Measurements of simultaneously recorded spiking activity and local field potentials suggest that spatial selection emerges in the frontal eye field

The frontal eye field (FEF) participates in selecting the location of behaviorally relevant stimuli for guiding attention and eye movements. We simultaneously recorded local field potentials (LFPs) and spiking activity in the FEF of monkeys performing memory-guided saccade and covert visual search tasks. We compared visual latencies and the time course of spatially selective responses in LFPs and spiking activity. Consistent with the view that LFPs represent synaptic input, visual responses appeared first in the LFPs followed by visual responses in the spiking activity. However, spatially selective activity identifying the location of the target in the visual search array appeared in the spikes about 30 ms before it appeared in the LFPs. Because LFPs reflect dendritic input and spikes measure neuronal output in a local brain region, this temporal relationship suggests that spatial selection necessary for attention and eye movements is computed locally in FEF from spatially nonselective inputs.     

Sensorimotor mismatch signals in primary visual cortex of the behaving mouse

Studies in anesthetized animals have suggested that activity in early visual cortex is mainly driven by visual input and is well described by a feedforward processing hierarchy. However, evidence from experiments on awake animals has shown that both eye movements and behavioral state can strongly modulate responses of neurons in visual cortex; the functional significance of this modulation, however, remains elusive. Using visual-flow feedback manipulations during locomotion in a virtual reality environment, we found that responses in layer 2/3 of mouse primary visual cortex are strongly driven by locomotion and by mismatch between actual and expected visual feedback. These data suggest that processing in visual cortex may be based on predictive coding strategies that use motor-related and visual input to detect mismatches between predicted and actual visual feedback.     

Neural basis of the ventriloquist illusion

The ventriloquist creates the illusion that his or her voice emerges from the visibly moving mouth of the puppet [1]. This well-known illusion exemplifies a basic principle of how auditory and visual information is integrated in the brain to form a unified multimodal percept. When auditory and visual stimuli occur simultaneously at different locations, the more spatially precise visual information dominates the perceived location of the multimodal event. Previous studies have examined neural interactions between spatially disparate auditory and visual stimuli [2-5], but none has found evidence for a visual influence on the auditory cortex that could be directly linked to the illusion of a shifted auditory percept. Here we utilized event-related brain potentials combined with event-related functional magnetic resonance imaging to demonstrate on a trial-by-trial basis that a precisely timed biasing of the left-right balance of auditory cortex activity by the discrepant visual input underlies the ventriloquist illusion. This cortical biasing may reflect a fundamental mechanism for integrating the auditory and visual components of environmental events, which ensures that the sounds are adaptively localized to the more reliable position provided by the visual input.     

Blinking suppresses the neural response to unchanging retinal stimulation

Blinks profoundly interrupt visual input but are rarely noticed, perhaps because of blink suppression, a visual-sensitivity loss that begins immediately prior to blink onset. Blink suppression is thought to result from an extra-retinal signal that is associated with the blink motor command and may act to attenuate the sensory consequences of the motor action. However, the neural mechanisms underlying this phenomenon remain unclear. They are challenging to study because any brain-activity changes resulting from an extra-retinal signal associated with the blink motor command are potentially masked by profound neural-activity changes caused by the retinal-illumination reduction that results from occlusion of the pupil by the eyelid. Here, we distinguished direct top-down effects of blink-associated motor signals on cortical activity from purely mechanical or optical effects of blinking on visual input by combining pupil-independent retinal stimulation with functional MRI (fMRI) in humans. Even though retinal illumination was kept constant during blinks, we found that blinking nevertheless suppressed activity in visual cortex and in areas of parietal and prefrontal cortex previously associated with awareness of environmental change. Our findings demonstrate active top-down modulation of visual processing during blinking, suggesting a possible mechanism by which blinks go unnoticed.     

Input-dependent wave attenuation in a critically-balanced model of cortex

A number of studies have suggested that many properties of brain activity can be understood in terms of critical systems. However it is still not known how the long-range susceptibilities characteristic of criticality arise in the living brain from its local connectivity structures. Here we prove that a dynamically critically-poised model of cortex acquires an infinitely-long ranged susceptibility in the absence of input. When an input is presented, the susceptibility attenuates exponentially as a function of distance, with an increasing spatial attenuation constant (i.e., decreasing range) the larger the input. This is in direct agreement with recent results that show that waves of local field potential activity evoked by single spikes in primary visual cortex of cat and macaque attenuate with a characteristic length that also increases with decreasing contrast of the visual stimulus. A susceptibility that changes spatial range with input strength can be thought to implement an input-dependent spatial integration: when the input is large, no additional evidence is needed in addition to the local input; when the input is weak, evidence needs to be integrated over a larger spatial domain to achieve a decision. Such input-strength-dependent strategies have been demonstrated in visual processing. Our results suggest that input-strength dependent spatial integration may be a natural feature of a critically-balanced cortical network.     

A model of the saccade-generating system that accounts for trajectory variations produced by competing visual stimuli

Variable saccade trajectories are produced in visual search paradigms in which multiple potential target stimuli are present. These variable trajectories provide a rich source of information that may lead to a deeper understanding of the basic control mechanisms of the saccadic system. We have used published behavioral observations and neural recordings in the superior colliculus (SC), gathered in monkeys performing visual search paradigms, to guide the construction of a new distributed model of the saccadic system. The new model can account for many of the variations in saccade trajectory produced by the appearance of multiple visual stimuli in a search paradigm. The model uses distributed feedback about current eye motion from the brainstem to the SC to reduce activity there at physiologically realistic rates during saccades. The long-range lateral inhibitory connections between SC cells used in previous models have been eliminated to match recent physiological evidence. The model features interactions between visually activated multiple populations of cells in the SC and distributed and topologically organized inhibitory input to the SC from the SNr to produce some of the types of variable saccadic trajectories, including slightly curved and averaging saccades, observed in visual search tasks. The distributed perisaccadic disinhibition of SC from the substantia nigra (SNr) is assumed to have broad spatial tuning. In order to produce the strongly curved saccades occasionally recorded in visual search, the existence of a parallel input to the saccadic burst generators in addition to that provided by the distributed input from the SC is required. The spatiotemporal form of this additional parallel input is computed based on the assumption that the input from the model SC is realistic. In accordance with other recent models, it is assumed that the parallel input comes from the cerebellum, but our model predicts that the parallel input is delayed during highly curved saccadic trajectories.     

Dynamics of parietal neural activity during spatial cognitive processing

Dynamic neural processing unrelated to changes in sensory input or motor output is likely to be a hallmark of cognitive operations. Here we show that neural representations of space in parietal cortex are dynamic while monkeys perform a spatial cognitive operation on a static visual stimulus. We recorded neural activity in area 7a during a visual maze task in which monkeys mentally followed a path without moving their eyes. We found that the direction of the followed path could be recovered from neuronal population activity. When the monkeys covertly processed a path that turned, the population representation of path direction shifted in the direction of the turn. This neural population dynamic took place during a period of unchanging visual input and showed characteristics of both serial and parallel processing. The data suggest that the dynamic evolution of parietal neuronal activity is associated with the progression of spatial cognitive operations.     

Spike suppression in a local cortical circuit induced by transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) noninvasively interferes with human cortical function, and is widely used as an effective technique for probing causal links between neural activity and cognitive function. However, the physiological mechanisms underlying TMS-induced effects on neural activity remain unclear. We examined the mechanism by which TMS disrupts neural activity in a local circuit in early visual cortex using a computational model consisting of conductance-based spiking neurons with excitatory and inhibitory synaptic connections. We found that single-pulse TMS suppressed spiking activity in a local circuit model, disrupting the population response. Spike suppression was observed when TMS was applied to the local circuit within a limited time window after the local circuit received sensory afferent input, as observed in experiments investigating suppression of visual perception with TMS targeting early visual cortex. Quantitative analyses revealed that the magnitude of suppression was significantly larger for synaptically-connected neurons than for isolated individual neurons, suggesting that intracortical inhibitory synaptic coupling also plays an important role in TMS-induced suppression. A conventional local circuit model of early visual cortex explained only the early period of visual suppression observed in experiments. However, models either involving strong recurrent excitatory synaptic connections or sustained excitatory input were able to reproduce the late period of visual suppression. These results suggest that TMS targeting early visual cortex disrupts functionally distinct neural signals, possibly corresponding to feedforward and recurrent information processing, by imposing inhibitory effects through intracortical inhibitory synaptic connections.     

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.     

On the cyclic nature of perception in vision versus audition

Does our perceptual awareness consist of a continuous stream, or a discrete sequence of perceptual cycles, possibly associated with the rhythmic structure of brain activity? This has been a long-standing question in neuroscience. We review recent psychophysical and electrophysiological studies indicating that part of our visual awareness proceeds in approximately 7–13 Hz cycles rather than continuously. On the other hand, experimental attempts at applying similar tools to demonstrate the discreteness of auditory awareness have been largely unsuccessful. We argue and demonstrate experimentally that visual and auditory perception are not equally affected by temporal subsampling of their respective input streams: video sequences remain intelligible at sampling rates of two to three frames per second, whereas audio inputs lose their fine temporal structure, and thus all significance, below 20–30 samples per second. This does not mean, however, that our auditory perception must proceed continuously. Instead, we propose that audition could still involve perceptual cycles, but the periodic sampling should happen only after the stage of auditory feature extraction. In addition, although visual perceptual cycles can follow one another at a spontaneous pace largely independent of the visual input, auditory cycles may need to sample the input stream more flexibly, by adapting to the temporal structure of the auditory inputs.     

Assessing visual requirements for social context-dependent activation of the songbird song system

Social context has been shown to have a profound influence on brain activation in a wide range of vertebrate species. Best studied in songbirds, when males sing undirected song, the level of neural activity and expression of immediate early genes (IEGs) in several song nuclei is dramatically higher or lower than when they sing directed song to other birds, particularly females. This differential social context-dependent activation is independent of auditory input and is not simply dependent on the motor act of singing. These findings suggested that the critical sensory modality driving social context-dependent differences in the brain could be visual cues. Here, we tested this hypothesis by examining IEG activation in song nuclei in hemispheres to which visual input was normal or blocked. We found that covering one eye blocked visually induced IEG expression throughout both contralateral visual pathways of the brain, and reduced activation of the contralateral ventral tegmental area, a non-visual midbrain motivation-related area affected by social context. However, blocking visual input had no effect on the social context-dependent activation of the contralateral song nuclei during female-directed singing. Our findings suggest that individual sensory modalities are not direct driving forces for the social context differences in song nuclei during singing. Rather, these social context differences in brain activation appear to depend more on the general sense that another individual is present.     

Predictive Coding or Evidence Accumulation? False Inference and Neuronal Fluctuations

Perceptual decisions can be made when sensory input affords an inference about what generated that input. Here, we report findings from two independent perceptual experiments conducted during functional magnetic resonance imaging (fMRI) with a sparse event-related design. The first experiment, in the visual modality, involved forced-choice discrimination of coherence in random dot kinematograms that contained either subliminal or periliminal motion coherence. The second experiment, in the auditory domain, involved free response detection of (non-semantic) near-threshold acoustic stimuli. We analysed fluctuations in ongoing neural activity, as indexed by fMRI, and found that neuronal activity in sensory areas (extrastriate visual and early auditory cortex) biases perceptual decisions towards correct inference and not towards a specific percept. Hits (detection of near-threshold stimuli) were preceded by significantly higher activity than both misses of identical stimuli or false alarms, in which percepts arise in the absence of appropriate sensory input. In accord with predictive coding models and the free-energy principle, this observation suggests that cortical activity in sensory brain areas reflects the precision of prediction errors and not just the sensory evidence or prediction errors per se.     

Perceptual echoes at 10 Hz in the human brain

The occipital alpha rhythm (～10 Hz) is the most prominent electrophysiological activity in the awake human brain, yet its functional role and relation to visual perception are little understood. Transient stimuli normally elicit a short series of positive and negative deflections lasting between 300 and 500 ms: the visual-evoked potential (VEP). Alpha oscillations, on the other hand, are generally suppressed by transient visual input; they only augment in response to periodic ("steady-state") inputs around 10 Hz. Here, we applied reverse-correlation techniques to the visual presentation of random, nonperiodic dynamic stimulation sequences and found that the brain response to each stimulus transient was not merely a short-lived VEP but also included a strong ～10 Hz oscillation that lasted for more than 1 s. In other words, the alpha rhythm implements an "echo" or reverberation of the input sequence. These echoes are correlated in magnitude and frequency with the observer's occipital alpha rhythm, are enhanced by visual attention, and can be rendered perceptually apparent in the form of ～10 Hz flicker. These findings suggest a role for the alpha rhythm in the maintenance of sensory representations over time.     

The convergent properties of the neocortical vestibular area in the cat]

In acute experiments on cats under nembutal-chloralose anaesthesia the evoked potentials and cellular reactions were studied of suprasylvian vestibular and auditory projection zones to stimulation of vestibular, acoustic and visual nerves and frontal paw. It has been shown that the suprasylvian vestibular zone represents the region of convergence of vestibular, auditory, somatic and visual afferentation. Properties of summary and cellular reactions of the vestibular zone and also the character of interaction of the evoked potentials of homo- and heteromodal origin testify to the absence of significant dominance of vestibular input to this area of the cerebral cortex in cats. Limitation of spreading of labyrinth activity in the cerebral cortex and the absence of dominance of homomodal input in the projection zone should, probably, be considered as typical property of the vestibular system presentation in the cortex, determining the disability of monomodal specific reaction in the sensory-perceptive sphere.     

Abstract coding of audiovisual speech: beyond sensory representation

Is there a neural representation of speech that transcends its sensory properties? Using fMRI, we investigated whether there are brain areas where neural activity during observation of sublexical audiovisual input corresponds to a listener's speech percept (what is "heard") independent of the sensory properties of the input. A target audiovisual stimulus was preceded by stimuli that (1) shared the target's auditory features (auditory overlap), (2) shared the target's visual features (visual overlap), or (3) shared neither the target's auditory or visual features but were perceived as the target (perceptual overlap). In two left-hemisphere regions (pars opercularis, planum polare), the target invoked less activity when it was preceded by the perceptually overlapping stimulus than when preceded by stimuli that shared one of its sensory components. This pattern of neural facilitation indicates that these regions code sublexical speech at an abstract level corresponding to that of the speech percept.     

Light elicited isolation of the complementary visual input systems in white-eye Drosophila.

Evidence is presented to show that the spectral sensitivity of the white-eye of Drosophila, indicated by the residual ERG following blue irradiation which renders the eye dark-depolarized, has a maximum around 460 nm, and represents the activity of R7 and possibly that of R8. Whereas the ERG of the repolarized dark-adapted white-eye, effected by orange irradiation, indicates a spectral sensitivity having a maximum around 490 to 500 nm, and represents the activity of R1 to 6 preferentially. Manipulation of these two visual input systems is achieved using various régimes of irradiation, the systems being switched at will. The critical flicker fusion frequency respectively for the two systems has been measured, that of R1 to 6 being twice as high as that of R7±8.Implications for the visual function of the eye are considered, in particular the significance of the wildtype red-eye colour. The ease of manipulation has considerable value to the experimentalist wishing to study the input systems in isolation and concomitantly.     

Multisensory convergence in the mushroom bodies of ants and bees

The mushroom bodies, central neuropils in the arthropod brain, are involved in learning and memory and in the control of complex behavior. In most insects, the mushroom bodies receive direct olfactory input in their calyx region. In Hymenoptera, olfactory input is layered in the calyx. In ants, several layers can be discriminated that correspond to different clusters of glomeruli in the antennal lobes, perhaps corresponding to different classes of odors. Only in Hymenoptera, the mushroom body calyx also receives direct visual input from the optic lobes. In bees, six calycal layers receive input from different classes of visual interneurons, probably representing different parts of the visual field and different visual properties. Taken together, the mushroom bodies receive distinct multisensory information in many segregated input layers.     

A contribution of synaptic plasticity in the basal ganglia to processing of visual information

The mechanism of involvement of the basal ganglia in processing of visual information on the basis of dopamine-dependent modulation of efficacy of synaptic transmission in interconnected parallel associative and limbic loops (cortex--basal ganglia--thalamus--cortex) is proposed. Each loop consists of one of the visual or prefrontal cortical areas connected with the thalamic nucleus and corresponding loci in different nuclei of the basal ganglia. Circulation of activity in such a loop provides reentrance of information into the thalamus and neocortex. Dopamine releasing in response to a visual stimulus oppositely modulates the efficacy of "strong" and "weak" corticostriatal inputs. Subsequent reorganization of activity in the loop leads to a disinhibition (inhibition) of activity of those cortical neurons that were "strongly" ("weakly)" excited by the visual stimulus simultaneously with activation of dopaminergic cells. A selected neuronal pattern in each cortical area represents a property of the visual stimulus processed by this area. Excitation of dopaminergic cells by the visual stimulus via the superior colliculi requires parallel activation of a disinhibitory input to the superior colliculi via the thalamus and a "direct" pathway through the basal ganglia. The prefrontal cortex excited by the visual stimulus via the mediodorsal thalamic nucleus performs a top-down control over the dopaminergic cell activity, supervising simultaneous dopamine release in different striatal loci and thus promotes the interconnected selection of neuronal representations of individual properties of the visual stimulus and their binding in an integrated image.     

Cellular mechanisms underlying stimulus-dependent gain modulation in primary visual cortex neurons in vivo

Gain modulation is a widespread neuronal phenomenon that modifies response amplitude without changing selectivity. Computational and in vitro studies have proposed cellular mechanisms of gain modulation based on the postsynaptic effects of background synaptic activation, but these mechanisms have not been studied in vivo. Here, we used intracellular recordings from cat primary visual cortex to measure neuronal gain while changing background synaptic activity with visual stimulation. We found that increases in the membrane fluctuations associated with increases in synaptic input do not obligatorily result in gain modulation in vivo. However, visual stimuli that evoked sustained changes in resting membrane potential, input resistance, and membrane fluctuations robustly modulated neuronal gain. The magnitude of gain modulation depended critically on the spatiotemporal properties of the visual stimulus. Gain modulation in vivo may thus be determined on a moment-to-moment basis by sensory context and the consequent dynamics of synaptic activation.     

The parvocellular LGN provides a robust disynaptic input to the visual motion area MT

Dorsal visual cortical areas are thought to be dominated by input from the magnocellular (M) visual pathway, with little or no parvocellular (P) contribution. These relationships are supported by a close correlation between the functional properties of these areas and the M pathway and by a lack of anatomical evidence for P input. Here we use rabies virus as a retrograde transynaptic tracer to show that the dorsal area MT receives strong input, via a single relay, from both M and P cells of the lateral geniculate nucleus. This surprising P input, likely relayed via layer 6 Meynert cells in primary visual cortex, can provide MT with sensitivity to a more complete range of spatial, temporal, and chromatic cues than the M pathway alone. These observations provide definitive evidence for P pathway input to MT and show that convergence of parallel visual pathways occurs in the dorsal stream.