A common neuronal code for perceptual processes in visual cortex? Comparing choice and attentional correlates in V5/MT.

In the past two decades, sensory neuroscience has moved from describing response properties to external stimuli in cerebral cortex to establishing connections between neuronal activity and sensory perception. The seminal studies by Newsome, Movshon and colleagues in the awake behaving macaque firmly link single cells in extrastriate area V5/MT and perception of motion. A decade later, extrastriate visual cortex appears awash with neuronal correlates for many different perceptual tasks. Examples are attentional signals, choice signals for ambiguous images, correlates for binocular rivalry, stereo and shape perception, and so on. These diverse paradigms are aimed at elucidating the neuronal code for perceptual processes, but it has been little studied how they directly compare or even interact. In this paper, I explore to what degree the measured neuronal signals in V5/MT for choice and attentional paradigms might reflect a common neuronal mechanism for visual perception.     

Visibility reflects dynamic changes of effective connectivity between V1 and fusiform cortex

Identifying the neural basis of visibility is central to understanding conscious visual perception. Visibility of basic features such as brightness is often thought to reflect activity in just early visual cortex. But here we show under metacontrast masking that fMRI activity in stimulus-driven areas of early visual cortex did not reflect parametric changes in the visibility of a brightness stimulus. The psychometric visibility function was instead correlated with activity in later visual regions plus parieto-frontal areas, and surprisingly, in representations of the unstimulated stimulus surround for primary visual cortex. Critically, decreased stimulus visibility was associated with a regionally-specific decoupling between early visual cortex and higher visual areas. This provides evidence that dynamic changes in effective connectivity can closely reflect visual perception.     

Responses to lightness variations in early human visual cortex

Lightness is the apparent reflectance of a surface, and it depends not only on the actual luminance of the surface but also on the context in which the surface is viewed [1-10]. The cortical mechanisms of lightness processing are largely unknown, and the role of early cortical areas is still a matter of debate [11-17]. We studied the cortical responses to lightness variations in early stages of the human visual system with functional magnetic resonance imaging (fMRI) while observers were performing a demanding fixation task. The set of dynamically presented visual stimuli included the rectangular version of the classic Craik-O'Brien stimulus [3, 18, 19] and a variant that led to a weaker lightness effect, as well as a pattern with actual luminance variations. We found that the cortical activity in retinotopic areas, including the primary visual cortex (V1), is correlated with context-dependent lightness variations.     

Emergence and transmission of visual awareness through optical coding in the brain: A redox molecular hypothesis on visual mental imagery

Does the primary visual cortex mediate consciousness for higher-level stages of information processing by providing an outlet for mental imagery? Evidence based on neural electrical activity is inconclusive as reflected in the “imagery debate” in cognitive science. Neural information and activity, however, also depend on regulated biophoton (optical) signaling. During encoding and retrieval of visual information, regulated electrical (redox) signals of neurons are converted into synchronized biophoton signals by bioluminescent radical processes. That is, visual information may be represented by regulated biophotons of mitochondrial networks in retinotopically organized cytochrome oxidase-rich neural networks within early visual areas. Therefore, we hypothesize that regulated biophotons can generate intrinsic optical representations in the primary visual cortex and then propagate variably degraded versions along cytochrome oxidase pathways during both perception and imagery. Testing this hypothesis requires to establish a methodology for measurement of in vivo and/or in vitro increases of biophoton emission in humans' brain during phosphene inductions by transcranial magnetic stimulation and to compare the decrease in phosphene thresholds during transcranial magnetic stimulation and imagery. Our hypothesis provides a molecular mechanism for the visual buffer and for imagery as the prevalent communication mode (through optical signaling) within the brain. If confirmed empirically, this hypothesis could resolve the imagery debate and the underlying issue of continuity between perception and abstract thought.     

Peripheral and central inputs shape network dynamics in the developing visual cortex in vivo

Spontaneous network activity constitutes a central theme during the development of neuronal circuitry [1, 2]. Before the onset of vision, retinal neurons generate waves of spontaneous activity that are relayed along the ascending visual pathway [3, 4] and shape activity patterns in these regions [5, 6]. The spatiotemporal nature of retinal waves is required to establish precise functional maps in higher visual areas, and their disruption results in enlarged axonal projection areas (e.g., [7-10]). However, how retinal inputs shape network dynamics in the visual cortex on the cellular level is unknown. Using in vivo two-photon calcium imaging, we identified two independently occurring patterns of network activity in the mouse primary visual cortex (V1) before and at the onset of vision. Acute manipulations of spontaneous retinal activity revealed that one type of network activity largely originated in the retina and was characterized by low synchronicity (L-) events. In addition, we identified a type of high synchronicity (H-) events that required gap junction signaling but were independent of retinal input. Moreover, the patterns differed in wave progression and developmental profile. Our data suggest that different activity patterns have complementary functions during the formation of synaptic circuits in the developing visual cortex.     

Interhemispheric connections shape subjective experience of bistable motion

The right and left visual hemifields are represented in different cerebral hemispheres and are bound together by connections through the corpus callosum. Much has been learned on the functions of these connections from split-brain patients [1-4], but little is known about their contribution to conscious visual perception in healthy humans. We used diffusion tensor imaging and functional magnetic resonance imaging to investigate which callosal connections contribute to the subjective experience of a visual motion stimulus that requires interhemispheric integration. The "motion quartet" is an ambiguous version of apparent motion that leads to perceptions of either horizontal or vertical motion [5]. Interestingly, observers are more likely to perceive vertical than horizontal motion when the stimulus is presented centrally in the visual field [6]. This asymmetry has been attributed to the fact that, with central fixation, perception of horizontal motion requires integration across hemispheres whereas perception of vertical motion requires only intrahemispheric processing [7]. We are able to show that the microstructure of individually tracked callosal segments connecting motion-sensitive areas of the human MT/V5 complex (hMT/V5+; [8]) can predict the conscious perception of observers. Neither connections between primary visual cortex (V1) nor other surrounding callosal regions exhibit a similar relationship.     

Primary visual cortex and visual awareness

The primary visual cortex (V1) is probably the best characterized area of primate cortex, but whether this region contributes directly to conscious visual experience is controversial. Early neurophysiological and neuroimaging studies found that visual awareness was best correlated with neural activity in extrastriate visual areas, but recent studies have found similarly powerful effects in V1. Lesion and inactivation studies have provided further evidence that V1 might be necessary for conscious perception. Whereas hierarchical models propose that damage to V1 simply disrupts the flow of information to extrastriate areas that are crucial for awareness, interactive models propose that recurrent connections between V1 and higher areas form functional circuits that support awareness. Further investigation into V1 and its interactions with higher areas might uncover fundamental aspects of the neural basis of visual awareness.     

Reconstructing visual experiences from brain activity evoked by natural movies

Quantitative modeling of human brain activity can provide crucial insights about cortical representations [1, 2] and can form the basis for brain decoding devices [3-5]. Recent functional magnetic resonance imaging (fMRI) studies have modeled brain activity elicited by static visual patterns and have reconstructed these patterns from brain activity [6-8]. However, blood oxygen level-dependent (BOLD) signals measured via fMRI are very slow [9], so it has been difficult to model brain activity elicited by dynamic stimuli such as natural movies. Here we present a new motion-energy [10, 11] encoding model that largely overcomes this limitation. The model describes fast visual information and slow hemodynamics by separate components. We recorded BOLD signals in occipitotemporal visual cortex of human subjects who watched natural movies and fit the model separately to individual voxels. Visualization of the fit models reveals how early visual areas represent the information in movies. To demonstrate the power of our approach, we also constructed a Bayesian decoder [8] by combining estimated encoding models with a sampled natural movie prior. The decoder provides remarkable reconstructions of the viewed movies. These results demonstrate that dynamic brain activity measured under naturalistic conditions can be decoded using current fMRI technology.     

Decoding seen and attended motion directions from activity in the human visual cortex

Functional neuroimaging has successfully identified brain areas that show greater responses to visual motion and adapted responses to repeated motion directions. However, such methods have been thought to lack the sensitivity and spatial resolution to isolate direction-selective responses to individual motion stimuli. Here, we used functional magnetic resonance imaging (fMRI) and pattern classification methods to show that ensemble activity patterns in human visual cortex contain robust direction-selective information, from which it is possible to decode seen and attended motion directions. Ensemble activity in areas V1-V4 and MT+/V5 allowed us to decode which of eight possible motion directions the subject was viewing on individual stimulus blocks. Moreover, ensemble activity evoked by single motion directions could effectively predict which of two overlapping motion directions was the focus of the subject's attention and presumably dominant in perception. Our results indicate that feature-based attention can bias direction-selective population activity in multiple visual areas, including MT+/V5 and early visual areas (V1-V4), consistent with gain-modulation models of feature-based attention and theories of early attentional selection. Our approach for measuring ensemble direction selectivity may provide new opportunities to investigate relationships between attentional selection, conscious perception, and direction-selective responses in the human brain.     

Binocular Flash Suppression in the Primary Visual Cortex of Anesthetized and Awake Macaques

Primary visual cortex (V1) was implicated as an important candidate for the site of perceptual suppression in numerous psychophysical and imaging studies. However, neurophysiological results in awake monkeys provided evidence for competition mainly between neurons in areas beyond V1. In particular, only a moderate percentage of neurons in V1 were found to modulate in parallel with perception with magnitude substantially smaller than the physical preference of these neurons. It is yet unclear whether these small modulations are rooted from local circuits in V1 or influenced by higher cognitive states. To address this question we recorded multi-unit spiking activity and local field potentials in area V1 of awake and anesthetized macaque monkeys during the paradigm of binocular flash suppression. We found that a small but significant modulation was present in both the anesthetized and awake states during the flash suppression presentation. Furthermore, the relative amplitudes of the perceptual modulations were not significantly different in the two states. We suggest that these early effects of perceptual suppression might occur locally in V1, in prior processing stages or within early visual cortical areas in the absence of top-down feedback from higher cognitive stages that are suppressed under anesthesia.     

Remembering visual motion: neural correlates of associative plasticity and motion recall in cortical area MT

The pictorial content of visual memories recalled by association is embodied by neuronal activity at the highest processing stages of primate visual cortex. This activity is elicited by top-down signals from the frontal lobe and recapitulates the bottom-up pattern normally obtained by the recalled stimulus. To explore the generality and mechanisms of this phenomenon, we recorded motion-sensitive neurons at an early stage of cortical processing. After monkeys learned to associate directions of motion with static shapes, these neurons exhibited unprecedented selectivity for the shapes. This emergent shape selectivity reflects activation of neurons representing the motion stimuli recalled by association, and it suggests that recall-related activity may be a general feature of neurons in visual cortex.     

MEG responses to the perception of global structure within glass patterns

Background

The perception of global form requires integration of local visual cues across space and is the foundation for object recognition. Here we used magnetoencephalography (MEG) to study the location and time course of neuronal activity associated with the perception of global structure from local image features. To minimize neuronal activity to low-level stimulus properties, such as luminance and contrast, the local image features were held constant during all phases of the MEG recording. This allowed us to assess the relative importance of striate (V1) versus extrastriate cortex in global form perception.

Methodology/Principal Findings

Stimuli were horizontal, rotational and radial Glass patterns. Glass patterns without coherent structure were viewed during the baseline period to ensure neuronal responses reflected perception of structure and not changes in local image features. The spatial distribution of task-related changes in source power was mapped using Synthetic Aperture Magnetometry (SAM), and the time course of activity within areas of maximal power change was determined by calculating time-frequency plots using a Hilbert transform. For six out of eight observers, passive viewing of global structure was associated with a reduction in 10–20 Hz cortical oscillatory power within extrastriate occipital cortex. The location of greatest power change was the same for each pattern type, being close to or within visual area V3a. No peaks of activity were observed in area V1. Time-frequency analyses indicated that neural activity was least for horizontal patterns.

Conclusions

We conclude: (i) visual area V3a is involved in the analysis of global form; (ii) the neural signature for perception of structure, as assessed using MEG, is a reduction in 10–20 Hz oscillatory power; (iii) different neural processes may underlie the perception of horizontal as opposed to radial or rotational structure; and (iv) area V1 is not strongly activated by global form in Glass patterns.     

Characterization of visual percepts evoked by noninvasive stimulation of the human posterior parietal cortex

Phosphenes are commonly evoked by transcranial magnetic stimulation (TMS) to study the functional organization, connectivity, and excitability of the human visual brain. For years, phosphenes have been documented only from stimulating early visual areas (V1-V3) and a handful of specialized visual regions (V4, V5/MT+) in occipital cortex. Recently, phosphenes were reported after applying TMS to a region of posterior parietal cortex involved in the top-down modulation of visuo-spatial processing. In the present study, we systematically characterized parietal phosphenes to determine if they are generated directly by local mechanisms or emerge through indirect activation of other visual areas. Using technology developed in-house to record the subjective features of phosphenes, we found no systematic differences in the size, shape, location, or frame-of-reference of parietal phosphenes when compared to their occipital counterparts. In a second experiment, discrete deactivation by 1 Hz repetitive TMS yielded a double dissociation: phosphene thresholds increased at the deactivated site without producing a corresponding change at the non-deactivated location. Overall, the commonalities of parietal and occipital phosphenes, and our ability to independently modulate their excitability thresholds, lead us to conclude that they share a common neural basis that is separate from either of the stimulated regions.     

Perceptual and neuronal correspondence in primary visual cortex

Recent findings from the study of primary visual cortex in humans and animals blur the distinction between early and late visual processing. Under some conditions, the activity of neurons in primary visual cortex appears as close or closer to perception than activity in 'higher' visual areas.     

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.     

Stimulus timing-dependent plasticity in high-level vision

Humans are able to efficiently learn and remember complex visual patterns after only a few seconds of exposure [1]. At a cellular level, such learning is thought to involve changes in synaptic efficacy, which have been linked to the precise timing of action potentials relative to synaptic inputs [2-4]. Previous experiments have tapped into the timing of neural spiking events by using repeated asynchronous presentation of visual stimuli to induce changes in both the tuning properties of visual neurons and the perception of simple stimulus attributes [5, 6]. Here we used a similar approach to investigate potential mechanisms underlying the perceptual learning of face identity, a high-level stimulus property based on the spatial configuration of local features. Periods of stimulus pairing induced a systematic bias in face-identity perception in a manner consistent with the predictions of spike timing-dependent plasticity. The perceptual shifts induced for face identity were tolerant to a 2-fold change in stimulus size, suggesting that they reflected neuronal changes in nonretinotopic areas, and were more than twice as strong as the perceptual shifts induced for low-level visual features. These results support the idea that spike timing-dependent plasticity can rapidly adjust the neural encoding of high-level stimulus attributes [7-11].     

Binocular depth perception and the cerebral cortex

Our ability to coordinate the use of our left and right eyes and to make use of subtle differences between the images received by each eye allows us to perceive stereoscopic depth, which is important for the visual perception of three-dimensional space. Binocular neurons in the visual cortex combine signals from the left and right eyes. Probing the roles of binocular neurons in different perceptual tasks has advanced our understanding of the stages within the visual cortex that lead to binocular depth perception.     

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.