Implications on visual apperception: Energy, duration, structure and synchronization

Although primary visual cortex (V1 or striate) activity per se is not sufficient for visual apperception (normal conscious visual experiences and conscious functions such as detection, discrimination, and recognition), the same is also true for extrastriate visual areas (such as V2, V3, V4/V8/VO, V5/M5/MST, IT, and GF). In the lack of V1 area, visual signals can still reach several extrastriate parts but appear incapable of generating normal conscious visual experiences. It is scarcely emphasized in the scientific literature that conscious perceptions and representations must have also essential energetic conditions. These energetic conditions are achieved by spatiotemporal networks of dynamic mitochondrial distributions inside neurons. However, the highest density of neurons in neocortex (number of neurons per degree of visual angle) devoted to representing the visual field is found in retinotopic V1. It means that the highest mitochondrial (energetic) activity can be achieved in mitochondrial cytochrome oxidase-rich V1 areas. Thus, V1 bear the highest energy allocation for visual representation.In addition, the conscious perceptions also demand structural conditions, presence of adequate duration of information representation, and synchronized neural processes and/or ‘interactive hierarchical structuralism.’ For visual apperception, various visual areas are involved depending on context such as stimulus characteristics such as color, form/shape, motion, and other features. Here, we focus primarily on V1 where specific mitochondrial-rich retinotopic structures are found; we will concisely discuss V2 where smaller riches of these structures are found. We also point out that residual brain states are not fully reflected in active neural patterns after visual perception. Namely, after visual perception, subliminal residual states are not being reflected in passive neural recording techniques, but require active stimulation to be revealed.     

Neuronal discharges and gamma oscillations explicitly reflect visual consciousness in the lateral prefrontal cortex

Neuronal discharges in the primate temporal lobe, but not in the striate and extrastriate cortex, reliably reflect stimulus awareness. However, it is not clear whether visual consciousness should be uniquely localized in the temporal association cortex. Here we used binocular flash suppression to investigate whether visual awareness is also explicitly reflected in feature-selective neural activity of the macaque lateral prefrontal cortex (LPFC), a cortical area reciprocally connected to the temporal lobe. We show that neuronal discharges in the majority of single units and recording sites in the LPFC follow the phenomenal perception of a preferred stimulus. Furthermore, visual awareness is reliably reflected in the power modulation of high-frequency (>50?Hz) local field potentials in sites where spiking activity is found to be perceptually modulated. Our results suggest that the activity of neuronal populations in at least two association cortical areas represents the content of conscious visual perception.     

Neuroimaging of visual awareness in patients and normal subjects

The immediacy and directness of our visual experience belies the complexity of the underlying neural mechanisms, which remain incompletely understood. Recent neuroimaging studies suggest that activity in ventral visual cortex is necessary but not sufficient for visual awareness. Experiments in both patients and normal subjects indicate that parietal and frontal areas make an important contribution to visual awareness, suggesting that reciprocal interactions between dorsal frontoparietal areas and ventral visual cortex may provide a fundamental neural substrate for conscious visual experience.     

Peripheral variability and central constancy in mammalian visual system evolution

Neural systems are necessarily the adaptive products of natural selection, but a neural system, dedicated to any particular function in a complex brain, may be composed of components that covary with functionally unrelated systems, owing to constraints beyond immediate functional requirements. Some studies support a modular or mosaic organization of the brain, whereas others emphasize coordination and covariation. To contrast these views, we have analysed the retina, striate cortex (V1) and extrastriate cortex (V2, V3, MT, etc.) in 30 mammals, examining the area of the neocortex and individual neocortical areas and the relative numbers of rods and cones. Controlling for brain size and species relatedness, the sizes of visual cortical areas (striate, extrastriate) within the brains of nocturnal and diurnal mammals are not statistically different from one another. The relative sizes of all cortical areas, visual, somatosensory and auditory, are best predicted by the total size of the neocortex. In the sensory periphery, the retina is clearly specialized for niche. New data on rod and cone numbers in various New World primates confirm that rod and cone complements of the retina vary substantially between nocturnal and diurnal species. Although peripheral specializations or receptor surfaces may be highly susceptible to niche-specific selection pressures, the areal divisions of the cerebral cortex are considerably more conservative.     

Primary visual cortex activity along the apparent-motion trace reflects illusory perception

The illusion of apparent motion can be induced when visual stimuli are successively presented at different locations. It has been shown in previous studies that motion-sensitive regions in extrastriate cortex are relevant for the processing of apparent motion, but it is unclear whether primary visual cortex (V1) is also involved in the representation of the illusory motion path. We investigated, in human subjects, apparent-motion-related activity in patches of V1 representing locations along the path of illusory stimulus motion using functional magnetic resonance imaging. Here we show that apparent motion caused a blood-oxygenation-level-dependent response along the V1 representations of the apparent-motion path, including regions that were not directly activated by the apparent-motion-inducing stimuli. This response was unaltered when participants had to perform an attention-demanding task that diverted their attention away from the stimulus. With a bistable motion quartet, we confirmed that the activity was related to the conscious perception of movement. Our data suggest that V1 is part of the network that represents the illusory path of apparent motion. The activation in V1 can be explained either by lateral interactions within V1 or by feedback mechanisms from higher visual areas, especially the motion-sensitive human MT/V5 complex.     

Computations in the early visual cortex.

This paper reviews some of the recent neurophysiological studies that explore the variety of visual computations in the early visual cortex in relation to geometric inference, i.e. the inference of contours, surfaces and shapes. It attempts to draw connections between ideas from computational vision and findings from awake primate electrophysiology. In the classical feed-forward, modular view of visual processing, the early visual areas (LGN, V1 and V2) are modules that serve to extract local features, while higher extrastriate areas are responsible for shape inference and invariant object recognition. However, recent findings in primate early visual systems reveal that the computations in the early visual cortex are rather complex and dynamic, as well as interactive and plastic, subject to influence from global context, higher order perceptual inference, task requirement and behavioral experience. The evidence argues that the early visual cortex does not merely participate in the first stage of visual processing, but is involved in many levels of visual computation.     

Conscious awareness of flicker in humans involves frontal and parietal cortex

Even when confined to the same spatial location, flickering and steady light evoke very different conscious experiences because of their distinct temporal patterns. The neural basis of such differences in subjective experience remains uncertain . Here, we used functional MRI in humans to examine the neural structures involved in awareness of flicker. Participants viewed a single point source of light that flickered at the critical flicker fusion (CFF) threshold, where the same stimulus is sometimes perceived as flickering and sometimes as steady (fused) . We were thus able to compare brain activity for conscious percepts that differed qualitatively (flickering or fused) but were evoked by identical physical stimuli. Greater brain activation was observed on flicker (versus fused) trials in regions of frontal and parietal cortex previously associated with visual awareness in tasks that did not require detection of temporal patterns . In contrast, greater activation was observed on fused (versus flicker) trials in occipital extrastriate cortex. Our findings indicate that activity of higher-level cortical areas is important for awareness of temporally distinct visual events in the context of a nonspatial task, and they thus suggest that frontal and parietal regions may play a general role in visual awareness.     

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.     

Independent parcellation of the embryonic visual cortex and thalamus revealed by combinatorial Eph/ephrin gene expression

The visual cortex in primates is parcellated into cytoarchitectonically, physiologically, and connectionally distinct areas: the striate cortex (V1) and the extrastriate cortex, consisting of V2 and numerous higher association areas [1]. The innervation of distinct visual cortical areas by the thalamus is especially segregated in primates, such that the lateral geniculate (LG) nucleus specifically innervates striate cortex, whereas pulvinar projections are confined to extrastriate cortex [2--8]. The molecular bases for the parcellation of the visual cortex and thalamus, as well as the establishment of reciprocal connections between distinct compartments within these two structures, are largely unknown. Here, we show that prospective visual cortical areas and corresponding thalamic nuclei in the embryonic rhesus monkey (Macaca mulatta) can be defined by combinatorial expression of genes encoding Eph receptor tyrosine kinases and their ligands, the ephrins, prior to obvious cytoarchitectonic differentiation within the cortical plate and before the establishment of reciprocal connections between the cortical plate and thalamus. These results indicate that molecular patterns of presumptive visual compartments in both the cortex and thalamus can form independently of one another and suggest a role for EphA family members in both compartment formation and axon guidance within the visual thalamocortical system.     

Mathematical modeling and parameter estimation of axonal cargo transport

This paper is about how cortical recurrent interactions in primary visual cortex (V1) together with feedback from extrastriate cortex can account for spectral peaks in the V1 local field potential (LFP). Recent studies showed that visual stimulation enhances the γ-band (25–90 Hz) of the LFP power spectrum in macaque V1. The height and location of the γ-band peak in the LFP spectrum were correlated with visual stimulus size. Extensive spatial summation, possibly mediated by feedback connections from extrastriate cortex and long-range horizontal connections in V1, must play a crucial role in the size dependence of the LFP. To analyze stimulus-effects on the LFP of V1 cortex, we propose a network model for the visual cortex that includes two populations of V1 neurons, excitatory and inhibitory, and also includes feedback to V1 from extrastriate cortex. The neural network model for V1 was a resonant system. The model’s resonance frequency (ResF) was in the γ-band and varied up or down in frequency depending on cortical feedback. The model’s ResF shifted downward with stimulus size, as in the real cortex, because increased size recruited more activity in extrastriate cortex and V1 thereby causing stronger feedback. The model needed to have strong local recurrent inhibition within V1 to obtain ResFs that agree with cortical data. Network resonance as a consequence of recurrent excitation and inhibition appears to be a likely explanation for γ-band peaks in the LFP power spectrum of the primary visual cortex.     

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.     

Retinotopic organization of striate and extrastriate visual cortex in the golden hamster (Mesocricetus auratus).

The visual topography within striate and lateral extrastriate visual cortices was studied in adult hamsters. The cortical areas 17 and 18a in the left hemisphere were electrophysiologically mapped upon stimulation of the right eye, correlating receptive field positions in the visual field with cortical recording sites. Reference lesions were placed at selected cortical sites. Like in rats and other mammals, the lateral extrastriate cortex contained multiple representations of the visual field. Rostral area 18a contained the rostrolateral maps, with medial and lateral divisions. More caudally and sharing a common border with V1, maps in lateromedial, posterolateral and posterior areas were found. More laterally and forming a "third tier" of visual maps, anterolateral, laterolateral-anterior, laterolateral and laterolateral-posterior areas were found. There was also an indication of a possible pararhinal map. The plan so defined is virtually identical to that of rats. The results may be useful to understand a basic mammalian plan in the organization of the visual cortex.     

Remapping for visual stability

Visual perception is based on both incoming sensory signals and information about ongoing actions. Recordings from single neurons have shown that corollary discharge signals can influence visual representations in parietal, frontal and extrastriate visual cortex, as well as the superior colliculus (SC). In each of these areas, visual representations are remapped in conjunction with eye movements. Remapping provides a mechanism for creating a stable, eye-centred map of salient locations. Temporal and spatial aspects of remapping are highly variable from cell to cell and area to area. Most neurons in the lateral intraparietal area remap stimulus traces, as do many neurons in closely allied areas such as the frontal eye fields the SC and extrastriate area V3A. Remapping is not purely a cortical phenomenon. Stimulus traces are remapped from one hemifield to the other even when direct cortico-cortical connections are removed. The neural circuitry that produces remapping is distinguished by significant plasticity, suggesting that updating of salient stimuli is fundamental for spatial stability and visuospatial behaviour. These findings provide new evidence that a unified and stable representation of visual space is constructed by redundant circuitry, comprising cortical and subcortical pathways, with a remarkable capacity for reorganization.     

Functional specialization of seven mouse visual cortical areas

To establish the mouse as a genetically tractable model for high-order visual processing, we characterized fine-scale retinotopic organization of visual cortex and determined functional specialization of layer 2/3 neuronal populations in seven retinotopically identified areas. Each area contains a distinct visuotopic representation and encodes a unique combination of spatiotemporal features. Areas LM, AL, RL, and AM prefer up to three times faster temporal frequencies and significantly lower spatial frequencies than V1, while V1 and PM prefer high spatial and low temporal frequencies. LI prefers both high spatial and temporal frequencies. All extrastriate areas except LI increase orientation selectivity compared to V1, and three areas are significantly more direction selective (AL, RL, and AM). Specific combinations of spatiotemporal representations further distinguish areas. These results reveal that mouse higher visual areas are functionally distinct, and separate groups of areas may be specialized for motion-related versus pattern-related computations, perhaps forming pathways analogous to dorsal and ventral streams in other species.     

Visual saliency and spike timing in the ventral visual pathway.

Visual saliency is a fundamental yet hard to define property of objects or locations in the visual world. In a context where objects and their representations compete to dominate our perception, saliency can be thought of as the "juice" that makes objects win the race. It is often assumed that saliency is extracted and represented in an explicit saliency map, which serves to determine the location of spatial attention at any given time. It is then by drawing attention to a salient object that it can be recognized or categorized. I argue against this classical view that visual "bottom-up" saliency automatically recruits the attentional system prior to object recognition. A number of visual processing tasks are clearly performed too fast for such a costly strategy to be employed. Rather, visual attention could simply act by biasing a saliency-based object recognition system. Under natural conditions of stimulation, saliency can be represented implicitly throughout the ventral visual pathway, independent of any explicit saliency map. At any given level, the most activated cells of the neural population simply represent the most salient locations. The notion of saliency itself grows increasingly complex throughout the system, mostly based on luminance contrast until information reaches visual cortex, gradually incorporating information about features such as orientation or color in primary visual cortex and early extrastriate areas, and finally the identity and behavioral relevance of objects in temporal cortex and beyond. Under these conditions the object that dominates perception, i.e. the object yielding the strongest (or the first) selective neural response, is by definition the one whose features are most "salient"--without the need for any external saliency map. In addition, I suggest that such an implicit representation of saliency can be best encoded in the relative times of the first spikes fired in a given neuronal population. In accordance with our subjective experience that saliency and attention do not modify the appearance of objects, the feed-forward propagation of this first spike wave could serve to trigger saliency-based object recognition outside the realm of awareness, while conscious perceptions could be mediated by the remaining discharges of longer neuronal spike trains.     

Neural correlates of the contents of visual awareness in humans

The immediacy and directness of our subjective visual experience belies the complexity of the neural mechanisms involved, which remain incompletely understood. This review focuses on how the subjective contents of human visual awareness are encoded in neural activity. Empirical evidence to date suggests that no single brain area is both necessary and sufficient for consciousness. Instead, necessary and sufficient conditions appear to involve both activation of a distributed representation of the visual scene in primary visual cortex and ventral visual areas, plus parietal and frontal activity. The key empirical focus is now on characterizing qualitative differences in the type of neural activity in these areas underlying conscious and unconscious processing. To this end, recent progress in developing novel approaches to accurately decoding the contents of consciousness from brief samples of neural activity show great promise.     

Spatial attention changes excitability of human visual cortex to direct stimulation

Conscious perception depends not only on sensory input, but also on attention [1, 2]. Recent studies in monkeys [3-6] and humans [7-12] suggest that influences of spatial attention on visual awareness may reflect top-down influences on excitability of visual cortex. Here we tested this specifically, by providing direct input into human visual cortex via cortical transcranial magnetic stimulation (TMS) to produce illusory visual percepts, called phosphenes. We found that a lower TMS intensity was needed to elicit a conscious phosphene when its apparent spatial location was attended, rather than unattended. Our results indicate that spatial attention can enhance visual-cortex excitability, and visual awareness, even when sensory signals from the eye via the thalamic pathway are bypassed.     

Increased activity in human visual cortex during directed attention in the absence of visual stimulation

When subjects direct attention to a particular location in a visual scene, responses in the visual cortex to stimuli presented at that location are enhanced, and the suppressive influences of nearby distractors are reduced. What is the top-down signal that modulates the response to an attended versus an unattended stimulus? Here, we demonstrate increased activity related to attention in the absence of visual stimulation in extrastriate cortex when subjects covertly directed attention to a peripheral location expecting the onset of visual stimuli. Frontal and parietal areas showed a stronger signal increase during this expectation than did visual areas. The increased activity in visual cortex in the absence of visual stimulation may reflect a top-down bias of neural signals in favor of the attended location, which derives from a fronto-parietal network.     

Temporal Sequence of Visuo-Auditory Interaction in Multiple Areas of the Guinea Pig Visual Cortex

Recent studies in humans and monkeys have reported that acoustic stimulation influences visual responses in the primary visual cortex (V1). Such influences can be generated in V1, either by direct auditory projections or by feedback projections from extrastriate cortices. To test these hypotheses, cortical activities were recorded using optical imaging at a high spatiotemporal resolution from multiple areas of the guinea pig visual cortex, to visual and/or acoustic stimulations. Visuo-auditory interactions were evaluated according to differences between responses evoked by combined auditory and visual stimulation, and the sum of responses evoked by separate visual and auditory stimulations. Simultaneous presentation of visual and acoustic stimulations resulted in significant interactions in V1, which occurred earlier than in other visual areas. When acoustic stimulation preceded visual stimulation, significant visuo-auditory interactions were detected only in V1. These results suggest that V1 is a cortical origin of visuo-auditory interaction.     

Neural representation of visual objects: encoding and top-down activation

Knowledge or experiences are voluntarily recalled from memory by reactivation of their neural representations in the association cortex. Mnemonic representations of visual objects, located in the ventral processing stream of visual perception, provide the best indication of how neuronal codes are created, organized and reactivated. Associative codes are created by neurons that have the ability to link the representations of temporally associated stimuli. Recent experiments suggest that not only bottom-up signals from the retina but also top-down signals from the prefrontal cortex can trigger the retrieval of associative codes, which may serve as a neural basis for conscious recall.