Chromatic sensitivity of neurones in area MT of the anaesthetised macaque monkey compared to human motion perception

We recorded activity from neurones in cortical motion-processing areas, middle temporal area (MT) and middle posterior superior temporal sulcus (MST), of anaesthetised and paralysed macaque monkeys in response to moving sinewave gratings modulated in luminance and chrominance. The activity of MT and MST neurones was highly dependent on luminance contrast. In three of four animals isoluminant chromatic modulations failed to activate MT/MST neurones significantly. At low luminance contrast a systematic dependence on chromaticity was revealed, attributable mostly to residual activity of the magnocellular pathway. Additionally, we found indications for a weak S-cone input, but rod intrusion could also have made a contribution. In contrast to the activity of MT and MST neurones, speed judgments and onset amplitude of evoked optokinetic eye movements in human subjects confronted with equivalent visual stimuli were largely independent of luminance modulation. Motion of every grating (including isoluminant) was readily visible for all but one observer. Similarity with the activity of MT/MST cells was found only for motion-nulling equivalent luminance contrast judgments at isoluminance. Our results suggest that areas MT and MST may not be involved in the processing of chromatic motion, but effects of central anaesthesia and/or the existence of intra- and inter-species differences must also be considered.     

Parvocellular and Magnocellular Contributions to the Initial Generators of the Visual Evoked Potential: High-Density Electrical Mapping of the “C1” Component

The C1 component of the VEP is considered to index initial afference of retinotopic regions of human visual cortex (V1 and V2). C1 onsets over central parieto–occipital scalp between 45 and 60 ms, peaks between 70 and 100 ms, and then resolves into the following P1 component. By exploiting isoluminant and low-contrast luminance stimuli, we assessed the relative contributions of the Magnocellular (M) and Parvocellular (P) pathways to generation of C1. C1 was maximal at 88 ms in a 100% luminance contrast condition (which stimulates both P and M pathways) and at 115 ms in an isoluminant chromatic condition (which isolates contributions of the P pathway). However, in a 4% luminance contrast condition (which isolates the M pathway), where the stimuli were still clearly perceived, C1 was completely absent. Absence of C1 in this low contrast condition is unlikely to be attributable to lack of stimulus energy since a robust P1–N1 complex was evoked. These data therefore imply that C1 may be primarily parvocellular in origin. The data do not, however, rule out some contribution from the M system at higher contrast levels. Nonetheless, that the amplitude of C1 to P-isolating isoluminant chromatic stimuli is equivalent to that evoked by 100% contrast stimuli suggests that even at high contrast levels, the P system is the largest contributor. These data are related to intracranial recordings in macaque monkeys that have also suggested that the initial current sink in layer IV may not propagate effectively to the scalp surface when M-biased stimuli are used. We also discuss how this finding has implications for a long tradition of attention research that has␣used C1 as a metric of initial V1 afference in humans. C1 has been repeatedly interrogated for potential selective attentional modulations, particularly in spatial attentional designs, under the premise that modulation of this component, or lack thereof, would be evidence for or against selection at the initial inputs to visual cortex. Given the findings here, we would urge that in interpreting C1 effects, a consideration of the dominant cellular contributions will be necessary. For example, it is plausible that spatial attention mechanisms could operate primarily through the M system and that as such C1 may not always represent an adequate dependent measure in such studies.     

Human VEPs to isoluminant chromatic and achromatic sinusoidal gratings: Separation of parvocellular components

Summary To extract the responses specific to the parvocellular system (color vision and form perception) in humans, visual evoked potentials (VEPs) in response to the onset of isoluminant chromatic (red-green) and achromatic (black-white) sinusoidal gratings were recorded in 15 young adults. Chromatic stimulation evoked a characteristic negative wave (N1) with peak latencies around 120 msec. The amplitude resembled an inverse U-shaped function against the spatial frequency with a peak at 2 c/deg. In contrast, VEPs to achromatic gratings showed different spatial frequency characteristics with a peak at 5.3 c/deg. With variations in the luminous intensity ratio between the red and green gratings, N1 was seen to respond maximally to isoluminant stimulation. These results indicate that the combined use of isoluminant chromatic and achromatic patterns could stimulate the parvocellular system selectively in humans.     

Wiener Filter-Magnetoencephalography of Visual Cortical Activity

This paper reports a revised Wiener filter to resolve the inverse problem for magnetoencephalograms (MEGs) according to the structural and functional constraints based on magnetic resonance imaging (MRI) and functional magnetic resonance imaging (fMRI). Wiener filter-MEG imaging for half field stimulation with the chromatic stimulus resolved fast, slow and late responses in V1, V4 and the inferotemporal cortex, respectively. The time courses of these responses were roughly comparable with those reported by unit recording studies of the corresponding monkey visual cortical areas. Wiener filter-MEG imaging had comparable spatial resolution and better signal to noise ratio than fMRI. The background noise was robust in fMRI responses, but became virtually eliminated in Wiener filter responses. Wiener filter-MEG imaging with upper and lower quadrant field stimulation demonstrated V1 responses differentially distributed respectively in the lower and upper banks of the calcarine sulcus. These results demonstrate that responses in two cortical areas facing close to each other can be resolved by Wiener filter-MEG. The present method provides a way to image brain activities with millisecond- and millimeter-order spatiotemporal resolution.     

Smooth pursuit eye movements to isoluminant targets

At slow speeds, chromatic isoluminant stimuli are perceived to move much slower than comparable luminance stimuli. We investigated whether smooth pursuit eye movements to isoluminant stimuli show an analogous slowing. Beside pursuit speed and latency, we studied speed judgments to the same stimuli during fixation and pursuit. Stimuli were either large sine wave gratings or small Gaussians blobs moving horizontally at speeds between 1 and 11 degrees /s. Targets were defined by luminance contrast or color. Confirming prior studies, we found that speed judgments of isoluminant stimuli during fixation showed a substantial slowing when compared with luminance stimuli. A similarly strong and significant effect of isoluminance was found for pursuit initiation: compared with luminance targets of matched contrasts, latencies of pursuit initiation were delayed by 50 ms at all speeds and eye accelerations were reduced for isoluminant targets. A small difference was found between steady-state eye velocities of luminance and isoluminant targets. For comparison, we measured latencies of saccades to luminance and isoluminant stimuli under similar conditions, but the effect of isoluminance was only found for pursuit. Parallel psychophysical experiments revealed that different from speed judgments of moving isoluminant stimuli made during fixation, judgments during pursuit are veridical for the same stimuli at all speeds. Therefore information about target speed seems to be available for pursuit eye movements and speed judgments during pursuit but is degraded for perceptual speed judgments during fixation and for pursuit initiation.     

Face specific broadband electrocorticographic spectral power change in the rhinal cortex

Recent studies have revealed additional face areas in the anterior temporal lobe in addition to the 'core' face areas (fusiform face area, occipital face area, and face area in the superior temporal sulcus). The electrocorticogram of a patient who underwent implantation of subdural grid electrodes in the right anterior ventral temporal lobe revealed a strong face-specific response both in event-related potentials (ERP) and in the induced broadband spectral power change at an electrode located on the anterior collateral sulcus, straddling the border between the perirhinal and entorhinal cortices. The ERP and induced broadband power changes were highly specific to facial stimuli, which was obvious even in a single trial analysis. The face-specific response was recorded in an area with perfect overlap of the 'anterior temporal face patch' in the anterior collateral sulcus, proposed based on human functional magnetic resonance imaging (fMRI) results. A recent fMRI study in monkeys reported a face-specific visual response in the rhinal cortex, suggesting that the basic structural configuration of face responsive areas are preserved across species. Although the rhinal cortex has long been regarded as part of the memory system, recent data suggest that it also plays a role in perception. The face-specific response in the present study might reflect visual processing based on complex conjunctions of visual features required for facial processing.     

Form and motion from colour in cerebral achromatopsia

Patients with cerebral achromatopsia, resulting from damage to ventromedial occipital cortex, cannot chromatically order, or discriminate, hue. Nevertheless, their chromatic contrast sensitivity can be indistinguishable from that of normal observers. A possible contributor to the detectability of chromatic gratings is the subadditive nature of certain colour combination such that mixtures of, for example, red and green (yielding yellow) appear dimmer than expected from the simple addition of luminances. This subadditivity is believed to reflect colour-opponent interactions between the outputs of long- and medium-wavelength cones. We performed a first-order compensation for such subadditivity in chromatic gratings and demonstrated that their detection was still not abolished in an achromatopsic patient. In addition, we used a two-alternative forced-choice procedure with an achromatopsic patient, who was required to judge the apparent relative velocity of two drifting gratings with different degrees of compensation for subadditivity. It is well known that isoluminant gratings, constructed by adding a red and green sinusoidal grating of identical peak luminances in antiphase, appear to drift substantially slower than an achromatic grating with the same velocity. Adding 2f luminance compensation to an isoluminant grating of spatial frequency f, resulted in an identical minimum of perceived velocity at a compensation contrast of 5% in both achromatopsics and normal observers. Furthermore, while compensation for subadditivity did not substantially compromise grating detection at low contrasts, such correction severely affected motion detection. Saccadic eye movement accuracy and latency were also measured to uncompensated chromatic, compensated chromatic and achromatic targets. We conclude first that subadditivity, resulting from colour-opponent P-channel processes, influences motion judgements. The ability to extract motion from chromatic differences alone is little, if at all, different in achromatopsic and normal vision. Second, the paradoxical detection of sinusoidally modulated chromatic gratings in achromatopsic patients is not merely a result of subadditivity. Third, saccadic latency, but not accuracy, to chromatic targets is affected by luminance compensation. Finally, and more generally, wavelength processing continues to contribute to several aspects of visual processing even when colour is not perceived.     

Loss of visual information in neglect: the effect of chromatic- versus luminance-contrast stimuli in a “what” task

One to four vertical bars were tachistoscopically presented at various eccentricities along the horizontal meridian to patients with right brain damage and neglect (n=7) and to a control group of right brain damaged patients without neglect (n=4). Luminance contrast stimuli and isoluminant chromatic contrast stimuli were used. The patients task was to report the number of bars. With luminance stimuli the neglect patients discrimination in the left visual field was reduced, particularly at the most leftward position tested (ca 20°) where about 20% of the bars were omitted. The loss of information was limited to luminance contrast stimuli. When chromatic contrast stimuli were used, accuracy was comparable in the two hemifields and between groups of patients. The differential pattern of results for chromatic and luminance contrast stimuli is consistent with the hypothesis of a selective deficit of the magno-cellular pathway in neglect.     

The physiological basis of attentional modulation in extrastriate visual areas.

Selective attention to color or motion enhances activity in specialized areas of extrastriate cortex, but mechanisms of attentional modulation remain unclear. By dissociating modulation of visually evoked transient activity from the baseline for a particular attentional set, human functional neuroimaging was used to investigate the physiological basis of such effects. Baseline activity in motion- and color-sensitive areas of extrastriate cortex was enhanced by selective attention to these attributes, even without moving or colored stimuli. Further, visually evoked responses increased along with baseline activity. These results are consistent with the hypothesis that attention modulates sensitivity of neuronal populations to inputs by changing background activity.     

Alternating optokinetic nystagmus (OKN) induced by intermittent display of stationary gratings

In this paper, we report a novel optokinetic nystagmus (OKN), which was evoked by stationary gratings presented intermittently. OKN eye movements were accurately measured by the electromagnetic scleral search-coil technique. For the luminance stimuli, alternating OKN was elicited when the interstimulus interval (ISI) ranged from 33 to 83 ms duration and the ISI luminance approximated to the mean luminance of the stimulus grating; for chromatic (red/green) stimuli, the OKN could be evoked in non-isoluminant condition and vanished in the isoluminant condition. It is a plausible explanation that the present OKN, intermittent display-of-gratings-induced OKN (IDG-OKN), might be related to the temporal impulse response of the luminance channel in vision.     

Human visual cortex responds to invisible chromatic flicker

When two isoluminant colors alternate at frequencies of 25 Hz or higher, observers perceive only one fused color. Chromatic flicker beyond the fusion frequency induces flicker adaptation in human observers and stimulates monkey V1 neurons. Here we use functional magnetic resonance imaging (fMRI) to show that many human visual cortical areas, with the exception of VO, can distinguish between fused chromatic flicker and its matched nonflickering control. This result supports the existence of significant intracortical temporal filtering of high-frequency chromatic information. The result also suggests that a considerable difference in cortical activation in many visual cortical areas does not necessarily lead to different conscious experiences.     

Extrastriate body area in human occipital cortex responds to the performance of motor actions

A region in human lateral occipital cortex (the 'extrastriate body area' or EBA) has been implicated in the perception of body parts. Here we report functional magnetic resonance imaging (fMRI) evidence that the EBA is strongly modulated by limb (arm, foot) movements to a visual target stimulus, even in the absence of visual feedback from the movement. Therefore, the EBA responds not only during the perception of other people's body parts, but also during goal-directed movements of the observer's body parts. In addition, both limb movements and saccades to a detected stimulus produced stronger signals than stimulus detection without motor movements ('covert detection') in the calcarine sulcus and lingual gyrus. These motor-related modulations cannot be explained by simple visual or attentional factors related to the target stimulus, and suggest a potentially widespread influence of actions on visual cortex.     

Diffusion tensor imaging shows white matter tracts between human auditory and visual cortex

Although it is known that sounds can affect visual perception, the neural correlates for crossmodal interactions are still disputed. Previous tracer studies in non-human primates revealed direct anatomical connections between auditory and visual brain areas. We examined the structural connectivity of the auditory cortex in normal humans by diffusion-weighted tensor magnetic resonance imaging and probabilistic tractography. Tracts were seeded in Heschl's region or the planum temporale. Fibres crossed hemispheres at the posterior corpus callosum. Ipsilateral fibres seeded in Heschl's region projected to the superior temporal sulcus, the supramarginal gyrus and intraparietal sulcus and the occipital cortex including the calcarine sulcus. Fibres seeded in the planum temporale terminated primarily in the superior temporal sulcus, the supramarginal gyrus, the central sulcus and adjacent regions. Our findings suggest the existence of direct white matter connections between auditory and visual cortex--in addition to subcortical, temporal and parietal connections.     

Peaked encoding of relative luminance in macaque areas V1 and V2

It is widely presumed that throughout the primate visual pathway neurons encode the relative luminance of objects (at a given light adaptation level) using two classes of monotonic function, one positively and the other negatively sloped. Based on computational considerations, we hypothesized that early visual cortex also contains neurons preferring intermediate relative luminance values. We tested this hypothesis by recording from single neurons in areas V1 and V2 of alert, fixating macaque monkeys during presentation of a large, spatially uniform patch oscillating slowly in luminance and surrounded by a static texture background. A substantial subset of neurons responsive to such low spatial frequency luminance stimuli in both areas exhibited prominent and statistically reliable response peaks to intermediate rather than minimal or maximal luminance values. When presented with static patches of different luminance but of the same spatial configuration, most neurons tested retained a preference for intermediate relative luminance. Control experiments using luminance modulation at multiple low temporal frequencies or reduced amplitude indicate that in the slow luminance-oscillating paradigm, responses were more strongly modulated by the luminance level than the rate of luminance change. These results strongly support our hypothesis and reveal a striking cortical transformation of luminance-related information that may contribute to the perception of surface brightness and lightness. In addition, we tested many luminance-sensitive neurons with large chromatic patches oscillating slowly in luminance. Many cells, including the gray-preferring neurons, exhibited strong color preferences, suggesting a role of luminance-sensitive cells in encoding information in three-dimensional color space.     

The effect of lesions to cortical areas V4 or AIT on pupillary responses to chromatic and achromatic stimuli in monkeys

We measured the pupillary response to achromatic and chromatic grating stimuli in left and right visual hemifields of two rhesus monkeys, who were trained to fixate the centre of a screen. After removing the rostral inferior temporal cortex of one hemisphere, the response to chromatically modulated gratings in the contralateral hemifield was abolished, whereas the response to the luminance modulated grating was unaffected. In one of the monkeys, in which area V4 of the other hemisphere was also removed, there was no effect on the pupillary response to either kind of grating presented in the hemifield contralateral to the V4 lesion. The results show that the cortical contribution to the response of the pupil to purely chromatic changes is mediated by rostral temporal cortex, not by area V4.     

Temporal analysis of the flow from V1 to the extrastriate cortex in humans

We previously examined the cortical processing in response to somatosensory, auditory and noxious stimuli, using magnetoencephalography in humans. Here, we performed a similar analysis of the processing in the human visual cortex for comparative purposes. After flash stimuli applied to the right eye, activations were found in eight cortical areas: the left medial occipital area around the calcarine fissure (primary visual cortex, V1), the left dorsomedial area around the parietooccipital sulcus (DM), the ventral (MOv) and dorsal (MOd) parts of the middle occipital area of bilateral hemispheres, the left temporo-occipito-parietal cortex corresponding to human MT/V5 (hMT), and the ventral surface of the medial occipital area (VO) of the bilateral hemispheres. The mean onset latencies of each cortical activity were (in ms): 27.5 (V1), 31.8 (DM), 32.8 (left MOv), 32.2 (right MOv), 33.4 (left MOd), 32.3 (right MOv), 37.8 (hMT), 46.9 (left VO), and 46.4 (right VO). Therefore the cortico-cortical connection time of visual processing at the early stage was 4-6 ms, which is very similar to the time delay between sequential activations in somatosensory and auditory processing. In addition, the activities in V1, MOd, DM, and hMT showed a similar biphasic waveform with a reversal of polarity after 10 ms, which is a common activation profile of the cortical activity for somatosensory, auditory, and pain-evoked responses. These results suggest similar mechanisms of the serial cortico-cortical processing of sensory information among all sensory areas of the cortex.     

The spatial transformation of color in the primary visual cortex of the macaque monkey

Perceptually, color is used to discriminate objects by hue and to identify color boundaries. The primate retina and the lateral geniculate nucleus (LGN) have cell populations sensitive to color modulation, but the role of the primary visual cortex (V1) in color signal processing is uncertain. We re-evaluated color processing in V1 by studying single-neuron responses to luminance and to equiluminant color patterns equated for cone contrast. Many neurons respond robustly to both equiluminant color and luminance modulation (color-luminance cells). Also, there are neurons that prefer luminance (luminance cells), and a few neurons that prefer color (color cells). Surprisingly, most color-luminance cells are spatial-frequency tuned, with approximately equal selectivity for chromatic and achromatic patterns. Therefore, V1 retains the color sensitivity provided by the LGN, and adds spatial selectivity for color boundaries.     

Grasping isoluminant stimuli

We used a virtual reality setup to let participants grasp discs, which differed in luminance, chromaticity and size. Current theories on perception and action propose a division of labor in the brain into a color proficient perception pathway and a less color-capable action pathway. In this study, we addressed the question whether isoluminant stimuli, which provide only a chromatic but no luminance contrast for action planning, are harder to grasp than stimuli providing luminance contrast or both kinds of contrast. Although we found that grasps of isoluminant stimuli had a slightly steeper slope relating the maximum grip aperture to disc size, all other measures of grip quality were unaffected. Overall, our results do not support the view that isoluminance of stimulus and background impedes the planning of a grasping movement.     

fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation

Small-field optokinetic nystagmus (OKN) was performed in seven healthy volunteers in order to analyze the activation and deactivation patterns of visual motion, ocular motor, and multisensory vestibular cortex areas by means of fMRI during coherent visual motion stimulation. BOLD signal decreases (deactivations) were found in the first and second long insular gyri and retroinsular areas (the human homologue of the parietoinsular vestibular cortex and the visual posterior sylvian area in the monkey) of both hemispheres, extending into the transverse temporal gyrus and inferior-anterior parts of the superior temporal gyrus (BA 22), and the precentral gyri at two separate sites (BA 4 and 6). Further deactivations were found in cranioposterior parts of the superior temporal gyrus (BA 22) and the adjacent inferior parietal lobule (BA 40), anterior cingulate gyrus, hippocampus, and corpus callosum. Most of these BOLD signal decreases involved parts of the "multisensory vestibular cortical circuit". These findings support the concept of a reciprocally inhibitory visual–vestibular interaction that has now been demonstrated not only for large-field visual motion stimulation that induces vection (without eye movements) but also for optokinetically induced eye movements (without vection). The functional significance of this concept may be related to the perception of self-motion, since both large-field visual motion stimulation and optokinetic nystagmus are linked to the visual control of self-motion. With respect to activation of the cortical ocular motor system two separate and distinct areas of activations were delineated in the precentral sulcus of both hemispheres, one ventrolaterally (in BA 9) and the other dorsomedially at the junction of the superior frontal sulcus with the precentral sulcus (in BA 6). Both probably correspond to different subregions of the frontal eye field and the premotor cortex for the ocular motor performance of OKN. Electronic Publication