Yves Trotter

Dynamics of orientation coding in area V1 of the awake primate.

To investigate the importance of feedback loops in visual information processing, we have analyzed the dynamic aspects of neuronal responses to oriented gratings in cortical area V1 of the awake primate. If recurrent feedback is important in generating orientation selectivity, the initial part of the neuronal response should be relatively poorly selective, and full orientation selectivity should only appear after a delay. Thus, by examining the dynamics of the neuronal responses it should be possible to assess the importance of feedback processes in the development of orientation selectivity. The results were base on a sample of 259 cells recorded in two monkeys, of which 89% were visually responsive. Of these, approximately two-thirds were orientation selective. Response latency varied considerably between neurons, ranging from a minimum of 41 ms to over 150 ms, although most had latencies of 50-70 ms. Orientation tuning (defined as the bandwidth at half-height) ranged from 16 deg to over 90 deg, with a mean value of around 55 deg. By examining the selectivity of these different neurons by 10-ms time slices, starting at the onset of the neuronal response, we found that the orientation selectivity of virtually every neuron was fully developed at the very start of the neuronal response. Indeed, many neurons showed a marked tendency to respond at somewhat longer latencies to stimuli that were nonoptimally oriented, with the result that orientation selectivity was highest at the very start of the neuronal response. Furthermore, there was no evidence that the neurons with the shortest onset latencies were less selective. Such evidence is inconsistent with the hypothesis that recurrent intracortical feedback plays an important role in the generation of orientation selectivity. Instead, we suggest that orientation selectivity is primarily generated using feedforward mechanisms, including feedforward inhibition. Such a strategy has the advantage of allowing orientation to be computed rapidly, and avoids the initially poorly selective neuronal responses that characterize processing involving recurrent loops.

Gaze direction controls response gain in primary visual-cortex neurons.

To localize objects in space, the brain needs to combine information about the position of the stimulus on the retinae with information about the location of the eyes in their orbits. Interaction between these two types of information occurs in several cortical areas, but the role of the primary visual cortex (area V1) in this process has remained unclear. Here we show that, for half the cells recorded in area V1 of behaving monkeys, the classically described visual responses are strongly modulated by gaze direction. Specifically, we find that selectivity for horizontal retinal disparity—the difference in the position of a stimulus on each retina which relates to relative object distance—and for stimulus orientation may be present at a given gaze direction, but be absent or poorly expressed at another direction. Shifts in preferred disparity also occurred in several neurons. These neural changes were most often present at the beginning of the visual response, suggesting a feedforward gain control by eye position signals. Cortical neural processes for encoding information about the three-dimensional position of a stimulus in space therefore start as early as area V1.

Photophobia in migraine: an interictal PET study of cortical hyperexcitability and its modulation by pain

Objective Photophobia is an abnormal sensitivity to light experienced by migraineurs and is perhaps caused by cortical hyperexcitability. In clinical studies, an inter-relation between light perception and trigeminal nociception has been demonstrated in migraineurs but not in controls. The purpose of the study was to verify this interaction by functional imaging. Methods The authors used H2O15 positron emitting tomography (PET) to study the cortical responses of seven migraineurs between attacks and the responses of seven matched control subjects to luminous stimulations at three luminance intensities: 0, 600 and 1800 Cd/m2. All three intensities were both with and without concomitant trigeminal pain stimulation. In order to facilitate habituation, the stimulations were started 30 s before PET acquisitions. Results When no concomitant pain stimulation was applied, luminous stimulations activated the visual cortex bilaterally in migraineurs (specifically in the cuneus, lingual gyrus and posterior cingulate cortex) but not in controls. Concomitant pain stimulation allowed visual cortex activation in control subjects and potentiated its activation in migraineurs. These activations by luminous stimulations were luminance-intensity-dependent in both groups. Concomitant stimulation by pain was associated with activation of the posterior parietal cortex (BA7) in migraineurs and controls. Interpretation The study shows the lack of habituation and/or cortical hyperexcitability to light in migraineurs. Moreover, the activation by light of several visual cortex areas (including the primary visual cortex) was potentiated by trigeminal pain, demonstrating multisensory integration in these areas.

Privileged Processing of the Straight-Ahead Direction in Primate Area V1

Gaze direction modulates the gain of neurons in most of the visual cortex, including the primary visual (V1) area. These gain modulations are thought to support a mechanism involved in the spatial localization of objects. In the present study, we show that part of them may reflect an additional function: enhancing the visual processing of the objects located straight ahead. Using single- and multiunit recordings in behaving macaques, we found that in peripheral V1, the gain of most neurons increases as their receptive fields (RF) are brought closer to the straight-ahead direction by changing the direction of gaze. No such tendency was observed in central V1, although the influence of gaze direction is similar in term of strength. This previously unknown organization of the gaze-related gain modulations might insure that objects located straight ahead still receive a privileged processing during eccentric fixation, reflecting the ecological importance of this particular egocentric direction.

Privileged visual processing of the straight-ahead direction in humans.

At any moment, the objects we face are endowed with a special behavioral status, either as potential obstacles during navigation or as optimal targets for visually guided actions. Yet, the gaze frequently jumps from one location to another when exploring the visual surroundings, so that objects located straight-ahead are often seen from the corner of the eyes. In the present study, we tested the hypothesis that peripheral vision might nevertheless ensure a privileged processing of these behaviorally important objects. Human subjects were asked to respond as fast as possible to the appearance of visual objects in their peripheral field of view while gazing successively in different directions. The visual objects formed similar images on the retina and differed only with respect to their egocentric location: either straight-ahead or eccentric with respect to the head/body midline. We found that straight-ahead objects elicit consistently shorter behavioral responses than eccentric objects (median difference of at least 10 ms). Additional experiments indicate that neither binocular visual cues nor full attentional resources play a fundamental role in this mechanism, and that it cannot be resumed to a simple preference for objects contralateral to the direction of gaze. These results are in agreement with recent electrophysiological findings showing that the early integration of gaze-related signals in the visual cortex of macaque monkeys lead to a higher neuronal sensitivity to the straight-ahead direction.

Neural correlates of chromostereopsis: An evoked potential study

Chromostereopsis is an illusion of depth arising from colour contrast: ocular chromatic aberrations usually make red appear closer to the viewer than blue. Whereas this phenomenon is widely documented from the optical and psychophysical point of view, its neural correlates have not been investigated. To determine the cortical processing of this colour-based depth effect, visual evoked potentials (VEPs) to contrasts of colour were recorded in 25 subjects. Chromostereopsis was found with the stimuli combining spectra extremes. VEP amplitude but not latency effects were observed to colour depth cues, suggesting an underlying, depth-specific slow negative wave, located using source modelling first in occipito-parietal, parietal, then temporal areas. The component was larger over the right hemisphere consistent with RH dominance in depth processing, likely due to context-dependent top-down modulation. These results demonstrate that the depth illusion obtained from contrast of colour implicates similar cortical areas as classic binocular depth perception.

Temporal limits of the susceptibility of depth perception to proprioceptive deafferentations of extraocular muscles

In a previous study, extraocular muscle proprioception (E.O.M.P.) was shown to play an important role in the postnatal development of depth perception: following unilateral or bilateral sections of the ophthalmic branch of the trigeminal nerve (V1th nerve) performed at 6-8 weeks of age, the binocular thresholds were 2 to 3 times higher than in control animals. Since the V1-sections produced no deficits when performed in adults, the temporal limits of a period of susceptibility remained to be determined. In order to assess the lower and upper limits of the period during which these perceptual deficits could be induced, unilateral or bilateral V1-sections were performed in kittens at different ages. Depth perception thresholds were measured by using the jumping stand technique. Sections of the V1 nerve only produced significant impairments of the binocular depth thresholds when performed after 3 weeks of age. They could be observed when unilateral sections were performed at up to 13 weeks of age and with bilateral sections at up to 10 weeks of age. These functional impairments appeared to remain permanently through adult life.

The spatial range of peripheral collinear facilitation

Contrast detection thresholds for a central Gabor patch (target) can be modulated by the presence of co-oriented and collinear high contrast Gabors flankers. In foveal vision collinear facilitation can be observed for target-to-flankers relative distances beyond two times the wavelength (λ) of the Gabor’s carrier, while for shorter relative distances (<2λ) there is suppression. These modulatory influences seem to disappear after 12λ. In this study, we measured contrast detection thresholds for different spatial frequencies (1, 4 and 6 cpd) and target-to-flankers relative distances ranging from 6 to 16λ, but with collinear configurations presented in near periphery at 4° of eccentricity. Results showed that in near periphery collinear facilitation extends beyond 12λ for the higher spatial frequencies tested (4 and 6 cpd), while it decays already at 10λ for the lowest spatial frequency used (i.e., 1 cpd). In addition, we found that increasing the spatial frequency the peak of collinear facilitation shifts towards larger target-to-flankers relative distances (expressed as multiples of the stimulus wavelength), an effect never reported neither for near peripheral nor for central vision. The results suggest that the peak and the spatial extent of collinear facilitation in near periphery depend on the spatial frequency of the stimuli used.

Processing of Egomotion-Consistent Optic Flow in the Rhesus Macaque Cortex

Abstract The cortical network that processes visual cues to self‐motion was characterized with functional magnetic resonance imaging in 3 awake behaving macaques. The experimental protocol was similar to previous human studies in which the responses to a single large optic flow patch were contrasted with responses to an array of 9 similar flow patches. This distinguishes cortical regions where neurons respond to flow in their receptive fields regardless of surrounding motion from those that are sensitive to whether the overall image arises from self‐motion. In all 3 animals, significant selectivity for egomotion‐consistent flow was found in several areas previously associated with optic flow processing, and notably dorsal middle superior temporal area, ventral intra‐parietal area, and VPS. It was also seen in areas 7a (Opt), STPm, FEFsem, FEFsac and in a region of the cingulate sulcus that may be homologous with human area CSv. Selectivity for egomotion‐compatible flow was never total but was particularly strong in VPS and putative macaque CSv. Direct comparison of results with the equivalent human studies reveals several commonalities but also some differences.

Visual straight-ahead preference in saccadic eye movements

Ocular saccades bringing the gaze toward the straight-ahead direction (centripetal) exhibit higher dynamics than those steering the gaze away (centrifugal). This is generally explained by oculomotor determinants: centripetal saccades are more efficient because they pull the eyes back toward their primary orbital position. However, visual determinants might also be invoked: elements located straight-ahead trigger saccades more efficiently because they receive a privileged visual processing. Here, we addressed this issue by using both pro- and anti-saccade tasks in order to dissociate the centripetal/centrifugal directions of the saccades, from the straight-ahead/eccentric locations of the visual elements triggering those saccades. Twenty participants underwent alternating blocks of pro- and anti-saccades during which eye movements were recorded binocularly at 1 kHz. The results confirm that centripetal saccades are always executed faster than centrifugal ones, irrespective of whether the visual elements have straight-ahead or eccentric locations. However, by contrast, saccades triggered by elements located straight-ahead are consistently initiated more rapidly than those evoked by eccentric elements, irrespective of their centripetal or centrifugal direction. Importantly, this double dissociation reveals that the higher dynamics of centripetal pro-saccades stem from both oculomotor and visual determinants, which act respectively on the execution and initiation of ocular saccades.