Visuo-haptic object-related activation in the ventral visual pathway

The ventral pathway is involved in primate visual object recognition. In humans, a central stage in this pathway is an occipito-temporal region termed the lateral occipital complex (LOC), which is preferentially activated by visual objects compared to scrambled images or textures. However, objects have characteristic attributes (such as three-dimensional shape) that can be perceived both visually and haptically. Therefore, object-related brain areas may hold a representation of objects in both modalities. Using fMRI to map object-related brain regions, we found robust and consistent somatosensory activation in the occipito-temporal cortex. This region showed clear preference for objects compared to textures in both modalities. Most somatosensory object-selective voxels overlapped a part of the visual object-related region LOC. Thus, we suggest that neuronal populations in the occipito-temporal cortex may constitute a multimodal object-related network.     

Concordance between perceptual and categorical repetition effects in the ventral visual stream

The process of object categorization is an integral part of human cognition. In the present study, we have used a repetition suppression paradigm to determine the degree to which the ventral visual cortex is sensitive to categorical relationships. By using images of animals and tools, suppression across perceptual (stimulus level) and categorical repetitions (basic level and domain level) was compared and contrasted across the domain-selective and hierarchical organization of the ventral visual stream. Both perceptual and categorical repetition effects were insensitive to domain-selective tuning, with suppression most prominent in regions responding maximally to images, irrespective of stimulus domain. Likewise, both perceptual and categorical repetition produced overlapping suppression across multiple regions of the visual hierarchy. Some divergent patterns were observed. The right superior temporal sulcus demonstrated repetition suppression only at the basic level (different examples of the same basic object), and the right anterior fusiform gyrus was sensitive to direct stimulus repetition but not basic-level categorical repetition. Because of the high concordance between the response profiles of perceptual and categorical repetition effects, we conclude they arise from a common cognitive mechanism.     

Temporal limitations in object processing across the human ventral visual pathway

Behavioral studies have shown that object recognition becomes severely impaired at fast presentation rates, indicating a limitation in temporal processing capacity. Here, we studied whether this behavioral limit in object recognition reflects limitations in the temporal processing capacity of early visual areas tuned to basic features or high-level areas tuned to complex objects. We used functional MRI (fMRI) to measure the temporal processing capacity of multiple areas along the ventral visual pathway progressing from the primary visual cortex (V1) to high-level object-selective regions, specifically the fusiform face area (FFA) and parahippocampal place area (PPA). Subjects viewed successive images of faces or houses at presentation rates varying from 2.3 to 37.5 items/s while performing an object discrimination task. Measures of the temporal frequency response profile of each visual area revealed a systematic decline in peak tuning across the visual hierarchy. Areas V1-V3 showed peak activity at rapid presentation rates of 18-25 items/s, area V4v peaked at intermediate rates (9 items/s), and the FFA and PPA peaked at the slowest temporal rates (4-5 items/s). Our results reveal a progressive loss in the temporal processing capacity of the human visual system as information is transferred from early visual areas to higher areas. These data suggest that temporal limitations in object recognition likely result from the limited processing capacity of high-level object-selective areas rather than that of earlier stages of visual processing.     

Perceptual scaling of visual and inertial cues

In the field of motion-based simulation, it was found that a visual amplitude equal to the inertial amplitude does not always provide the best perceived match between visual and inertial motion. This result is thought to be caused by the “quality” of the motion cues delivered by the simulator motion and visual systems. This paper studies how different visual characteristics, like field of view (FoV) and size and depth cues, influence the scaling between visual and inertial motion in a simulation environment. Subjects were exposed to simulator visuals with different fields of view and different visual scenes and were asked to vary the visual amplitude until it matched the perceived inertial amplitude. This was done for motion profiles in surge, sway, and yaw. Results showed that the subjective visual amplitude was significantly affected by the FoV, visual scene, and degree-of-freedom. When the FoV and visual scene were closer to what one expects in the real world, the scaling between the visual and inertial cues was closer to one. For yaw motion, the subjective visual amplitudes were approximately the same as the real inertial amplitudes, whereas for sway and especially surge, the subjective visual amplitudes were higher than the inertial amplitudes. This study demonstrated that visual characteristics affect the scaling between visual and inertial motion which leads to the hypothesis that this scaling may be a good metric to quantify the effect of different visual properties in motion-based simulation.     

Perceptual distortions in the neural representation of visual space

 The visual mechanism by which human observers determine the separation between objects has long been of interest. This study examines the extent to which separation in visual space can be misperceived in foveal and extrafoveal vision. Foveally, vertical separations were consistently overestimated relative to horizontal separations, a result which is consistent with the well-documented horizontal-vertical illusion (HVI). Extrafoveally, much larger misrepresentations of visual space were perceived. In addition, separations tangential to fixation were consistently perceived as being greater than separations in a radial direction. These marked misperceptions of visual space which occur in extrafoveal vision take the form of a radial/tangential anisotropy combined with an overestimation of vertical distance. The results have important implications for meridional anisotropies which have previously been documented in a number of visual performance tasks. Received: 17 July 1998 / Accepted: 14 October 1998     

The subjective visual vertical and the perceptual upright

The direction of 'up' has traditionally been measured by setting a line (luminous if necessary) to the apparent vertical, a direction known as the 'subjective visual vertical' (SVV); however for optimum performance in visual skills including reading and facial recognition, an object must to be seen the 'right way up'--a separate direction which we have called the 'perceptual upright' (PU). In order to measure the PU, we exploited the fact that some symbols rely upon their orientation for recognition. Observers indicated whether the symbol 'horizontal P' presented in various orientations was identified as either the letter 'p' or the letter 'd'. The average of the transitions between 'p-to-d' and 'd-to-p' interpretations was taken as the PU. We have labelled this new experimental technique the Oriented CHAracter Recognition Test (OCHART). The SVV was measured by estimating whether a line was rotated clockwise or counter-clockwise relative to gravity. We measured the PU and SVV while manipulating the orientation of the visual background in different observer postures: upright, right side down and (for the PU) supine. When the body, gravity and the visual background were aligned, the SVV and the PU were similar, but as the background orientation and observer posture orientations diverged, the two measures varied markedly. The SVV was closely aligned with the direction of gravity whereas the PU was closely aligned with the body axis. Both probes showed influences of all three cues (body orientation, vision and gravity) and these influences could be predicted from a weighted vectorial sum of the directions indicated by these cues. For the SVV, the ratio was 0.2:0.1:1.0 for the body, visual and gravity cues, respectively. For the PU, the ratio was 2.6:1.2:1.0. In the case of the PU, these same weighting values were also predicted by a measure of the reliability of each cue; however, reliability did not predict the weightings for the SVV. This is the first time that maximum likelihood estimation has been demonstrated in combining information between different reference frames. The OCHART technique provides a new, simple and readily applicable method for investigating the PU which complements the SVV. Our findings suggest that OCHART is particularly suitable for investigating the functioning of visual and non-visual systems and their contributions to the perceived upright of novel environments such as high- and low-g environments, and in patient and ageing populations, as well as for normal observers.     

Permanent perceptual and neurophysiological effects of visual deprivation in the cat

Summary The purpose of the present study was to analyze recovery of visual perception in kittens whose deprived eye had permanently lost access to most selective cortical neurons. Twelve kittens were reared monocularly for 3 months or more; then the deprived eye was opened and the experienced eye was shut (cross-suture treatment) in an attempt to push recovery. Monocular training through the deprived eye was administered on a series of discrimination problems and transposition tests. Some recovery from the monocular deprivation was evident. These kittens learned an orientation problem (horizontal vs. vertical stripes) in an abstract manner. However, on the form problem (upright vs. inverted triangle) they were still noteably deficient when compared to normal controls: 1. Acquisition of the form problem was shown to be strongly dependent on flux cues and 2. Interocular transfer was deficient. Microelectrode and visual evoked potential recording with the cross-suture group revealed no discernible recovery from the deprivation treatment at the visual cortex. Of 34 neurons recorded from 4 animals, only one could be driven by the initially deprived eye. No binocularly driven cells were found. Late components of the VEP were reduced in amplitude when elicited through the deprived eye. We conclude that when forced to use an eye which influences only a small number of neurons, all of which have abnormal receptive fields, animals can learn a wide variety of form problems, but only by using local flux cues. Form perception with a normal degree of stability in the presence of environmental changes appears to depend on cortical neurons with form-selective receptive fields.     

Asymmetry and ventral course of the human geniculostriate pathway as determined by hippocampal visual evoked potentials and subsequent visual field defects after temporal lobectomy

Summary Twenty-two patients with psychomotor epilepsy were implanted with depth electrodes along the axis of the mesial temporal lobe to identify an operable unilateral epileptic focus. Neuronal and field potentials were recorded in response to diffuse retinal illumination and clear short-latency responses were found in parahippocampal gyrus. These visual afferents in the mesial temporal lobe are assumed to be both from subcortical and cortical visual areas. There was a clear asymmetry in the ventral trajectory of the geniculostriate pathway as evidenced by asymmetric neuronal and field potential responses to brief flashes in right vs. left hippocampal gyrus and confirmed by a corresponding partial visual field deficit following therapeutic anterior temporal lobectomy. These results demonstrate that there is a retinotopic organization of fibers in the human geniculostriate pathway and that this pathway may have considerable variability in the anterior and ventral course these fibers take through the temporal lobe. These findings adequately account for the presence of direct projections from geniculate to hippocampal cortex and for unexpected hemianopsias with standard resections of the temporal lobe when there is a deviant detour of the geniculostriate pathway.Supported by grant no. NS 02808 and the Ralph Smith Foundation     

Perceptual learning and top-down influences in primary visual cortex

Neuronal responses at early stages in visual cortical processing, including those in primary visual cortex (V1), are subject to the influences of visual context, experience and attention. Here we show that for monkeys trained in a shape discrimination task, V1 neurons took on novel functional properties related to the attributes of the trained shapes. Furthermore, these properties depended on the perceptual task being performed; neurons responded very differently to an identical visual stimulus under different visual discrimination tasks. These top-down influences were seen from the very beginning and throughout the entire time course of the neural responses. Information theoretic analysis showed that neurons carried more information about a stimulus attribute when the animals were performing a task related to that attribute. Our findings suggest that the output from V1 reflects both sensory and behavioral context.     

Electrophysiological correlates of visual perceptual masking in monkeys

Summary Monkeys were trained to discriminate with nearly 100% accuracy between a square and a triangle presented simultaneously in a brief tachistoscopic flash. Perceptual masking was demonstrated by inability to perform this trained visual discrimination at better than chance level when the information flash was followed in less than 20 msec by a blank second flash. In order to determine the nature and locus of this retroactive visual perceptual masking effect, electrical potentials were recorded simultaneously from three points along the optic pathways: optic nerve or tract, lateral geniculate body, and visual cortex. Potentials were computer-averaged and correlated with the monkey's ability or inability to make a correct behavioral response to the information contained in the first or test flash (T). When the perception of T was masked by the second or blanking flash (B), only the evoked potential characteristic of B was observed at all recording sites, including the optic nerve or tract. This suggested that the interaction underlying masking occurred in the retina since optic nerve or tract responses are dependent upon retinal ganglion cells. When T was not masked, an early portion of the evoked response to T could be detected at all recording sites. Perception of T was possible when only the initial segment of the T-potential (15 msec or less) was present at each recording site. Thus the visual information transfer essential to the performance of an already learned visual discrimination task appears to occur very early in the course of the evoked response and is not dependent upon later or secondary components.Supported by grants from the Office of Naval Research (Nonr-4756) and National Aeronautics and Space Administration (NASA NGL 05-007-049). Aided by National Institute of Mental Health Training Grant 5 TI MH-6415.     

Neural substrates for visual perceptual grouping in humans

Two experiments investigated the neural mechanisms of Gestalt grouping by recording high-density event-related brain potentials (ERPs) during discrimination tasks. In Experiment 1, stimulus arrays contained luminance-defined local elements that were either evenly spaced or grouped into columns or rows based on either proximity or similarity of shape. Proximity grouping was indexed by a short-latency positivity (110-120 ms) over the medial occipital cortex and a subsequent right occipitoparietal negativity. Grouping by similarity was reflected only in a long-latency occipitotemporal negativity. In Experiment 2, proximity grouping was examined when local elements were defined by motion cues, and was again associated with a medial occipital positivity. However, the subsequent long-latency negativity was now enhanced over the left posterior areas. The implications of these results to the neural substrates subserving different grouping processes are discussed.     

ERP topography and human perceptual learning in the peripheral visual field.

We studied human perceptual learning in the peripheral visual field in 16 healthy adults. Horizontal or vertical vernier stimuli were presented simultaneously at 8 locations at an eccentricity of 4 degrees . One of the stimuli displayed an offset, and subjects were asked to detect the target offset. Training was performed with either vertical or horizontal stimuli by the repeated presentation of stimuli. Discrimination performance was also measured with the untrained stimuli. Before and after the psychophysical experiment, EEG was recorded from 30 electrodes over the occipital areas (between the inion and Cz) while targets were presented at all locations as vernier onset/offset stimuli. The EEG was averaged for each orientation separately. Improvement in discrimination performance was observed in about 70% of the subjects with the trained orientation only. The evoked potential maps displayed three components occurring between 80 and 160, 180 and 260, and 280 and 340 ms. The potential field topography of the first and third component showed significant differences before and after learning. In addition, field strength (global field power) of the second and third component increased with learning. No effects were seen with the untrained stimuli in the psychophysical and electrophysiological experiments. Our findings suggest that perceptual learning in the peripheral visual field is specifically related to neurophysiological changes induced by training, and it is not caused by unspecific changes of spatial attention. The changes of electrical brain activity reflect short-term plasticity related to human perceptual learning.     

Specificity of auditory-guided visual perceptual learning suggests crossmodal plasticity in early visual cortex

Sounds modulate visual perception. Blind humans show altered brain activity in early visual cortex. However, it is still unclear whether crossmodal activity in visual cortex results from unspecific top-down feedback, a lack of visual input, or genuinely reflects crossmodal interactions at early sensory levels. We examined how sounds affect visual perceptual learning in sighted adults. Visual motion discrimination was tested prior to and following eight sessions in which observers were exposed to irrelevant moving dots while detecting sounds. After training, visual discrimination improved more strongly for motion directions that were paired with a relevant sound during training than for other directions. Crossmodal learning was limited to visual field locations that overlapped with the sound source and was little affected by attention. The specificity and automatic nature of these learning effects suggest that sounds automatically guide visual plasticity at a relatively early level of processing.     

Microstimulation of visual cortex affects the speed of perceptual decisions

Direction-selective neurons in the middle temporal visual area (MT) are crucially involved in motion perception, although it is not known exactly how the activity of these neurons is interpreted by the rest of the brain. Here we report that in a two-alternative task, the activity of MT neurons is interpreted as evidence for one direction and against the other. We measured the speed and accuracy of decisions as rhesus monkeys performed a direction-discrimination task. On half of the trials, we stimulated direction-selective neurons in area MT, thereby causing the monkeys to choose the neurons' preferred direction more often. Microstimulation quickened decisions in favor of the preferred direction and slowed decisions in favor of the opposite direction. Even on trials in which microstimulation did not induce a preferred direction choice, it still affected response times. Our findings suggest that during the formation of a decision, sensory evidence for competing propositions is compared and accumulates to a decision-making threshold.     

The visual cortico-striato-nigral pathway in the rat

The organization of the visual cortico-striato-nigral pathway in the rat has been investigated in two sets of experiments using anterograde autoradiographic tracing techniques. First, in one group of animals, injections of tritiated amino acids were placed throughout the visual cortex to demonstrate the visual corticostriatal pathway. The results indicate that visual corticostriatal fibres terminate in a distinctive clustered pattern throughout the entire length of the ipsilateral dorsomedial striatum. The projection shows a longitudinal topographic organization with cortical loci projecting onto narrow longitudinal regions of the dorsomedial striatum. In addition to the ipsilateral projection, a substantially smaller contralateral visual corticostriatal projection was also demonstrated. In the second set of experiments, the visual corticorecipient region of the striatum demonstrated in the first set of experiments was injected with tritiated amino acids to demonstrate the "visual" striatonigral projection. The results indicate that striatonigral fibres from the dorsomedial striatum project throughout the rostrocaudal extent of the ventral region of the pars reticulata. As with the visual corticostriatal pathway, the projection shows a longitudinal topographic organization with striatal loci projecting onto longitudinal regions of the ventral pars reticulata; the most rostral regions of the dorsal striatum project to the most medial regions of the ventral pars reticulata and, likewise, successively more caudal regions of the dorsal striatum project to successively more lateral regions of the ventral pars reticulata. In addition to the main projection to the ventral pars reticulata, a second smaller component of the striatonigral pathway was traced to adjacent regions of the dorsal pars reticulata and ventral pars compacta. These findings provide evidence of a visual cortico-striato-nigral pathway to both the pars reticulata and pars compacta in the rat. It is suggested that the major projection onto the ventral pars reticulata may provide an input onto nigrotectal neurons and thereby complete an indirect visual corticotectal connection mediated via links in the basal ganglia.     

A tectocortical visual pathway in the rat

Injections of tritiated leucine into the superior colliculus of the rat were used to study the efferents of the colliculus. The superficial layers of the colliculus project to the lateral posterior nucleus, the lateral geniculate nucleus and the pretectum. Two distinct subdivisions of the lateral posterior nucleus were found, a caudomedial region which receives a bilateral projection from the superior colliculus and an anterolateral region which receives a unilateral projection from the superior colliculus. Injections of horseradish peroxidase into the lateral prestriate visual cortex showed that the lateral posterior nucleus sends a dense projection to this area. There was no evidence that the caudomedial and anterolateral parts of the lateral posterior nucleus project to different regions of the lateral prestriate cortex.The tectothalamocortical pathway in the rat provides a major route outside the geniculostriate projection by which visual information from the retina can reach the cortex.     

Comparison of shape encoding in primate dorsal and ventral visual pathways

Ventral and dorsal visual pathways perform fundamentally different functions. The former is involved in object recognition, whereas the latter carries out spatial localization of stimuli and visual guidance of motor actions. Despite the association of the dorsal pathway with spatial vision, recent studies have reported shape selectivity in the dorsal stream. We compared shape encoding in anterior inferotemporal cortex (AIT), a high-level ventral area, with that in lateral intraparietal cortex (LIP), a high-level dorsal area, during a fixation task. We found shape selectivities of individual neurons to be greater in anterior inferotemporal cortex than in lateral intraparietal cortex. At the neural population level, responses to different shapes were more dissimilar in AIT than LIP. Both observations suggest a greater capacity in AIT for making finer shape distinctions. Multivariate analyses of AIT data grouped together similar shapes based on neural population responses, whereas such grouping was indistinct in LIP. Thus in a first comparison of shape response properties in late stages of the two visual pathways, we report that AIT exhibits greater capability than LIP for both object discrimination and generalization. These differences in the two visual pathways provide the first neurophysiological evidence that shape encoding in the dorsal pathway is distinct from and not a mere duplication of that formed in the ventral pathway. In addition to shape selectivity, we observed stimulus-driven cognitive effects in both areas. Stimulus repetition suppression in LIP was similar to the well-known repetition suppression in AIT and may be associated with the "inhibition of return" memory effect observed during reflexive attention.     

Role of the extra-geniculate pathway in visual guidance

Summary We investigated the effect of superior colliculus lesions on the performance of a visually guided paw movement. Six cats were trained to perform a paw movement toward a lever moving in front of them at an adjustable speed. The target was visible and accessible for approximately 700 ms, corresponding to the time needed to traverse the aperture situated in front of the animal. To receive a food pellet reward the cat had to press on the lever during this presentation period. Efficient and misguided movements were recorded, and their relative proportions calculated. For each rewarded movement, the response time (delay between the appearance of the lever in the aperture and the cat's press) was automatically computed. After stabilization of their performance, each cat underwent a bilateral electrolytic lesion of the superior colliculi. In all cases it markedly affected precision. The cats first recovered their ability to reach an immobile lever and later on their ability to point to the lever while it was moving. However, even after two months of postoperative training, two cats had still not completely recovered their preoperative precision. All lesioned animals displayed a perturbation in their response time distribution. Anterior lesions, involving area centralis projection, were more effective in producing the deficits than more posterior ones. The results are discussed in relation to the involvement of the superior colliculus in the analysis of peripheral fixed or moving stimuli.     

Synchronization between the end stages of the dorsal and the ventral visual stream

The end stage areas of the ventral (IT) and the dorsal (AIP) visual streams encode the shape of disparity-defined three-dimensional (3D) surfaces. Recent anatomical tracer studies have found direct reciprocal connections between the 3D-shape selective areas in IT and AIP. Whether these anatomical connections are used to facilitate 3D-shape perception is still unknown. We simultaneously recorded multi-unit activity (MUA) and local field potentials in IT and AIP while monkeys discriminated between concave and convex 3D shapes and measured the degree to which the activity in IT and AIP synchronized during the task. We observed strong beta-band synchronization between IT and AIP preceding stimulus onset that decreased shortly after stimulus onset and became modulated by stereo-signal strength and stimulus contrast during the later portion of the stimulus period. The beta-coherence modulation was unrelated to task-difficulty, regionally specific, and dependent on the MUA selectivity of the pairs of sites under study. The beta-spike-field coherence in AIP predicted the upcoming choice of the monkey. Several convergent lines of evidence suggested AIP as the primary source of the AIP-IT synchronized activity. The synchronized beta activity seemed to occur during perceptual anticipation and when the system has stabilized to a particular perceptual state but not during active visual processing. Our findings demonstrate for the first time that synchronized activity exists between the end stages of the dorsal and ventral stream during 3D-shape discrimination.