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.     

Attentional load modifies early activity in human primary visual cortex

Recent theories of selective attention assume that the more attention is required by a task, the earlier are irrelevant stimuli filtered during perceptual processing. Previous functional MRI studies have demonstrated that primary visual cortex (V1) activation by peripheral distractors is reduced by higher task difficulty at fixation, but it remains unknown whether such changes affect initial processing in V1 or subsequent feedback. Here we manipulated attentional load at fixation while recording peripheral visual responses with high-density EEG in 28 healthy volunteers, which allowed us to track the exact time course of attention-related effects on V1. Our results show a modulation of the earliest component of the visual evoked potential (C1) as a function of attentional load. Additional topographic and source localization analyses corroborated this finding, with significant load-related differences observed throughout the first 100 ms post-stimulus. However, this effect was observed only when stimuli were presented in the upper visual field (VF), but not for symmetrical positions in the lower VF. Our findings demonstrate early filtering of irrelevant information under increased attentional demands, thus supporting models that assume a flexible mechanism of attentional selection, but reveal important functional asymmetries across the VF.     

Organization of direction preferences in cat visual cortex

Single unit recordings were made from the visual cortex of 5 adult cats. Visual stimuli were used to determine the stimulus orientation and direction of movement preferred by cortical cells. Analysis of the sequence of neurons recorded along each electrode penetration and their direction preferences indicates that neurons preferring similar directions of movement are clustered together in the cortex.     

Motion opponency and transparency in the human middle temporal area

Motion transparency is the perception of multiple, moving surfaces within the same retinal location (for example, a ripple on the surface of a drifting stream), and is an interesting challenge to motion models because multiple velocities must be represented within the same region of space. When these motion vectors are in opposite directions, brief in duration and spatially constrained within a very local region, the result is little or no perceived motion (motion opponency). Both motion transparency and motion opponency inhibit the firing rate of single middle temporal area (MT) neurons as compared with the preferred direction alone, but neither generally influences the firing rate of primary visual cortex neurons. Surprisingly, neuroimaging studies of human middle temporal area (hMT+) have found less activation due only to motion opponency and an increase in neural responses for motion transparency. Here we parametrically manipulate the local balance between competing motion vectors and find an interaction between motion opponency and transparency in the population blood oxygen level-dependent (BOLD) response. We find reduced BOLD amplitude for motion opponency throughout visual cortex, but weakened responses due to perceptual transparency that is most apparent only within the hMT+. We interpret our results as evidence for two distinct mechanisms mediating opponency and transparency.     

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.     

Separate spatial and temporal frequency tuning to visual motion in human MT+ measured with ECoG

The human middle temporal complex (hMT+) has a crucial biological relevance for the processing and detection of direction and speed of motion in visual stimuli. Here, we characterized how neuronal populations in hMT+ encode the speed of moving visual stimuli. We evaluated human intracranial electrocorticography (ECoG) responses elicited by square‐wave dartboard moving stimuli with different spatial and temporal frequency to investigate whether hMT+ neuronal populations encode the stimulus speed directly, or whether they separate motion into its spatial and temporal components. We extracted two components from the ECoG responses: (1) the power in the high‐frequency band (HFB: 65–95 Hz) as a measure of the neuronal population spiking activity and (2) a specific spectral component that followed the frequency of the stimulus's contrast reversals (SCR responses). Our results revealed that HFB neuronal population responses to visual motion stimuli exhibit distinct and independent selectivity for spatial and temporal frequencies of the visual stimuli rather than direct speed tuning. The SCR responses did not encode the speed or the spatiotemporal frequency of the visual stimuli. We conclude that the neuronal populations measured in hMT+ are not directly tuned to stimulus speed, but instead encode speed through separate and independent spatial and temporal frequency tuning. Hum Brain Mapp 38:293–307, 2017. © 2016 Wiley Periodicals, Inc.     

Covariations in ERP and PET measures of spatial selective attention in human extrastriate visual cortex

In a previous study using positron emission tomography (PET), we demonstrated that focused attention to a location in the visual field produced increased regional cerebral blood flow in the fusiform gyrus contralateral to the attended hemifield (Heinze et al. [1994]: Nature 372:543). We related these effects to modulations in the amplitude of the P1 component (80–130 msec latency) of the visual event-related brain potentials (ERPs) recorded from the same subjects, under the identical stimulus and task conditions. Here, we replicate and extend these findings by showing that attention effects in the fusiform gyrus and the P1 component were similarly modulated by the perceptual load of the task. When subjects performed a perceptually demanding symbol-matching task within the focus of spatial attention, the fusiform activity and P1 component of the ERP were of greater magnitude than when the subjects performed a less perceptually demanding task that required only luminance detection at the attended location. In the latter condition, both the PET and ERP attention effects were reduced. In addition, in the present data significant activations were also obtained in the middle occipital gyrus contralateral to the attended hemifield, thereby demonstrating that multiple regions of extrastriate visual cortex are modulated by spatial attention. The findings of covariations between the P1 attention effect and activity in the posterior fusiform gyrus reinforce our hypothesis that common neural sources exist for these complementary, but very different measures of human brain activity. Hum. Brain Mapping 5:273–279, 1997. © 1997 Wiley-Liss, Inc.     

Sensitivity to direction and orientation of random dot stereobars in the monkey visual cortex

We are able to judge the direction of movement and orientation of objects because they have contrast-defined edges. However, we are also able to perceive the orientation and direction of movement of stereobars made of random dot stereograms in the absence of contrast-defined edges. We recorded 207 disparity-sensitive cells from visual areas V1 and V2 of two Macaca mulatta monkeys while performing an attentive fixation task. Luminance defined bars and random-dot stereo-defined bars were used to assess direction and orientation selectivity of these cells. Orientation and direction preference for luminance bars and for stereobars showed a statistically significant relationship (r=0.83, P<0.01 for direction; r=0.63, P<0.01 for orientation). However, disparity-sensitive cells from these areas seem to be more sensitive to luminance than to stereobars regarding orientation and direction of movement. Similar results were obtained when the two areas were considered separately. Our results show that cells in areas V1 and V2 of the monkey visual cortex are able to detect the orientation and direction of movement of stereobars in a manner similar to those of luminance-defined bars. This finding is relevant because to detect the direction and orientation of stereobars a comparison between left and right eye inputs is required.     

Regeneration of specific nerve cells in lesioned visual cortex of the human brain: An indirect evidence after constant stimulation with different spots of light

The defective parts of the visual field of two braininjured patients were stimulated with different spots of light. There is evidence for at least five independent visual functions which can be restored due to constant stimulation of the blind part of the visual field: (1) The constant stimulation of the blind part of the visual field with spots of white light leads to an increase of the visual field for the perception of white light only. (2) The constant stimulation with spots of light of different wavelengths leads to an increase of the visual field for different color perception. To enlarge the visual field for the perception of the color red, a light stimulus with the wavelength of 656 nanometers (nm) was used; for the visual field for the perception of the color green 525 nm; for yellow 578 nm; and for blue 450 nm. (3) The constant stimulation of the blind visual field with black and white light bars of different orientations and constellations leads to an increase of the foveal acuity and an improvement of form perception in the periphery of the visual field. The results suggest that the recovery of visual functions, different color perception and form perception, may depend upon neuronal regeneration in the human visual cortex; regeneration occurs with adequate and constant stimulation of its specific neurons. © 1995 Wiley-Liss, Inc.     

Hemifield effects of spatial attention in early human visual cortex

Early visual areas (V1, V2, V3/VP, V4v) contain representations of the contralateral hemifield within each hemisphere. Little is known about the role of the visual hemifields along the visuo-spatial attention processing hierarchy. It is hypothesized that attentional information processing is more efficient across the hemifields (known as bilateral field advantage) and that the integration of information is greater within one hemifield as compared with across the hemifields. Using functional magnetic resonance imaging we examined the effect of distance and hemifield on parallel attentional processing in the early visual areas (V1-V4v) at individually mapped retinotopic locations aligned adjacently or separately within or across the hemifields. We found that the bilateral field advantage in parallel attentional processing over separated attended locations can be assigned, at least partly, to differences in distractor position integration in early visual areas. These results provide evidence for a greater integration of locations between two attended locations within one hemifield than across both hemifields. This nicely correlates with behavioral findings of a bilateral field advantage in parallel attentional processing (when distractors in between cannot be excluded) and a unilateral field advantage if attention has to be shifted across separated locations (when locations in between were integrated).     

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.     

Retinotopic distribution of chromatic responses in human primary visual cortex

In non-human primates at least three anatomically and functionally distinct channels convey signals from the retina to the primary visual cortex (V1). Two of these channels, the parvocellular and the koniocellular, are sensitive to chromatic contrasts and form the basis of color vision. In humans, common phylogenetic history with other primates and psychophysical experiments suggest identical retinocortical mechanisms but separate evaluation of the distinct anatomical channels has been difficult because signals are already combined in V1. We studied the spatial distribution of activation to chromatic stimuli along the two opponent chromatic axes in human V1 with multifocal functional magnetic resonance imaging. The signal strength was quantified from three experiments with stimuli up to 20 degrees eccentricity. The hypothesis was that, although the parvo- and koniocellular signals are mixed in V1, distinct distributions of signal strength would be evident. We found that whereas different conditions activated the same areas of cortex, indicating that they have identical magnification factors, the responses to red/green stimulation were stronger close to the fovea whereas the blue/yellow responses were much less diminished with increasing eccentricity. Both chromatic axes showed saturating contrast response functions. Our measure directly from human V1 is in line with earlier psychophysical studies suggesting relatively stronger parvocellular channel representation close to the fovea, and more uniform distribution of the koniocellular and achromatic channels. In addition, our study presents a way to rapidly quantify retinotopic signal transmission in distinct retinocortical pathways of individual subjects.     

Functional organization of human visual cortex in occipital polymicrogyria

Polymicrogyrias (PMG) are cortical malformations resulting from developmental abnormalities. In animal models PMG has been associated with abnormal anatomy, function, and organization. The purpose of this study was to describe the function and organization of human polymicrogyric cortex using functional magnetic resonance imaging. Three patients with epilepsy and bilateral parasagittal occipital polymicrogyri were studied. They all had normal vision as tested by Humphrey visual field perimetry. The functional organization of the visual cortex was reconstructed using phase-encoded retinotopic mapping analysis. This method sequentially stimulates each point in the visual field along the axes of a polar-coordinate system, thereby reconstructing the representation of the visual field on the cortex. We found normal cortical responses and organization of early visual areas (V1, V2, and V3/VP). The locations of these visual areas overlapped substantially with the PMG. In five out of six hemispheres the reconstructed primary visual cortex completely fell within polymicrogyric areas. Our results suggest that human polymicrogyric cortex is not only organized in a normal fashion, but is also actively involved in processing of visual information and contributes to normal visual perception.     

Distinct mechanisms for size tuning in primate visual cortex

Most neurons in primary visual cortex (V1) are selective for stimulus size, a property with important implications for salient feature detection. Size selectivity involves dynamic interactions between neuronal circuits that establish the classical (center) and extraclassical (surround) of a neuron's receptive field. Although much is known about the tuning properties and stimulus selectivity of the center and surround subunits, relatively little is known about how these subunits interact to achieve size selectivity. To address this question, we examined the temporal dynamics of size selectivity in two classes of pyramidal neurons at similar hierarchical processing stages in V1 of alert monkeys. These two classes were comprised of neurons in cortical layer 6 with identified projections to the lateral geniculate nucleus. While both neuronal groups displayed comparable levels of size selectivity, the temporal dynamics of their tuning differed significantly. We compared the size tuning profiles of each cell type with a series of sum-of-Gaussian models and discovered that the receptive fields of neurons with fast-conducting axons contained an excitatory center and a suppressive surround with similar onset timing. In contrast, neurons with slow-conducting axons used two center components-an early wide-field component and a delayed narrow-field component that increased activity-in addition to the surround component. The early, wide-field component represents a novel mechanism for cortical neurons to integrate contextual information. These results demonstrate that size tuning in cortical neurons is established via multiple unique mechanisms, dictated by the rich circuit architecture in which neurons are embedded.     

Motion opponency examined throughout visual cortex with multivariate pattern analysis of fMRI data

This study explores how the human brain solves the challenge of flicker noise in motion processing. Despite providing no useful directional motion information, flicker is common in the visual environment and exhibits omnidirectional motion energy which is processed by low‐level motion detectors. Models of motion processing propose a mechanism called motion opponency that reduces flicker processing. Motion opponency involves the pooling of local motion signals to calculate an overall motion direction. A neural correlate of motion opponency has been observed in human area MT+/V5, whereby stimuli with perfectly balanced motion energy constructed from dots moving in counter‐phase elicit a weaker response than nonbalanced (in‐phase) motion stimuli. Building on this previous work, we used multivariate pattern analysis to examine whether the activation patterns elicited by motion opponent stimuli resemble that elicited by flicker noise across the human visual cortex. Robust multivariate signatures of opponency were observed in V5 and in V3A. Our results support the notion that V5 is centrally involved in motion opponency and in the reduction of flicker. Furthermore, these results demonstrate the utility of multivariate analysis methods in revealing the role of additional visual areas, such as V3A, in opponency and in motion processing more generally.     

Spatio‐temporal dynamics of adaptation in the human visual system: a high‐density electrical mapping study

When sensory inputs are presented serially, response amplitudes to stimulus repetitions generally decrease as a function of presentation rate, diminishing rapidly as inter‐stimulus intervals (ISIs) fall below 1 s. This ‘adaptation’ is believed to represent mechanisms by which sensory systems reduce responsivity to consistent environmental inputs, freeing resources to respond to potentially more relevant inputs. While auditory adaptation functions have been relatively well characterized, considerably less is known about visual adaptation in humans. Here, high‐density visual‐evoked potentials (VEPs) were recorded while two paradigms were used to interrogate visual adaptation. The first presented stimulus pairs with varying ISIs, comparing VEP amplitude to the second stimulus with that of the first (paired‐presentation). The second involved blocks of stimulation (N = 100) at various ISIs and comparison of VEP amplitude between blocks of differing ISIs (block‐presentation). Robust VEP modulations were evident as a function of presentation rate in the block‐paradigm, with strongest modulations in the 130–150 ms and 160–180 ms visual processing phases. In paired‐presentations, with ISIs of just 200–300 ms, an enhancement of VEP was evident when comparing S2 with S1, with no significant effect of presentation rate. Importantly, in block‐presentations, adaptation effects were statistically robust at the individual participant level. These data suggest that a more taxing block‐presentation paradigm is better suited to engage visual adaptation mechanisms than a paired‐presentation design. The increased sensitivity of the visual processing metric obtained in the block‐paradigm has implications for the examination of visual processing deficits in clinical populations.     

Unidirectional visual motion adaptation induces reciprocal inhibition of human early visual cortex excitability

ObjectivesBehavioural observations provided by the waterfall illusion suggest that motion perception is mediated by a comparison of responsiveness of directional selective neurones. These are proposed to be optimally tuned for motion detection in different directions. Critically however, despite the behavioural observations, direct evidence of this relationship at a cortical level in humans is lacking. By utilising the state dependant properties of transcranial magnetic stimulation (TMS), one can probe the excitability of specific neuronal populations using the perceptual phenomenon of phosphenes.MethodWe exposed subjects to unidirectional visual motion adaptation and subsequently simultaneously measured early visual cortex (V1) excitability whilst viewing motion in the adapted and non-adapted direction.ResultFollowing adaptation, the probability of perceiving a phosphene whilst viewing motion in the adapted direction was diminished reflecting a reduction in V1 excitability. Conversely, V1 excitability was enhanced whilst viewing motion in the opposite direction to that used for adaptation.ConclusionOur results provide support that in humans a process of reciprocal inhibition between oppositely tuned directionally selective neurones in V1 facilitates motion perception.SignificanceThis paradigm affords a unique opportunity to investigate changes in cortical excitability following peripheral vestibular disorders.     

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.     

Effects of EEG-vigilance regulation patterns on early perceptual processes in human visual cortex

ObjectiveTo investigate influences of EEG-vigilance regulation patterns on perceptual processing during sustained visual attention in early visual areas.MethodsWe compared a subject group with stable vigilance regulation to a group with unstable EEG-vigilance regulation. A rapid serial visual presentation stream (RSVP) elicited a 7.5 Hz steady state visual evoked potential (SSVEP), a continuous sinusoidal brain response as a measure of attentional resource allocation during sustained attention in early visual cortex. Subjects performed a target discrimination task. 150 trials were divided into two parts (75 trials each, trial duration: 11 s).ResultsA significant interaction vigilance group by experimental part provided significantly greater SSVEP amplitudes for the unstable group in the second compared to the first part of the experiment. Both groups showed training effects with increased hit rates and d′-values in the second part of the experiment.ConclusionsThe unexpected finding of SSVEP amplitude increase for the unstable group might be due to competitive interactions for neural resources between the alpha response and SSVEPs.SignificanceIndividual patterns of EEG-vigilance regulation have a moderate impact on early sensory processing during sustained visual attention that is not paralleled in task performance.     

Directional anisotropy of motion responses in retinotopic cortex

Recently, evidence has emerged for a radial orientation bias in early visual cortex. These results predict that in early visual cortex a tangential bias should be present for motion direction. We tested this prediction in a human imaging study, using a translating random dot pattern that slowly rotated its motion direction 360° in cycles of 54 s. In addition, polar angle and eccentricity mapping were performed. This allowed the measurement of the BOLD response across the visual representations of the different retinotopic areas. We found that, in V1, V2, and V3, BOLD responses were consistently enhanced for centrifugal and centripetal motion, relative to tangential motion. The relative magnitude of the centrifugal and centripetal response biases changed with visual eccentricity. We found no motion direction biases in MT+. These results are in line with previously observed anisotropies in motion sensitivity across the visual field. However, the observation of radial motion biases in early visual cortex is surprising considering the evidence for a radial orientation bias. An additional experiment was performed to resolve this apparent conflict in results. The additional experiment revealed that the observed motion direction biases most likely originate from anisotropies in long range horizontal connections within visual cortex. Hum Brain Mapp, 2009. © 2009 Wiley‐Liss, Inc.