in monkeys trained to perform spatial tasks with peripheral visual stimuli and a nonspatial task with foveally presented pictures of objects and faces-tasks identical to those we have previously used to map regional specializations in the dorso- and ventro-lateral prefrontal cortex, respectively. We found that MD neurons exhibited categorical specificity-either responding selectively to locations in the spatial tasks or preferentially to specific representations of faces and objects in the nonspatial task. Spatially tuned neurons were located in parts of the MD connected with the dorsolateral prefrontal cortex while neurons responding to the identity of stimuli mainly occupied more ventral positions in the nucleus that has its connections with the inferior prefrontal convexity. Neuronal responses to auditory stimuli were also examined, and vocalization sensitive neurons were found in more posterior portions of the MD. We conclude that MD neurons are dissociable by their spatial and nonspatial coding properties in line with their cortical connections and that the principle of information segregation in cortico-cortical pathways extends to the "association" nuclei of the thalamus.     

Shape-coding in IT cells generalizes over contrast and mirror reversal, but not figure-ground reversal

We assessed how the visual shape preferences of neurons in the inferior temporal cortex of awake, behaving monkeys generalized across three different stimulus transformations. Stimulus-preferences of particular cells among different polygon displays were correlated across reversed contrast polarity or mirror reversal, but not across figure-ground reversal. This corresponds with psychological findings on human shape judgments. Our results imply that neurons in inferior temporal cortex respond to components of visual shape derived only after figure-ground assignment of contours, not to the contours themselves.     

Cortical and subcortical influences on the nucleus of the optic tract of the opossum

In the present work we propose a new phylogenetic hypothesis for the role played by cortical and subcortical afferents to the nucleus of the optical tract, the main visual relay station of the horizontal optokinetic reflex in mammals. The hypothesis is supported by anatomical and physiological data obtained in the South American opossum (Didelphis aurita) using the following experimental approaches: (i) single-unit recordings in the nucleus of the optic tract and simultaneous electrical stimulation of the contralateral nucleus of the optic tract; (ii) single-unit recordings in the nucleus of the optic tract and simultaneous electrical stimulation of the ipsilateral striate cortex; (iii) injection of cholera toxin subunit B into the striate cortex and subsequent immunohistochemical reaction to reveal the presence of the marker in the thalamus and mesencephalon; and (iv) single-unit recordings in the nucleus of the optic tract both before and after ablation of the ipsilateral visual cortex. The main results are: (i) there is a strong inhibitory reciprocal effect upon the nucleus of the optic tract following stimulation of its contralateral counterpart; (ii) electrophysiological and anatomical data imply that the visual cortex does not project directly to the nucleus of the optic tract. Rather, cortical terminals seem to target the nearby anterior and posterior pretectal nuclei and orthodromic latencies in the nucleus of the optic tract following stimulation of the visual cortex were twice as large as in the superior colicullus; and (iii) ablation of the entire visual cortex did not have any effect upon binocularity of cells in the nucleus of the optic tract. These results strengthen the model proposed here for the role of the interactions between the nuclei of the optic tract under optokinetic stimulation. The hypothesis in the present work is that the cortical influences upon the nucleus of the optical tract, in addition to the subcortical ones, appeared only recently in phylogenesis. In more primitive mammals, such as the opossum, subcortical interactions are thought to play a relatively important role. With the emergence of retinal specializations, such as the fovea, one might suppose that there followed the appearance of new ocular movements, such as the smooth pursuit and certain types of saccades, that came to join the pre-existent optokinetic reflex.     

Role of GABAB receptor-mediated inhibition in reciprocal interareal pathways of rat visual cortex

In neocortex, synaptic inhibition is mediated by gamma-aminobutyric acid-A (GABAA) and GABAB receptors. By using intracellular and patch-clamp recordings in slices of rat visual cortex we studied the balance of excitation and inhibition in different intracortical pathways. The study was focused on the strength of fast GABAA- and slow GABAB-mediated inhibition in interareal forward and feedback connections between area 17 and the secondary, latero-medial visual area (LM). Our results demonstrate that in most layer 2/3 neurons forward inputs elicited excitatory postsynaptic potentials (EPSPs) that were followed by fast GABAA- and slow GABAB-mediated hyperpolarizing inhibitory postsynaptic potentials (IPSPs). These responses resembled those elicited by horizontal connections within area 17 and those evoked by stimulation of the layer 6/white matter border. In contrast, in the feedback pathway hyperpolarizing fast and slow IPSPs were rare. However weak fast and slow IPSPs were unmasked by bath application of GABAB receptor antagonists. Because in the feedback pathway disynaptic fast and slow IPSPs were rare, polysynaptic EPSPs were more frequent than in forward, horizontal, and interlaminar circuits and were activated over a broader stimulus range. In addition, in the feedback pathway large-amplitude polysynaptic EPSPs were longer lasting and showed a late component whose onset coincided with that of slow IPSPs. In the forward pathway these late EPSPs were only seen with stimulus intensities that were below the activation threshold of slow IPSPs. Unlike strong forward inputs, feedback stimuli of a wide range of intensities increased the rate of ongoing neuronal firing. Thus, when forward and feedback inputs are simultaneously active, feedback inputs may provide late polysynaptic excitation that can offset slow IPSPs evoked by forward inputs and in turn may promote recurrent excitation through local intracolumnar circuits. This may provide a mechanism by which feedback inputs from higher cortical areas can amplify afferent signals in lower areas.     

Perceptual continuity and the emergence of perceptual persistence in the ventral visual pathway

Perceptual continuity is an important aspect of our experience of the visual world. In this study, we focus on an example of perceptual continuity involving the maintenance of figure-ground segregation despite the removal of binding cues that initiated the segregation. Fragmented line drawings of objects were superimposed on a background of randomly oriented lines. Global forms could be discriminated from the background based on differences in motion or differences in color/brightness. Furthermore, perception of a global form persisted after the binding cue had been removed. A comparison between the persistence of forms constructed from motion or color demonstrated that both forms produced persistence after the object defining cues were removed. Functional imaging showed a gradual increase in the persistence of brain activity in the lower visual areas (V1, V2, VP), which reached significance in V4v and peaked in the lateral occipital area. There was no difference in the location of persistence for color- or motion-defined forms. These results suggest that the retention of a global percept is an emerging property of the ventral visual processing stream and the maintenance of grouped visual elements is independent of cue type. We postulated that perceptual persistence depends on a system of perceptual memory reflecting the state of perceptual organization.     

Inter-trial neuronal activity in inferior temporal cortex: a putative vehicle to generate long-term visual associations

When monkeys perform a delayed match-to-sample task, some neurons in the anterior inferotemporal cortex show sustained activity following the presentation of specific visual stimuli, typically only those that are shown repeatedly. When sample stimuli are shown in a fixed temporal order, the few images that evoke delay activity in a given neuron are often neighboring stimuli in the sequence, suggesting that this delay activity may be the neural correlate of associative long-term memory. Here we report that stimulus-selective sustained activity is also evident following the presentation of the test stimulus in the same task. We use a neural network model to demonstrate that persistent stimulus-selective activity across the intertrial interval can lead to similar mnemonic representations (distributions of delay activity across the neural population) for neighboring visual stimuli. Thus, inferotemporal cortex may contain neural machinery for generating long-term stimulus-stimulus associations.     

Visceral signals reach visual cortex during slow wave sleep: study in monkeys

Propagation of signals from the gastro-intestinal system towards the occipital cortex within sleep-wake cycle was investigated in three monkeys used in the study of sleep impairment in a chronic MPTP model of parkinsonism. The monkeys differed in motor abilities and sleep structure. e animal (M1) was non-motor disabled and had no sleep alterations. The other two monkeys were severely motor affected, but one (M2) had normal sleep cycles; meanwhile, the other (M3) had no complete sleep cycles. To evaluate the level of sleep and to record cortical evoked responses screw electrodes were implanted over the occipital cortex. Two hours before overnight recordings, two hook electrodes were injected intraperitoneally (under light Ketanest anesthesia) and anchored in gut. Using these electrodes, electric stimulation was applied during slow wave sleep, and in wakefulness. Cortical evoked responses to intraperitoneal stimulation were found indeed during sleep in experiments with M1 and M2. These results show that also in primates with normal sleep pattern visceral information is transferred to the cerebral cortex during slow wave sleep.     

Cross-correlation study of the temporal interactions between areas V1 and V2 of the macaque monkey

Cross-correlation studies performed in cat visual cortex have shown that neurons in different cortical areas of the same hemisphere or in corresponding areas of opposite hemispheres tend to synchronize their activities. The presence of synchronization may be related to the parallel organization of the cat visual system, in which different cortical areas can be activated in parallel from the lateral geniculate nucleus. We wanted to determine whether interareal synchronization of firing can also be observed in the monkey, in which cortical areas are thought to be organized in a hierarchy spanning different levels. Cross-correlation histograms (CCHs) were calculated from pairs of single or pairs of multiunit activities simultaneously recorded in areas V1 and V2 of paralyzed and anesthetized macaque monkeys. Moving bars and flashed bars were used as stimuli. The shift predictor was calculated and subtracted from the raw CCH to reveal interactions of neuronal origin in isolation. Significant CCH peaks, indicating interactions of neuronal origin, were obtained in 11% of the dual single-unit recordings and 46% of the dual multiunit recordings with moving bars. The incidence of nonflat CCHs with flashed bars was 29 and 78%, respectively. For the pairs of recording sites where both flashed and moving stimuli were used, the incidences of significant CCHs were very similar. Three types of peaks were distinguished on the basis of their width at half-height: T (<16 ms), C (between 16 and 180 ms), and H peaks (>180 ms). T peaks were very rarely observed (<1% in single-unit recordings). H peaks were observed in 7-16% of the single-unit CCHs, and C peaks in 6-16%, depending on the stimulus used. C and H peaks were observed more often when the receptive fields were overlapping or distant by <2 degrees. To test for the presence of synchronization between neurons in areas V1 and V2, we measured the position of the CCH peak with respect to the origin of the time axis of the CCH. Only in the case of a few T peaks did we find displaced peaks, indicating a possible drive of the V2 neuron by the simultaneously recorded V1 cell. All the other peaks were either centered on the origin or overlapped the origin of time with their upper halves. Thus similarly to what has been reported for the cat, neurons belonging to different cortical areas in the monkey tend to synchronize the time of emission of their action potentials with three different levels of temporal precision. For peaks calculated from flashed stimuli, we compared the peak position with the difference between latencies of V1 and V2 neurons. There was a clear correlation for single-unit pairs in the case of C peaks. Thus the position of a C peak on the time axis appears to reflect the order of visual activation of the correlated neurons. The coupling strength for H peaks was smaller during visual drive compared with spontaneous activity. On the contrary, C peaks were seen more often and were stronger during visual stimulation than during spontaneous activity. This suggests that C-type synchronization is associated with the processing of visual information. The origin of synchronized activity in a serially organized system is discussed.     

Supplementary motor area encodes reward expectancy in eye-movement tasks

Neural activity signifying the expectation of reward has been found recently in many parts of the brain, including midbrain and cortical structures. These signals can facilitate goal-directed behavior or the learning of new skills based on reinforcements. Here we show that neurons in the supplementary motor area (SMA), an area concerned with movements of the body and limbs, also carry a reward expectancy signal in the postsaccadic period of oculomotor tasks. While the monkeys performed blocks of memory-guided and object-based saccades, the neurons discharged a burst after a approximately 200-ms delay following the target-acquiring saccade in the memory task but often fired concurrently with the target-acquiring saccade in the object task. The hypothesis that this postsaccadic bursting activity reflects the expectation of a reward was tested with a series of manipulations to the memory-guided saccade task. It was found that although the timing of the bursting activity corresponds to a visual feedback stimulus, the visual feedback is not required for the neurons to discharge a burst. Second, blocks of no-reward trials reveal an extinction of the bursting activity as the monkeys come to understand that they would not be rewarded for properly generated saccades. Finally, the delivery of unexpected rewards confirmed that in many of the neurons, the activity is not related to a motor plan to acquire the reward (e.g., licking). Thus we conclude that reward expectancy is represented by the activity of SMA neurons, even in the context of an oculomotor task. These results suggest that the reward expectancy signal is broadcast over a large extent of motor cortex, and may facilitate the learning of new, coordinated behavior between different body parts.     

Convergence of unimodal and polymodal sensory input to the entorhinal cortex in the fascicularis monkey

The hippocampal formation is a key structure in memory formation and consolidation. The hippocampus receives information from different cortical and subcortical sources. Cortical information is mostly funneled to the hippocampus through the entorhinal cortex (EC) in a bi-directional way that ultimately ends in the cortex. Retrograde tracing studies in the nonhuman primate indicate that more than two-thirds of the cortical afferents to the EC come from polymodal sensory association areas. Although some evidence for the projection from visual unimodal cortex to the EC exists, inputs from other visual and auditory unimodal association areas, and the possibility of their convergence with polymodal input in the EC remains largely undisclosed. We studied 10 Macaca fascicularis monkeys in which cortical deposits of the anterograde tracer biotinylated dextran-amine were made into different portions of visual and auditory unimodal association cortices in the temporal lobe, and in polymodal association cortex at the upper bank of the superior temporal sulcus. Visual and auditory unimodal as well as polymodal cortical areas projected to the EC. Both visual unimodal and polymodal association cortices presented dense projections, while those from unimodal auditory association cortex were more patchy and less dense. In all instances, the projection distributed in both the superficial and deep layers of the EC. However, while polymodal cortex projected to all layers (including layer I), visual unimodal cortex did not project to layer I, and auditory unimodal cortex projected less densely, scattered through all layers. Topographically, convergence from the three cortical areas studied can be observed in the lateral rostral and lateral caudal subfields. The present study suggests that unimodal and polymodal association cortical inputs converge in the lateral EC, thereby providing the possibility for the integration of complex stimuli for internal representations in declarative memory elaboration.     

Visual cortex maps are optimized for uniform coverage

Cat visual cortex contains a topographic map of visual space, plus superimposed, spatially periodic maps of ocular dominance, spatial frequency and orientation. It is hypothesized that the layout of these maps is determined by two constraints: continuity or smooth mapping of stimulus properties across the cortical surface, and coverage uniformity or uniform representation of combinations of map features over visual space. Here we use a quantitative measure of coverage uniformity (c') to test the hypothesis that cortical maps are optimized for coverage. When we perturbed the spatial relationships between ocular dominance, spatial frequency and orientation maps obtained in single regions of cortex, we found that cortical maps are at a local minimum for c'. This suggests that coverage optimization is an important organizing principle governing cortical map development.