Adaptation to stimulus orientation in mouse primary visual cortex

Information processing in the visual system is shaped by recent stimulus history, such that prolonged viewing of an adapting stimulus can alter the perception of subsequently presented test stimuli. In the tilt‐after‐effect, the perceived orientation of a grating is often repelled away from the orientation of a previously viewed adapting grating. A possible neural correlate for the tilt‐after‐effect has been described in cat and macaque primary visual cortex (V1), where adaptation produces repulsive shifts in the orientation tuning curves of V1 neurons. We investigated adaptation to stimulus orientation in mouse V1 to determine whether known species differences in orientation processing, notably V1 functional architecture and proportion of tightly tuned cells, are important for these repulsive shifts. Unlike the consistent repulsion reported in other species, we found that repulsion was only about twice as common as attraction in our mouse data. Furthermore, adapted responses were attenuated across all orientations. A simple model that captured key physiological findings reported in cats and mice indicated that the greater proportion of broadly tuned neurons in mice may explain the observed species differences in adaptation.     

Disentangling neural structures for processing of high- and low-speed visual motion

Human psychophysical and electrophysiological evidence suggests at least two separate visual motion pathways, one tuned to a lower and one tuned to a broader and partly overlapping range of higher speeds. It remains unclear whether these two different channels are represented by different cortical areas or by sub-populations within a single area. We recorded evoked potentials at 59 scalp locations to the onset of a slow (3.5 degrees /s) and fast (32 degrees /s) moving test pattern, preceded by either a slow or fast adapting pattern that moved in either the same direction or opposite to the test motion. Baseline potentials were recorded for slow and fast moving test patterns after adaptation to a static pattern. Comparison of adapted responses with baseline responses revealed that the N2 peak around 180 ms after test stimulus onset was modulated by the preceding adaptation. This modulation depended on both direction and speed. Source localization of baseline potentials as well as direction-independent motion adaptation revealed cortical areas activated by fast motion to be more dorsal, medial and posterior compared with neural structures underlying slow motion processing. For both speeds, the direction-dependent component of this adaptation modulation occurred in the same area, located significantly more dorsally compared with neural structures that were adapted in a direction-independent manner. These results demonstrate for the first time the cortical separation of more ventral areas selectively activated by visual motion at low speeds (and not high speeds) and dorsal motion-sensitive cortical areas that are activated by both high and low speeds.     

Role of primary visual cortex in the binocular integration of plaid motion perception

This study assessed the early mechanisms underlying perception of plaid motion. Thus, two superimposed gratings drifting in a rightward direction composed plaid stimuli whose global motion direction was perceived as the vector sum of the two components. The first experiment was aimed at comparing the perception of plaid motion when both components were presented to both eyes (dioptic) or separately to each eye (dichoptic). When components of the patterns had identical spatial frequencies, coherent motion was correctly perceived under dioptic and dichoptic viewing condition. However, the perceived direction deviated from the predicted direction when spatial frequency differences were introduced between components in both conditions. The results suggest that motion integration follows similar rules for dioptic and dichoptic plaids even though performance under dichoptic viewing did not reach dioptic levels. In the second experiment, the role of early cortical areas in the processing of both plaids was examined. As convergence of monocular inputs is needed for dichoptic perception, we tested the hypothesis that primary visual cortex (V1) is required for dichoptic plaid processing by delivering repetitive transcranial magnetic stimulation to this area. Ten minutes of magnetic stimulation disrupted subsequent dichoptic perception for approximately 15 min, whereas no significant changes were observed for dioptic plaid perception. Taken together, these findings suggest that V1 is not crucial for the processing of dioptic plaids but it is necessary for the binocular integration underlying dichoptic plaid motion perception.     

Neural correlates of subsecond time distortion in the middle temporal area of visual cortex

How does the brain represent the passage of time at the subsecond scale? Although different conceptual models for time perception have been proposed, its neurophysiological basis remains unknown. We took advantage of a visual duration illusion produced by stimulus novelty to link changes in cortical activity in monkeys with distortions of duration perception in humans. We found that human subjects perceived the duration of a subsecond motion pulse with a novel direction longer than a motion pulse with a repeated direction. Recording from monkeys viewing identical motion stimuli but performing a different behavioral task, we found that both the duration and amplitude of the neural response in the middle temporal area of visual cortex were positively correlated with the degree of novelty of the motion direction. In contrast to previous accounts that attribute distortions in duration perception to changes in the speed of a putative internal clock, our results suggest that the known adaptive properties of neural activity in visual cortex contributes to subsecond temporal distortions.     

Investigating visual motion perception using the transcranial magnetic stimulation-adaptation paradigm

The state-dependency approach of transcranial magnetic stimulation (TMS) enables differential stimulation of functionally distinct neural populations within the affected region of cortex. Here we tested the validity of a paradigm based on state-dependency, the TMS-adaptation paradigm, in the context of visual motion perception. Visual adaptation was used to induce an activity imbalance in direction-selective neurons in the visual cortex, after which participants performed a motion direction discrimination task. When TMS was applied over the motion-selective area V5/MT before each experimental trial, the detection of the direction encoded by the adapted neurons was facilitated relative to the direction encoded by the nonadapted neurons. This finding demonstrates, in the domain of visual motion detection, the state-dependency of TMS effects and the validity of the TMS-adaptation paradigm.     

Dynamics of population response to changes of motion direction in primary visual cortex

The visual system is thought to represent the direction of moving objects in the relative activity of large populations of cortical neurons that are broadly tuned to the direction of stimulus motion, but how changes in the direction of a moving stimulus are represented in the population response remains poorly understood. Here we take advantage of the orderly mapping of direction selectivity in ferret primary visual cortex (V1) to explore how abrupt changes in the direction of a moving stimulus are encoded in population activity using voltage-sensitive dye imaging. For stimuli moving in a constant direction, the peak of the V1 population response accurately represented the direction of stimulus motion, but following abrupt changes in motion direction, the peak transiently departed from the direction of stimulus motion in a fashion that varied with the direction offset angle and was well predicted from the response to the component directions. We conclude that cortical dynamics and population coding mechanisms combine to place constraints on the accuracy with which abrupt changes in direction of motion can be represented by cortical circuits.     

Spatiotemporal frequency and speed tuning in the owl visual wulst

The avian visual wulst is hodologically equivalent to the mammalian primary visual cortex (V1). In contrast to most birds, owls have a massive visual wulst, which shares striking functional similarities with V1. To provide a better understanding of how motion is processed within this area, we used sinusoidal gratings to characterize the spatiotemporal frequency and speed tuning profiles of 131 neurones recorded from awake burrowing owls. Cells were found to be clearly tuned to both spatial and temporal frequencies, and in a way that is similar to what has been reported in the striate cortex of primates and carnivores. Our results also suggest the presence of spatial frequency tuning domains in the wulst. Speed tuning was assessed by several methods devised to measure the degree of dependence between spatial and temporal frequency tuning. Although many neurones were found to be independently tuned, a significant proportion of cells showed at least some degree of dependence, compatible with the idea that some kind of initial transformation towards an explicit representation of speed is being carried out by the owl wulst. Interestingly, under certain constraints, a higher incidence of spatial frequency-invariant speed tuned profiles was obtained by combining our experimentally measured responses using a recent cortical model of speed tuning. Overall, our findings reinforce the notion that, like V1, the owl wulst is an important initial stage for motion processing, a function that is usually attributed to areas of the tectofugal pathway in lateral-eyed birds.     

Direction-selective motion blindness after unilateral posterior brain damage

Motion blindness (MB) is defined as the selective disturbance of visual motion perception despite intact perception of other features of the visual scene. MB is characterized by a pandirectional deficit of motion direction discrimination and is assumed to result from damage to the visual motion pathway, especially area MT/V5. However, the most characteristic feature of primate MT/V5 neurons is not their motion selectivity but their preference for one direction of motion (direction selectivity), which changes incrementally at neighbouring columns. In addition to this microscopic directional organization, studies in nonhuman and human primates suggest that single directions of motion are also coded at a more macroscopic level. We thus hypothesized that if MB in humans results from damage to direction-selective neurons in the visual motion pathway, posterior brain damage might cause MB which is direction selective, not pandirectional. The present study investigated motion direction discrimination in patients with posterior unilateral brain damage and determined separate psychophysical thresholds for the four cardinal directions. In addition, we analysed whether the direction of erroneous motion perception (i.e. the perception of right motion for upward motion) was random or showed a directional bias. We report three principal findings. First, motion direction discrimination was severely impaired in one or two directions while it was normal in the other directions. This constituted direction-selective MB. Second, MB was characterized not only by a quantitative direction-selective increase in psychophysical thresholds but also by a qualitative impairment of perceiving motion direction systematically in wrong directions. Both findings suggest that the cortical modules specialized for the perception of a single direction of motion might be larger than previously thought. Third, lesion analysis showed that unilateral damage, not only the human homologue of MT/V5 but also to parieto-occipital cortex, leads to MB.     

Direct current stimulation over V5 enhances visuomotor coordination by improving motion perception in humans

The primary aim of this study was to determine the extent to which human MT+/V5, an extrastriate visual area known to mediate motion processing, is involved in visuomotor coordination. To pursue this we increased or decreased the excitability of MT+/V5, primary motor, and primary visual cortex by the application of 7 min of anodal and cathodal transcranial direct current stimulation (tDCS) in healthy human subjects while they were performing a visuomotor tracking task involving hand movements. The percentage of correct tracking movements increased specifically during and immediately after cathodal stimulation, which decreases cortical excitability, only when V5 was stimulated. None of the other stimulation conditions affected visuomotor performance. We propose that the improvement in performance caused by cathodal tDCS of V5 is due to a focusing effect on to the complex motion perception conditions involved in this task. This hypothesis was proven by additional experiments: Testing simple and complex motion perception in dot kinetograms, we found that a diminution in excitability induced by cathodal stimulation improved the subject's perception of the direction of the coherent motion only if this was presented among random dots (complex motion perception), and worsened it if only one motion direction was presented (simple movement perception). Our data suggest that area V5 is critically involved in complex motion perception and identification processes important for visuomotor coordination. The results also raise the possibility of the usefulness of tDCS in rehabilitation strategies for neurological patients with visuomotor disorders.     

On the use of visual motion perception to assess magnocellular integrity

It has been proposed, particularly in connection with dyslexia and schizophrenia, that motion perception can be used to assess magnocellular integrity. This suggestion is examined in this paper. The following observations are made: (1) motion information, i.e., information about direction and speed, is extracted at the cortical level, (2) the magnocellular system provides input to the motion selective cortical entities, and (3) so do the parvo- and koniocellular systems. Therefore, although the magnocellular system clearly has the ability to influence motion perception so do other parts of the visual system, e.g., cortical mechanisms. It is concluded that motion perception by itself is not a reliable test of magnocellular integrity.     

Transcranial ultrasound stimulation to human middle temporal complex improves visual motion detection and modulates electrophysiological responses

BackgroundTranscranial ultrasound stimulation (TUS) holds promise as a novel technology for non-invasive neuromodulation, with greater spatial precision than other available methods and the ability to target deep brain structures. However, its safety and efficacy for behavioural and electrophysiological modulation remains controversial and it is not yet clear whether it can be used to manipulate the neural mechanisms supporting higher cognitive function in humans. Moreover, concerns have been raised about a potential TUS-induced auditory confound.ObjectivesWe aimed to investigate whether TUS can be used to modulate higher-order visual function in humans in an anatomically-specific way whilst controlling for auditory confounds.MethodsWe used participant-specific skull maps, functional localisation of brain targets, acoustic modelling and neuronavigation to guide TUS delivery to human visual motion processing cortex (hMT+) whilst participants performed a visual motion detection task. We compared the effects of hMT+ stimulation with sham and control site stimulation and examined EEG data for modulation of task-specific event-related potentials. An auditory mask was applied which prevented participants from distinguishing between stimulation and sham trials.ResultsCompared with sham and control site stimulation, TUS to hMT+ improved accuracy and reduced response times of visual motion detection. TUS also led to modulation of the task-specific event-related EEG potential. The amplitude of this modulation correlated with the performance benefit induced by TUS. No pathological changes were observed comparing structural MRI obtained before and after stimulation.ConclusionsThe results demonstrate for the first time the precision, efficacy and safety of TUS for stimulation of higher-order cortex and cognitive function in humans whilst controlling for auditory confounds.     

The neural processing of 3‐D visual information: evidence from eye movements

Primates have several reflexes that generate eye movements to compensate for bodily movements that would otherwise disturb their gaze and undermine their ability to process visual information. Two vestibulo-ocular reflexes compensate selectively for rotational and translational disturbances of the head, and each has visual backups that operate as negative feedback tracking mechanisms to deal with any residual disturbances of gaze. Of particular interest here are three recently discovered visual tracking mechanisms that specifically address translational disturbances and operate in machine-like fashion with ultra-short latencies (< 60 ms in monkeys, < 85 ms in humans). These visual reflexes deal with motions in all three dimensions and operate as automatic servos, using preattentive parallel processing to provide signals that initiate eye movements before the observer is even aware that there has been a disturbance. This processing is accomplished by visual filters each tuned to a different feature of the binocular images located in the immediate vicinity of the plane of fixation. Two of the reflexes use binocular stereo cues and the third is tuned to particular patterns of optic flow associated with the observer's forward motion. Some stereoanomalous subjects show tracking deficits that can be attributed to a lack of just one subtype of cortical cell encoding motion in one particular direction in a narrow depth plane centred on fixation. Despite their rapid, reflex nature, all three mechanisms rely on cortical processing and evidence from monkeys supports the hypothesis that all are mediated by the medial superior temporal (MST) area of cortex. Remarkably, MST seems to represent the first stage in cortical motion processing at which the visual error signals driving each of the three reflexes are fully elaborated at the level of individual cells.     

Direction-specific motion blindness induced by focal stimulation of human extrastriate cortex

Motion blindness (MB) or akinetopsia is the selective disturbance of visual motion perception while other features of the visual scene such as colour and shape are normally perceived. Chronic and transient forms of MB are characterized by a global deficit of direction discrimination (pandirectional), which is generally assumed to result from damage to, or interference with, the motion complex MT+/V5. However, the most characteristic feature of primate MT-neurons is not their motion specificity, but their preference for one direction of motion (direction specificity). Here, we report that focal electrical stimulation in the human posterior temporal lobe selectively impaired the perception of motion in one direction while the perception of motion in other directions was completely normal (unidirectional MB). In addition, the direction of MB was found to depend on the brain area stimulated. It is argued that direction specificity for visual motion is not only represented at the single neuron level, but also in much larger cortical units.     

The involvement of centralized and distributed processes in sub‐second time interval adaptation: an ERP investigation of apparent motion

Accumulating evidence suggests that the timing of brief stationary sounds affects visual motion perception. Recent studies have shown that auditory time interval can alter apparent motion perception not only through concurrent stimulation but also through brief adaptation. The adaptation after‐effects for auditory time intervals was found to be similar to those for visual time intervals, suggesting the involvement of a central timing mechanism. To understand the nature of cortical processes underlying such after‐effects, we adapted observers to different time intervals using either brief sounds or visual flashes and examined the evoked activity to the subsequently presented visual apparent motion. Both auditory and visual time interval adaptation led to significant changes in the ERPs elicited by the apparent motion. However, the changes induced by each modality were in the opposite direction. Also, they mainly occurred in different time windows and clustered over distinct scalp sites. The effects of auditory time interval adaptation were centred over parietal and parieto‐central electrodes while the visual adaptation effects were mostly over occipital and parieto‐occipital regions. Moreover, the changes were much more salient when sounds were used during the adaptation phase. Taken together, our findings within the context of visual motion point to auditory dominance in the temporal domain and highlight the distinct nature of the sensory processes involved in auditory and visual time interval adaptation.     

Auditory motion direction encoding in auditory cortex and high-level visual cortex

The aim of this functional magnetic resonance imaging (fMRI) study was to identify human brain areas that are sensitive to the direction of auditory motion. Such directional sensitivity was assessed in a hypothesis-free manner by analyzing fMRI response patterns across the entire brain volume using a spherical-searchlight approach. In addition, we assessed directional sensitivity in three predefined brain areas that have been associated with auditory motion perception in previous neuroimaging studies. These were the primary auditory cortex, the planum temporale and the visual motion complex (hMT/V5+). Our whole-brain analysis revealed that the direction of sound-source movement could be decoded from fMRI response patterns in the right auditory cortex and in a high-level visual area located in the right lateral occipital cortex. Our region-of-interest-based analysis showed that the decoding of the direction of auditory motion was most reliable with activation patterns of the left and right planum temporale. Auditory motion direction could not be decoded from activation patterns in hMT/V5+. These findings provide further evidence for the planum temporale playing a central role in supporting auditory motion perception. In addition, our findings suggest a cross-modal transfer of directional information to high-level visual cortex in healthy humans.     

Mechanism of visual network dysfunction in relapsing-remitting multiple sclerosis and its relation to cognition

ObjectiveTo investigate if changes in brain network function and connectivity contribute to the abnormalities in visual event related potentials (ERP) in relapsing-remitting multiple sclerosis (RRMS), and explore their relation to a decrease in cognitive performance.MethodsWe evaluated 72 patients with RRMS and 89 healthy control subjects in a cross-sectional study. Visual ERP were generated using illusory and non-illusory stimuli and recorded using 21 EEG scalp electrodes. The measured activity was modelled using Dynamic Causal Modelling. The model network consisted of 4 symmetric nodes including the primary visual cortex (V1/V2) and the Lateral Occipital Complex. Patients and controls were tested with a neuropsychological test battery consisting of 18 cognitive tests covering six cognitive domains.ResultsWe found reduced cortical connectivity in bottom-up and interhemispheric connections to the right lateral occipital complex in patients (p < 0.001). Furthermore, interhemispherical connections were related to cognitive dysfunction in several domains (attention, executive function, visual perception and organization, processing speed and global cognition) for patients (p < 0.05). No relation was seen between cortical network connectivity and cognitive function in the healthy control subjects.ConclusionChanges in the functional connectivity to higher cortical regions provide a neurobiological explanation for the changes of the visual ERP in RRMS.SignificanceThis study suggests that changes in connectivity to higher cortical regions partly explain visual network dysfunction in RRMS where a lower interhemispheric connectivity may contribute to impaired cognitive function.     

Direction-selective patterns of activity in human visual cortex suggest common neural substrates for different types of motion

A sense of motion can be elicited by the movement of both luminance- and texture-defined patterns, what is commonly referred to as first- and second-order, respectively. Although there are differences in the perception of these two classes of motion stimuli, including differences in temporal and spatial sensitivity, it is debated whether common or separate direction-selective mechanisms are responsible for processing these two types of motion. Here, we measured direction-selective responses to luminance- and texture-defined motion in the human visual cortex by using functional MRI (fMRI) in conjunction with multivariate pattern analysis (MVPA). We found evidence of direction selectivity for both types of motion in all early visual areas (V1, V2, V3, V3A, V4, and MT+), implying that none of these early visual areas is specialized for processing a specific type of motion. More importantly, linear classifiers trained with cortical activity patterns to one type of motion (e.g., first-order motion) could reliably classify the direction of motion defined by the other type (e.g., second-order motion). Our results suggest that the direction-selective mechanisms that respond to these two types of motion share similar spatial distributions in the early visual cortex, consistent with the possibility that common mechanisms are responsible for processing both types of motion.     

Directional responses of visual wulst neurones to grating and plaid patterns in the awake owl

The avian retinothalamofugal pathway reaches the telencephalon in an area known as visual wulst. A close functional analogy between this area and the early visual cortex of mammals has been established in owls. The goal of the present study was to assess quantitatively the directional selectivity and motion integration capability of visual wulst neurones, aspects that have not been previously investigated. We recorded extracellularly from a total of 101 cells in awake burrowing owls. From this sample, 88% of the units exhibited modulated directional responses to sinusoidal gratings, with a mean direction index of 0.74 +/- 0.03 and tuning bandwidth of 28 +/- 1.16 degrees . A direction index higher than 0.5 was observed in 66% of the cells, thereby qualifying them as direction selective. Motion integration was tested with moving plaids, made by adding two sinusoidal gratings of different orientations. We found that 80% of direction-selective cells responded optimally to the motion direction of the component gratings, whereas none responded to the global motion of plaids, whose direction was intermediate to that of the gratings. The remaining 20% were unclassifiable. The strength of component motion selectivity rapidly increased over a 200 ms period following stimulus onset, maintaining a relatively sustained profile thereafter. Overall, our data suggest that, as in the mammalian primary visual cortex, the visual wulst neurones of owls signal the local orientated features of a moving object. How and where these potentially ambiguous signals are integrated in the owl brain might be important for understanding the mechanisms underlying global motion perception.     

Mechanisms of selective inhibition in visual spatial attention are indexed by alpha-band EEG synchronization

Electroencephalographic studies in humans have demonstrated that orienting of visual attention induces a decrease in oscillatory alpha-band activity (alpha-desynchronization) over cortical areas tuned to the attended visual space. This is interpreted as reflecting intentionally enhanced excitability of these areas to facilitate upcoming visual processing. However, the inverse mechanism might also apply. Brain areas that process task-irrelevant space might be actively suppressed by increased alpha-activity (alpha-synchronization) to protect against input of distracter information. In the present study, we demonstrate that such suppression mechanisms are highly selective and are taking place even without distracters that need to be ignored. During voluntary orienting of attention, we found alpha-synchronization to dominate over desynchronization, to be topographically specific for each of eight attention positions, and to occur over areas processing unattended space in a retinotopically organized pattern. This indicates that alpha-synchronization is an important component of selective attention, serving active suppression of unattended positions during visual spatial orienting.     

tACS phase-specifically biases brightness perception of flickering light

BackgroundVisual phenomena like brightness illusions impressively demonstrate the highly constructive nature of perception. In addition to physical illumination, the subjective experience of brightness is related to temporal neural dynamics in visual cortex.ObjectiveHere, we asked whether biasing the temporal pattern of neural excitability in visual cortex by transcranial alternating current stimulation (tACS) modulates brightness perception of concurrent rhythmic visual stimuli.MethodsParticipants performed a brightness discrimination task of two flickering lights, one of which was targeted by same-frequency electrical stimulation at varying phase shifts. tACS was applied with an occipital and a periorbital active control montage, based on simulations of electrical currents using finite element head models.ResultsExperimental results reveal that flicker brightness perception is modulated dependent on the phase shift between sensory and electrical stimulation, solely under occipital tACS. Phase-specific modulatory effects by tACS were dependent on flicker-evoked neural phase stability at the tACS-targeted frequency, recorded prior to electrical stimulation. Further, the optimal timing of tACS application leading to enhanced brightness perception was correlated with the neural phase delay of the cortical flicker response.ConclusionsOur results corroborate the role of temporally coordinated neural activity in visual cortex for brightness perception of rhythmic visual input in humans. Phase-specific behavioral modulations by tACS emphasize its efficacy to transfer perceptually relevant temporal information to the cortex. These findings provide an important step towards understanding the basis of visual perception and further confirm electrical stimulation as a tool for advancing controlled modulations of neural activity and related behavior.