Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry

Cortical synchronization at gamma-frequencies (35-90 Hz) has been proposed to define the connectedness among the local parts of a perceived visual object. This hypothesis is still under debate. We tested it under conditions of binocular rivalry (BR), where a monkey perceived alternations among conflicting gratings presented singly to each eye at orthogonal orientations. We made multi-channel microelectrode recordings of multi-unit activity (MUA) and local field potentials (LFP) from striate cortex (V1) during BR while the monkey indicated his perception by pushing a lever. We analyzed spectral power and coherence of MUA and LFP over 4-90 Hz. As in previous work, coherence of gamma-signals in most pairs of recording locations strongly depended on grating orientation when stimuli were presented congruently in both eyes. With incongruent (rivalrous) stimulation LFP power was often consistently modulated in consonance with the perceptual state. This was not visible in MUA. These perception-related modulations of LFP occurred at low and medium frequencies (< 30 Hz), but not at gamma-frequencies. Perception-related modulations of LFP coherence were also restricted to the low-medium range. In conclusion, our results do not support the expectation that gamma-synchronization in V1 is related to the perceptual state during BR, but instead suggest a perception-related role of synchrony at low and medium frequencies.     

A computational model for the development of multiple maps in primary visual cortex

Primary visual cortex contains multiple maps of features of the visual scene, including visual field position, orientation, direction, ocular dominance and spatial frequency. The complex relationships between these maps provide clues to the strategies the cortex uses for representing and processing information. Here we simulate the combined development of all these map systems using a computational model, the elastic net. We show that this model robustly produces combined maps of these four variables that bear a close resemblance to experimental maps. In addition we show that the experimentally observed effects of monocular deprivation and single-orientation rearing can be reproduced in this model, and we make some testable predictions. These results provide strong support for the hypothesis that cortical representations attempt to optimize a trade-off between coverage and continuity.     

Irradiation of 850-nm laser light changes the neural activities in rat primary visual cortex

Although infrared laser was proven to be an alternative approach for neural stimulation, there is very little known about the neural response to infrared laser irradiation in visual cortex. This study is to investigate the effect of near-infrared laser irradiation on neural activities at the cortex level. A 850-nm pigtailed diode laser was applied to stimulate the rat primary visual cortex while the horizontal black and white stripe pattern was used as standard visual stimulation to evoke visual-evoked potential (VEP). Both amplitude and latency of VEP P100 was measured with or without infrared pulse stimulation applied in rat primary visual cortex. Paired t test and one-way analysis of variance were used to evaluate the impact of infrared irradiation and its pulse width on the amplitudes and latencies of P100, respectively. The results from our preliminary study revealed that, the pulsed near-infrared laser depressed the VEP amplitude and shortened the latency of P100; with the increment of pulse width of infrared irradiation, further decline of VEP amplitude and much shortened latency of P100 were observed. The present work suggests that near-infrared laser irradiation can alter the neural activities in primary visual cortex transiently, and could provide a novel contactless artificial neural stimulus to brain cortex with high spatial selectivity.     

Self-organization model of cytochrome oxidase blobs and ocular dominance columns in the primary visual cortex

There are regularly arranged blobs that contain neurons labeled by cytochrome oxidase (CO) in the supragranular layer of the primary visual cortex (V1) of monkeys and cats. This theoretical study demonstrates that CO-blob-like patterns can be reproduced based on the thermodynamic model for the activity-dependent self-organization of afferent inputs from two different groups of neurons to the supragranular layer of the visual cortex. Computer simulation based on the model shows that within a particular parameter range each blob is centered in the ocular dominance (OD) band, as observed in macaque monkeys and galagos. Furthermore, by increasing the strength of correlation in activity between inputs from the two eyes, nearby blobs merge across OD borders, as seen in the cat visual cortex. Finally, for monocular deprivation, blobs in the deprived eyes shrink as observed in monkeys and cats. For binocular deprivation, less intensely labeled blobs were reproduced, while the blob density did not change as observed in monkeys.     

Large-scale neural model for visual attention: integration of experimental single-cell and fMRI data

A computational neuroscience framework is proposed to better understand the role and the neuronal correlate of spatial attention modulation in visual perception. The model consists of several interconnected modules that can be related to the different areas of the dorsal and ventral paths of the visual cortex. Competitive neural interactions are implemented at both microscopic and interareal levels, according to the biased competition hypothesis. This hypothesis has been experimentally confirmed in studies in humans using functional magnetic resonance imaging (fMRI) techniques and also in single-cell recording studies in monkeys. Within this neuro-dynamical approach, numerical simulations are carried out that describe both the fMRI and the electrophysiological data. The proposed model draws together data of different spatial and temporal resolution, as are the above-mentioned imaging and single-cell results.     

A comparison of hemodynamic and neural responses in cat visual cortex using complex stimuli

We compare fMRI-BOLD responses in anesthetized cats with local field potentials (LFPs), aggregate high-frequency responses (analog-Mua) and spiking activity recorded in primary and higher visual cortex of alert animals. The similarity of the activations in these electrophysiological signals to those in the BOLD is quantified by counting recording sites where different stimuli elicit the same relative activation as in the imaging experiments. Using artificial stimuli, a comparison of BOLD and LFP strongly depends on the frequency range used. Stimulating with complex or natural stimuli reduces this frequency dependence and yields a good match of LFP and BOLD. In general, this match is best between 20 and 50 Hz. The measures of high-frequency activity behave qualitatively different: the responses of the analog-Mua match those of the LFP; the spiking activity shows a low concordance with the BOLD signal. This dissociation of BOLD and spiking activity is most prominent upon stimulation with natural stimuli.     

Representation of surface luminance and contrast in primary visual cortex

In visual perception, object identification requires both the ability to define regions of uniform luminance and zones of luminance contrast. Neural processes underlying contrast detection have been well studied, while those defining luminance remain poorly understood and controversial. Partially because stimuli comprised of uniform luminance are relatively ineffective in driving responses of cortical neurons, little effort has been made to systematically compare responses of individual neurons to both uniform luminance and contrast. Using large static uniform luminance and contrast stimuli, modulated temporally in luminance or contrast, we found a continuum of responses ranging from a few cells modulated only by luminance (luminance-only), to many cells modulated by both luminance and contrast (luminance-contrast), and to many others modulated only by contrast (contrast-only) in primary visual cortex. Moreover, luminance-contrast cells had broader orientation tuning, larger receptive field (RF) and lower spatial frequency Preference, on average, than contrast-only cells. Contrast-only cells had contrast responses more linearly correlated to the spatial structure of their RFs than luminance-contrast cells. Taken together these results suggest that luminance and contrast are represented, to some degree, by independent mechanisms that may be shaped by different classes of subcortical and/or cortical inputs.     

A study of pyramidal cell structure in the cingulate cortex of the macaque monkey with comparative notes on inferotemporal and primary visual cortex

Recent studies have revealed a marked degree of variation in the pyramidal cell phenotype in visual, somatosensory, motor and prefrontal cortical areas in the brain of different primates, which are believed to subserve specialized cortical function. In the present study we carried out comparisons of dendritic structure of layer III pyramidal cells in the anterior and posterior cingulate cortex and compared their structure with those sampled from inferotemporal cortex (IT) and the primary visual area (V1) in macaque monkeys. Cells were injected with Lucifer Yellow in flat-mounted cortical slices, and processed for a light-stable DAB reaction product. Size, branching pattern, and spine density of basal dendritic arbors was determined, and somal areas measured. We found that pyramidal cells in anterior cingulate cortex were more branched and more spinous than those in posterior cingulate cortex, and cells in both anterior and posterior cingulate were considerably larger, more branched, and more spinous than those in area V1. These data show that pyramidal cell structure differs between posterior dysgranular and anterior granular cingulate cortex, and that pyramidal neurons in cingulate cortex have different structure to those in many other cortical areas. These results provide further evidence for a parallel between structural and functional specialization in cortex.     

Organization of horizontal axons in the inferior temporal cortex and primary visual cortex of the macaque monkey

We investigated the organization of horizontal connections at two distinct hierarchical levels in the ventral visual cortical pathway of the monkey, the inferior temporal (TE) and primary visual (V1) cortices. After injections of anterograde tracers into layers 2 and 3, clusters of terminals ('patches') of labeled horizontal collaterals in TE appeared at various distances up to 8 mm from the injection site, while in V1 clear patches were distributed only within 2 mm. The size and spacing of these patches in TE were larger and more irregular than those observed in V1. The labeling intensity of patches in V1 declined sharply with distance from the injection site. This tendency was less obvious in TE; a number of densely labeled patches existed at distant sites beyond weakly labeled patches. While injections into both areas resulted in an elongated pattern of patches, the anisotropy was greater in TE than in V1 for injections of a similar size. Dual tracer injections and larger-sized injections further revealed that the adjacent sites in TE had spatially distinct horizontal projections, compared to those in V1. These area-specific characteristics of the horizontal connections may contribute to the differences in visual information processing of TE and V1.     

Representation and integration of auditory and visual stimuli in the primate ventral lateral prefrontal cortex

Through the influence of Goldman-Rakic, much research has been focused on the role of the dorsolateral prefrontal cortex in spatial working memory, decision making, and saccade generation, whereas functions of other parts of the frontal lobe including the ventrolateral prefrontal cortex (VLPFC) are less clear. Previous studies in non-human primates have shown that some VLPFC cells are selectively responsive to faces. Recent findings indicate that adjacent to the region where face- and object-selective cells have been recorded are neurons which respond to complex sounds including human and monkey vocalizations. Furthermore, when neurons in this same region are tested with combined face and voice communication stimuli, it is apparent that some cells in VLPFC are multisensory and respond to audiovisual stimuli. The determination that ventral prefrontal neurons are multisensory and responsive to auditory and visual communication stimuli may help to establish an animal model to assist in the investigation of the circuit and cellular basis of human communication. This will also aid in the understanding of general frontal lobe function and the processes that go awry in disorders including autism and schizophrenia, where disturbances in prefrontal function have been noted.     

The timing of perceptual decisions for ambiguous face stimuli in the human ventral visual cortex

When observers must discriminate a weak sensory signal in noise, early sensory areas seem to reflect the instantaneous strength of the sensory signal. In contrast, high-level parietal and prefrontal areas appear to integrate these signals over time with activity peaking at the time of the observer's decision. Here, we used functional magnetic resonance imaging to investigate how the brain forms perceptual decisions about complex visual forms in a challenging task, requiring the discrimination of ambiguous 2-tone Mooney faces and visually similar nonface images. Face-selective areas in the ventral visual cortex showed greater activity when subjects reported perceiving a face as compared with a nonface, even on error trials. More important, activity was closely related to the time of the subject's decision for face judgments, even on individual trials, and resembled the time course of activity in motor cortex corresponding to the subject's behavioral report. These results indicate that perceptual decisions about ambiguous face-like stimuli are reflected early in the sensorimotor pathway, in face-selective regions of the ventral visual cortex. Activity in these areas may represent a potential rate-limiting step in the pathway from sensation to action when subjects must reach a decision about ambiguous face-like stimuli.     

The intrinsic shape of human and macaque primary visual cortex

Previous studies have reported considerable variability in primary visual cortex (V1) shape in both humans and macaques. Here, we demonstrate that much of this variability is due to the pattern of cortical folds particular to an individual and that V1 shape is similar among individual humans and macaques as well as between these 2 species. Human V1 was imaged ex vivo using high-resolution (200 microm) magnetic resonance imaging at 7 T. Macaque V1 was identified in published histological serial section data. Manual tracings of the stria of Gennari were used to construct a V1 surface, which was computationally flattened with minimal metric distortion of the cortical surface. Accurate flattening allowed investigation of intrinsic geometric features of cortex, which are largely independent of the highly variable cortical folds. The intrinsic shape of V1 was found to be similar across human subjects using both nonparametric boundary matching and a simple elliptical shape model fit to the data and is very close to that of the macaque monkey. This result agrees with predictions derived from current models of V1 topography. In addition, V1 shape similarity suggests that similar developmental mechanisms are responsible for establishing V1 shape in these 2 species.     

Role of the ipsilateral primary motor cortex in controlling the timing of hand muscle recruitment

The precise contribution of the ipsilateral primary motor cortex (iM1) to hand movements remains controversial. To address this issue, we elicited transient virtual lesions of iM1 by means of transcranial magnetic stimulation (TMS) in healthy subjects performing either a grip-lift task or a step-tracking task with their right dominant hand. We found that, irrespective of the task, a virtual lesion of iM1 altered the timing of the muscle recruitment. In the grip-lift task, this led to a less coordinated sequence of grip and lift movements and in the step-tracking task, to a perturbation of the movement trajectory. In the step-tracking task, we have demonstrated that disrupting iM1 activity may, depending on the TMS delay, either advance or delay the muscle recruitment. The present study suggests that iM1 plays a critical role in hand movements by contributing to the setting of the muscle recruitment timing, most likely through either inhibitory or facilitatory transcallosal influences onto the contralateral M1 (cM1). iM1 would therefore contribute to shape precisely the muscular command originating from cM1.     

Descending projections from extrastriate visual cortex modulate responses of cells in primary auditory cortex

Primary sensory cortical responses are modulated by the presence or expectation of related sensory information in other modalities, but the sources of multimodal information and the cellular locus of this integration are unclear. We investigated the modulation of neural responses in the murine primary auditory cortical area Au1 by extrastriate visual cortex (V2). Projections from V2 to Au1 terminated in a classical descending/modulatory pattern, with highest density in layers 1, 2, 5, and 6. In brain slices, whole-cell recordings revealed long latency responses to stimulation in V2L that could modulate responses to subsequent white matter (WM) stimuli at latencies of 5-20 ms. Calcium responses imaged in Au1 cell populations showed that preceding WM with V2L stimulation modulated WM responses, with both summation and suppression observed. Modulation of WM responses was most evident for near-threshold WM stimuli. These data indicate that corticocortical projections from V2 contribute to multimodal integration in primary auditory cortex.     

The effects of aging on layer 1 of primary visual cortex in the rhesus monkey

The effect of age on layer 1 in primary visual cortex was determined in 19 rhesus monkeys of various ages. Twelve of the monkeys had been behaviorally tested. With age layer 1 becomes thinner and the glial limiting membrane becomes thicker. In the neuropil of layer 1 many of the dendrites in old monkeys appear to be degenerating and, as a consequence, electron micrographs from old monkeys display fewer dendritic and spine profiles per unit area than in young monkeys. As determined using both the disector and size-frequency methods, there is also a concomitant decrease in the numerical density of synapses with age. Although there is a significant correlation between the thinning of layer 1 in area 17 and age, there is no significant correlation between either the thinning of layer 1 or its loss of synapses and any of the behavioral measures of memory function obtained from the 12 behaviorally tested monkeys. Similar morphological changes with age occur in layer 1 of prefrontal cortex of these same monkeys, but in area 46 both the thinning of layer 1 and the loss of synapses show a significant correlation with behavioral measures of memory function. These differences between layer 1 in these two cortical areas presumably relate to the fact that prefrontal cortex has a greater role in subserving cognition than does primary visual cortex.     

Strabismic suppression is mediated by inhibitory interactions in the primary visual cortex

Most strabismic observers do not suffer from double vision because of suppression from conscious perception of 1 of the 2 eyes' conflicting views. Direct evidence for the site and neural substrate of strabismic suppression has not been available so far, although psychophysical data suggest a cortical origin. On the other hand, cross-orientation suppression among conflicting stimuli presented monocularly has recently been shown to have a strong thalamic component. Here we present evidence, using both visual stimulation and pharmacological techniques, that strabismic suppression occurs in the primary visual cortex and involves gamma-amino butyric acid (GABA)-mediated inhibition. We show that its dependency on the drift rate of the suppressing stimulus is consistent with a cortical origin; unlike monocular cross-orientation suppression, it cannot be evoked by very fast-moving stimuli. Furthermore, strabismic suppression is greatly reduced when GABAergic inhibition is locally blocked by the GABA(A) antagonist bicuculline.     

Loss of neurofilament labeling in the primary visual cortex of monocularly deprived monkeys

Visual experience during early life is important for the development of neural organizations that support visual function. Closing one eye (monocular deprivation) during this sensitive period can cause a reorganization of neural connections within the visual system that leaves the deprived eye functionally disconnected. We have assessed the pattern of neurofilament labeling in monocularly deprived macaque monkeys to examine the possibility that a cytoskeleton change contributes to deprivation-induced reorganization of neural connections within the primary visual cortex (V-1). Monocular deprivation for three months starting around the time of birth caused a significant loss of neurofilament labeling within deprived-eye ocular dominance columns. Three months of monocular deprivation initiated in adulthood did not produce a loss of neurofilament labeling. The evidence that neurofilament loss was found only when deprivation occurred during the sensitive period supports the notion that the loss permits restructuring of deprived-eye neural connections within the visual system. These results provide evidence that, in addition to reorganization of LGN inputs, the intrinsic circuitry of V-1 neurons is altered when monocular deprivation occurs early in development.     

A neural model of how horizontal and interlaminar connections of visual cortex develop into adult circuits that carry out perceptual grouping and learning

A neural model suggests how horizontal and interlaminar connections in visual cortical areas V1 and V2 develop within a laminar cortical architecture and give rise to adult visual percepts. The model suggests how mechanisms that control cortical development in the infant lead to properties of adult cortical anatomy, neurophysiology and visual perception. The model clarifies how excitatory and inhibitory connections can develop stably by maintaining a balance between excitation and inhibition. The growth of long-range excitatory horizontal connections between layer 2/3 pyramidal cells is balanced against that of short-range disynaptic interneuronal connections. The growth of excitatory on-center connections from layer 6-to-4 is balanced against that of inhibitory interneuronal off-surround connections. These balanced connections interact via intracortical and intercortical feedback to realize properties of perceptual grouping, attention and perceptual learning in the adult, and help to explain the observed variability in the number and temporal distribution of spikes emitted by cortical neurons. The model replicates cortical point spread functions and psychophysical data on the strength of real and illusory contours. The on-center, off-surround layer 6-to-4 circuit enables top-down attentional signals from area V2 to modulate, or attentionally prime, layer 4 cells in area V1 without fully activating them. This modulatory circuit also enables adult perceptual learning within cortical area V1 and V2 to proceed in a stable way.     

Connectivity of GABAergic calretinin-immunoreactive neurons in rat primary visual cortex.

In rat visual cortex neurons that are immunoreactive for the calcium-binding protein calretinin (CR+) constitute a distinct family which accounts for 17% of gamma-aminobutyric acid (GABA)-expressing cells. It is not clear, however, (i) whether CR is expressed exclusively in GABAergic neurons and (ii) how CR+ neurons are incorporated into neuronal circuits of rat visual cortex. To address these questions we studied synaptic relationships of CR+ neurons with GABA+ and GABA- elements in the neuropil of rat primary visual cortex (area 17). All CR+ neurons are nonpyramidal cells with smooth or sparsely spiny and often beaded dendrites. Of all CR+ neurons, 56% are located in layers 1 and 2/3. In layer 2/3, most CR+ neurons are bipolar-shaped and have vertically oriented dendrites. Many ascending dendritic branches reach layer 1 where they run parallel to pial surface. CR+ axons are thin, highly branched near the cell body and often send descending collaterals to layers 5 and 6. Double immunofluorescence labeling revealed GABA in 94% of CR+ cell bodies in layer 2/3. Electron microscopic analysis shows that all CR+ axon terminals contain elongated vesicles and form symmetric synapses. Postembedding staining shows that 98% of CR+ terminals are GABA+. GABA-immunoreactivity is also present in somata and thick dendrites of CR+ neurons but many thin dendrites are GABA-. CR+ somata, dendrites and axon terminals are enriched in mitochondria. Somata and thick CR+ dendrites are densely innervated. At least 68% of the targets of CR+ terminals in layer 2/3 are GABA+ and > or = 50% of these are other CR+ neurons. The remainder (32%) of targets of CR+ terminals are thin dendrites of GABA- cells. In contrast, in layers 5 and 6, 60% of CR+ terminals form synapses with GABA- somatic profiles. The preferential interactions of layer 2/3 CR+ neurons with GABAergic neurons, and with CR+ neurons in particular, suggests that these cells play a role in the inhibition of inhibitory neurons of the same layer. Through these interactions CR+ cells may reduce inhibition of pyramidal cells in layers 2/3, 5 and 6 and thus disinhibit a column of neurons.