Motion parallax processing in pigeon (Columba livia) pretectal neurons

In the visual system of invertebrates and vertebrates there are specialised groups of motion‐sensitive neurons, with large receptive fields, which are optimally tuned to respond to optic flow produced by the animals' movement through the 3‐D world. From their response characteristics, shared frame of reference with the vestibular or inertial system, and anatomical connections, these neurons have been implicated in the stabilisation of retinal images, the control of posture and balance, and the animal's motion trajectories through the world. Using standard electrophysiological techniques and computer‐generated stimuli, we show that some of these flow‐field neurons in the pretectal nucleus lentiformis mesencephali in pigeons appear to be processing motion parallax. Two large overlapping planes of random dots moving independently were used to simulate motion parallax, in which one with larger dots was moved fast and the other with smaller dots was moved slowly in the opposite direction. Their neural responses to these two superimposed planes were facilitated above those produced by a single plane of moving dots and those produced by two layers moving in the same direction. Furthermore, some of these neurons preferred backward motion in the visual field and others preferred forward motion, suggesting that they may separately code visual objects ‘nearer’ and ‘farther’ than the stabilised (‘on’) plane during forward translational motion. A simple system is proposed whereby the relative activity in ‘near’, ‘far’ and ‘on’ populations could code depth through motion parallax in a metameric manner similar to that employed to code color vision and stereopsis.     

Distance estimation in the hooded rat: experimental evidence for the role of motion cues

The role of motion cues, generated by vertical head movements, in distance estimation by hooded rats was investigated in a jumping task in which animals were trained to jump randomly varying gaps between two elevated platforms. In the first experiment it was shown that the disposition of texture cues influenced the number of head movements made prior to jumping, showing that the movements are related to visual aspects of the task. In the second experiment it was shown that stroboscopic illumination disrupted accurate jumping but animals could jump accurately to a platform when only the leading edge was visible, showing that they depend on motion cues but not motion parallax.     

Binocular disparity tuning and visual-vestibular congruency of multisensory neurons in macaque parietal cortex

Many neurons in the dorsal medial superior temporal (MSTd) and ventral intraparietal (VIP) areas of the macaque brain are multisensory, responding to both optic flow and vestibular cues to self-motion. The heading tuning of visual and vestibular responses can be either congruent or opposite, but only congruent cells have been implicated in cue integration for heading perception. Because of the geometric properties of motion parallax, however, both congruent and opposite cells could be involved in coding self-motion when observers fixate a world-fixed target during translation, if congruent cells prefer near disparities and opposite cells prefer far disparities. We characterized the binocular disparity selectivity and heading tuning of MSTd and VIP cells using random-dot stimuli. Most (70%) MSTd neurons were disparity selective with monotonic tuning, and there was no consistent relationship between depth preference and congruency of visual and vestibular heading tuning. One-third of disparity-selective MSTd cells reversed their depth preference for opposite directions of motion [direction-dependent disparity tuning (DDD)], but most of these cells were unisensory with no tuning for vestibular stimuli. Inconsistent with previous reports, the direction preferences of most DDD neurons do not reverse with disparity. By comparison to MSTd, VIP contains fewer disparity-selective neurons (41%) and very few DDD cells. On average, VIP neurons also preferred higher speeds and nearer disparities than MSTd cells. Our findings are inconsistent with the hypothesis that visual/vestibular congruency is linked to depth preference, and also suggest that DDD cells are not involved in multisensory integration for heading perception.     

Stereoscopic illusory contours--cortical neuron responses and human perception

In human perception, figure-ground segregation suggests that stereoscopic cues are grouped over wide areas of the visual field. For example, two abutting rectangles of equal luminance and size are seen as a uniform surface when presented at the same depth, but appear as two surfaces separated by an illusory contour and a step in depth when presented with different retinal disparities. Here, we describe neurons in the monkey visual cortex that signal such illusory contours and can be selective for certain figure-ground directions that human observers perceive at these contours. The results suggest that these neurons group stereoscopic cues over distances up to 8 degrees. In addition, we compare these results with human perception and show that the mean stimulus parameters required by these neurons also induce optimal percepts of illusory contours in human observers.     

Motion parallax enables depth processing for action in a visual form agnosic when binocular vision is unavailable

Visual-form agnosic patient DF, who has severe difficulties in using visual information about size, shape and orientation for perceptual report, can nevertheless—under normal viewing conditions—use the same information to accurately guide her hand movements. However, her performance of prehension tasks requiring the analysis of visual depth is severely disrupted when binocular vision is prevented. We have suggested that this deterioration in visuomotor control is due to an inability to use pictorial depth cues to compensate for the removal of binocular vision. In the current study we investigated whether DF was able to use motion parallax as an alternative to binocular cues. We asked her to grasp a square plaque slanted at different orientations in depth, under two monocular testing conditions. In one condition her head remained stationary on a chin rest, and in the other condition she made large lateral head movements just prior to each prehension movement. The results confirmed that DF is impaired in adjusting her hand orientation to the orientation of the target object when reaching monocularly with her head stationary. In contrast, when she made head movements, her manual performance was restored to almost normal levels. Our results are consistent with the idea that the processing of pictorial depth cues depends on the cortical ventral stream, which is known to be disrupted by DF’s lesion. They further indicate that orientation in depth can be computed from motion parallax just as well as from binocular cues in the absence of a normally functioning ventral stream.     

Visual experience during a sensitive period plays a critical role in vestibular compensation: neuronal substrates within Deiters' nucleus in the alert cat

In a previous study [31], we showed that Deiters' neurons ipsilateral to a vestibular neurectomy temporarily exhibit increased sensitivity to visual cues about fast movement. It was proposed that this change in the deafferented vestibular neuron response observed only during the first 3 weeks post-lesion plays an important role in the vestibular compensation process. The present study was aimed at analyzing the potential influence over the first 2 weeks post-lesion of visual motion cue deprivation (cats housed in stroboscopic light) and passive visual experience (visual information not correlated to head or body movement) on the visually induced activity of Deiters' cells. The extra-cellular response of single units was recorded during sinusoidal translation of a whole field optokinetic stimulus in six alert cats. Following the deprivation of visual motion cues, vestibular unit responses were found to be tuned to low frequencies of visual stimulation, as in intact cats, and to display a phase lag re. velocity during rapid visual stimulation. Passive visual stimulation was also found to impede the increase in neuronal sensitivity to visual input, although the cats had benefited from normal vision from the 15th day post-lesion. These results are discussed in relation to the functional implication of interactive visual experience within the early stages (sensitive period) of the vestibular compensation process.     

Binocular eye movements evoked by self-induced motion parallax

Perception often triggers actions, but actions may sometimes be necessary to evoke percepts. This is most evident in the recovery of depth by self-induced motion parallax. Here we show that depth information derived from one's movement through a stationary environment evokes binocular eye movements consistent with the perception of three-dimensional shape. Human subjects stood in front of a display and viewed a simulated random-dot sphere presented monocularly or binocularly. Eye movements were recorded by a head-mounted eye tracker, while head movements were monitored by a motion capture system. The display was continuously updated to simulate the perspective projection of a stationary, transparent random dot sphere viewed from the subject's vantage point. Observers were asked to keep their gaze on a red target dot on the surface of the sphere as they moved relative to the display. The movement of the target dot simulated jumps in depth between the front and back surfaces of the sphere along the line of sight. We found the subjects' eyes converged and diverged concomitantly with changes in the perceived depth of the target. Surprisingly, even under binocular viewing conditions, when binocular disparity signals conflict with depth information from motion parallax, transient vergence responses were observed. These results provide the first demonstration that self-induced motion parallax is sufficient to drive vergence eye movements under both monocular and binocular viewing conditions.     

Occlusion and the interpretation of visual motion: perceptual and neuronal effects of context.

Visual motion can be represented in terms of the dynamic visual features in the retinal image or in terms of the moving surfaces in the environment that give rise to these features. For natural images, the two types of representation are necessarily quite different because many moving features are only spuriously related to the motion of surfaces in the visual scene. Such "extrinsic" features arise at occlusion boundaries and may be detected by virtue of the depth-ordering cues that exist at those boundaries. Although a number of studies have provided evidence of the impact of depth ordering on the perception of visual motion, few attempts have been made to identify the neuronal substrate of this interaction. To address this issue, we devised a simple contextual manipulation that decouples surface motion from the motions of visual image features. By altering the depth ordering between a moving pattern and abutting static regions, the perceived direction of motion changes dramatically while image motion remains constant. When stimulated with these displays, many neurons in the primate middle temporal visual area (area MT) represent the implied surface motion rather than the motion of retinal image features. These neurons thus use contextual depth-ordering information to achieve a representation of the visual scene consistent with perceptual experience.     

Stimulus‐specific adaptation to visual but not auditory motion direction in the barn owl's optic tectum

Whether the auditory and visual systems use a similar coding strategy to represent motion direction is an open question. We investigated this question in the barn owl's optic tectum (OT) testing stimulus‐specific adaptation (SSA) to the direction of motion. SSA, the reduction of the response to a repetitive stimulus that does not generalize to other stimuli, has been well established in OT neurons. SSA suggests a separate representation of the adapted stimulus in upstream pathways. So far, only SSA to static stimuli has been studied in the OT. Here, we examined adaptation to moving auditory and visual stimuli. SSA to motion direction was examined using repeated presentations of moving stimuli, occasionally switching motion to the opposite direction. Acoustic motion was either mimicked by varying binaural spatial cues or implemented in free field using a speaker array. While OT neurons displayed SSA to motion direction in visual space, neither stimulation paradigms elicited significant SSA to auditory motion direction. These findings show a qualitative difference in how auditory and visual motion is processed in the OT and support the existence of dedicated circuitry for representing motion direction in the early stages of visual but not the auditory system.     

The effect of eye/head deviation and visual conflict on visually evoked postural responses

Three interrelated experiments on visually evoked postural responses (VEPR) are presented to investigate the effect of lack of coplanarity between retinal and body coordinates (Experiment I) and the effect of directionally conflicting information in the visual stimulus. Experiment I showed that the direction of VEPR is modified by eye-in-orbit and head-on-trunk position signals, presumably of proprioceptive origin. Experiments II and III showed that VEPR can be critically suppressed by the presence of conflict within the visual stimulus (Experiment II: a linear, tagential component of visual motion acting in the opposite direction to the main angular component of a roll-motion display; Experiment III: a non congruent “improbable” visual motion parallax linear motion stimulus). A conceptual model of the postural system is presented, incorporating a gain control unit for the visuo-postural loop with inputs from the ocular/cervical proprioceptive system and from intra- and intersensory conflict detectors (comparators).     

Neural Mechanism for Coding Depth from Motion Parallax in Area MT: Gain Modulation or Tuning Shifts?

There are two distinct sources of retinal image motion: objects moving in the world and observer movement. When the eyes move to track a target of interest, the retinal velocity of some object in the scene will depend on both eye velocity and that object''s motion in the world. Thus, to compute the object''s velocity relative to the head, a coordinate transformation must be performed by vectorially adding eye velocity and retinal velocity. In contrast, a very different interaction between retinal and eye velocity signals has been proposed to underlie estimation of depth from motion parallax, which involves computing the ratio of retinal and eye velocities. We examined how neurons in the middle temporal (MT) area of male macaques combine eye velocity and retinal velocity, to test whether this interaction is more consistent with a partial coordinate transformation (for computing head-centered object motion) or a multiplicative gain interaction (for computing depth from motion parallax). We find that some MT neurons show clear signatures of a partial coordinate transformation for computing head-centered velocity. Even a small shift toward head-centered velocity tuning can account for the observed depth-sign selectivity of MT neurons, including a strong dependence on speed preference that was previously unexplained. A formal model comparison reveals that the data from many MT neurons are equally well explained by a multiplicative gain interaction or a partial transformation toward head-centered tuning, although some responses can only be well fit by the coordinate transform model. Our findings shed new light on the neural computations performed in area MT, and raise the possibility that depth-sign selectivity emerges from a partial coordinate transformation toward representing head-centered velocity.SIGNIFICANCE STATEMENT Eye velocity signals modulate the responses of neurons in the middle temporal (MT) area to retinal image motion. Two different types of interactions between retinal and eye velocities have previously been considered: a vector addition computation for computing head-centered velocity, and a multiplicative gain interaction for computing depth from motion parallax. Whereas previous work favored a multiplicative gain interaction in MT, we demonstrate that some MT neurons show clear evidence of a partial shift toward coding head-centered velocity. Moreover, we demonstrate that even a small shift toward head coordinates is sufficient to account for the depth-sign selectivity observed previously in area MT, thus raising the possibility that a partial coordinate transformation may also provide a mechanism for computing depth from motion parallax.     

Rotation of visual landmark cues influences the spatial response profile of hippocampal neurons in freely-moving homing pigeons

Pigeon hippocampal neurons display two spatial response profiles: location fields frequently at goals, and path fields connecting goals. We recorded from 15 location and six path cells, with color cues positioned near four goal locations. Following color cue rotation, most location cells (12/15) shifted their response fields; path cells (5/6) lost their fields. Therefore, local visual cues can independently define a reference frame for location cells, but path cells may be more broadly tuned to context or alternative reference frames.     

Figure-Ground Segregation at Contours: a Neural Mechanism in the Visual Cortex of the Alert Monkey

An important task of vision is the segregation of figure and ground in situations of spatial occlusion. Psychophysical evidence suggests that the depth order at contours is defined early in visual processing. We have analysed this process in the visual cortex of the alert monkey. The animals were trained on a visual fixation task which reinforced foveal viewing. During periods of active visual fixation, we recorded the responses of single neurons in striate and prestriate cortex (areas V1, V2, and V3/V3A). The stimuli mimicked situations of spatial occlusion, usually a uniform light (or dark) rectangle overlaying a grating texture of opposite contrast. The direction of figure and ground at the borders of these rectangles was defined by the direction of the terminating grating lines (occlusion cues). Neuronal responses were analysed with respect to figure-ground direction and contrast polarity at such contours. Striate neurons often failed to respond to such stimuli, or were selective for contrast polarity; others were non-selective. Some neurons preferred a certain combination of figure-ground direction and contrast polarity. These neurons were rare both in striate and prestriate cortex. The majority of neurons signalled figure-ground direction independent of contrast polarity. These neurons were only found in prestriate cortex. We explain these responses in terms of a model which also explains neuronal signals of illusory contours. These results suggest that occlusion cues are used at an early level of processing to segregate figure and ground at contours.     

Conjunctive effects of reward and behavioral episodes on hippocampal place-differential neurons of rats on a mobile treadmill

Previous studies reported context (or behavior)-dependent activities of hippocampal place cells, which are suggested to be the neural basis of episodic memory. However, it remains unclear what distinctive items these context-dependent activities encode. We investigated separately the effects of space, locomotion, and episodes with positive/negative reinforcements on activity of place-differential neurons in the hippocampal CA1 area. Rats were placed on a treadmill affixed to a motion stage translocated along a figure 8-shaped track. The track could be navigated by two different routes that shared a common central stem. The stage was paused at the start and end of the routes, where conditioned response tasks with different reinforcements were imposed. As the rats passed the common central stem, some neurons fired differently depending on the route. Comparison of hippocampal spatial firing patterns across different conditions with and without treadmill operation and/or the tasks indicated that these route-dependent spatial firing patterns were sensitive to locomotion, the tasks, and vestibular sensation or visual cues such as optic flow. The results suggest that external sensory inputs, path integration, and reinforcement context are all integrated in the hippocampus, which might provide the neural basis of episodic memory.     

Changes of spatial and temporal frequency tuning properties of neurons in the middle temporal area of aged rhesus monkeys

Aged humans exhibit severe deficits in visual motion perception and contrast sensitivity under various levels of spatial and temporal modulation. Previous studies indicated that many of these deficits are probably mediated by the neural degradation of the central visual system. To clarify the neuronal response mechanisms underlying the visual degradation during aging, we examined the spatial and temporal frequency tuning properties of neurons from anesthetised and paralysed aged monkeys at the middle temporal area (area MT), which is downstream of the primary visual cortex in the visual processing pathway and thought to be critical for motion perception. We found that the preferred spatial and temporal frequencies, spatial resolution and high temporal frequency cutoff of area MT neurons were reduced in aged monkeys, and were accompanied by the broadened tuning width of spatial frequency, elevated spontaneous activity, and decreased signal‐to‐noise ratio. These results showed that, for neurons in area MT, aging significantly changed both the spatial and temporal frequency response tuning properties. Such evidence provides new insight into the changes occurring at the electrophysiological level that may be related to the aging‐related visual deficits, especially in processing spatial and temporal information.     

Global motion integration in the cat''s lateral posterior-pulvinar complex

Our laboratory previously showed that thalamic neurons in an extrageniculate nucleus, the lateral posterior-pulvinar complex (LP-pulvinar) could perform higher-order neuronal operations that had until then only been attributed to higher-level cortical areas. To further assess the role of the thalamus in the analysis of complex percepts, we have investigated whether neurons in the LP-pulvinar complex can signal the direction of motion of random-dot kinematograms wherein the individual elements of the pattern do not provide coherent motion cues. Our results indicate that a subset of LP-pulvinar cells can integrate the displacement of individual elements into a global motion percept and that their large receptive fields permit the integration of motion for elements separated by large spatial intervals. We also found that almost all of the global motion-sensitive neurons were not systematically pattern-motion-selective when tested with plaid patterns. The results indicate that LP-pulvinar cells can perform the higher-level spatio-temporal integration required to detect the global displacement of objects in a complex visual scene, further supporting the notion that extrageniculate thalamic cells are involved in higher-order motion processing. Furthermore, these results provide some evidence that there may be specialized mechanisms for processing different types of complex motion within the LP-pulvinar complex.     

Rat anterodorsal thalamic head direction neurons depend upon dynamic visual signals to select anchoring landmark cues

Head direction cells, which are functionally coupled to 'place' cells of the hippocampus, a structure critically involved in spatial cognition, are likely neural substrates for the sense of direction. Here we studied the mechanism by which head direction cells are principally anchored to background visual cues [M.B. Zugaro et al. (2001) J. Neurosci., 21, RC154,1-5]. Anterodorsal thalamic head direction cells were recorded while the rat foraged on a small elevated platform in a 3-m diameter cylindrical enclosure. A large card was placed in the background, near the curtain, and a smaller card was placed in the foreground, near the platform. The cards were identically marked, proportionally dimensioned, subtended the same visual angles from the central vantage point and separated by 90 degrees. The rat was then disoriented in darkness, the cards were rotated by 90 degrees in opposite directions about the center and the rat was returned. Preferred directions followed either the background card, foreground card or midpoint between the two cards. In continuous lighting, preferred directions shifted to follow the background cue in most cases (30 of the 53 experiments, Batschelet V-test, P < 0.01). Stroboscopic illumination, which perturbs dynamic visual signals (e.g. motion parallax), blocked this selectivity. Head direction cells remained equally anchored to the background card, foreground card or configuration of the two cards (Watson test, P > 0.1). This shows that dynamic visual signals are critical in distinguishing typically more stable background cues which govern spatial neuronal responses and orientation behaviors.     

Stereoscopic depth magnitude estimation: effects of stimulus spatial frequency and eccentricity

To determine the effects of stimulus spatial frequency and retinal eccentricity on the perception of depth magnitude derived from disparity cues alone, subjects were asked to estimate the magnitude of depth of a stereoscopically viewed Gabor patch presented to the central or peripheral field with either crossed or uncrossed absolute disparity. Disparity vergence responses to the same Gabor stimuli were separately estimated subjectively by determining the offset required for dichoptic nonius alignment following presentation of the stimulus. The normalized stereoscopic magnitude estimation data generally showed that crossed disparities were perceived with greater depth than uncrossed disparities of the same magnitude, whether presented to the central or peripheral field. Asymmetries in magnitude of depth perception ranged from mild differences between depth directions to complete lack of depth perception for one direction. Disparity vergence response functions varied from (1) appropriate initiation of vergence to both directions of disparity, (2) initiation of vergence to only one direction of disparity, or (3) an attenuated initiation of vergence response to either direction of disparity. Within subjects, their asymmetries in magnitude of depth perception did not correlate with their asymmetries in vergence initiation. The similarity of the asymmetric depth magnitude estimation for a given individual at both stimulus locations tested suggests that common neural mechanisms are responsible for central and peripheral depth magnitude estimation. The lack of correlation between the perceptual and motor responses to the same stimuli suggests that the neural pathways for these responses diverge shortly after the detection of disparity in primary visual cortex.     

Psychoanatomical substrates of Bálint''s syndrome

OBJECTIVES: From a series of glimpses, we perceive a seamless and richly detailed visual world. Cerebral damage, however, can destroy this illusion. In the case of Bálint's syndrome, the visual world is perceived erratically, as a series of single objects. The goal of this review is to explore a range of psychological and anatomical explanations for this striking visual disorder and to propose new directions for interpreting the findings in Bálint's syndrome and related cerebral disorders of visual processing. METHODS: Bálint's syndrome is reviewed in the light of current concepts and methodologies of vision research. RESULTS: The syndrome affects visual perception (causing simultanagnosia/visual disorientation) and visual control of eye and hand movement (causing ocular apraxia and optic ataxia). Although it has been generally construed as a biparietal syndrome causing an inability to see more than one object at a time, other lesions and mechanisms are also possible. Key syndrome components are dissociable and comprise a range of disturbances that overlap the hemineglect syndrome. Inouye's observations in similar cases, beginning in 1900, antedated Bálint's initial report. Because Bálint's syndrome is not common and is difficult to assess with standard clinical tools, the literature is dominated by case reports and confounded by case selection bias, non-uniform application of operational definitions, inadequate study of basic vision, poor lesion localisation, and failure to distinguish between deficits in the acute and chronic phases of recovery. CONCLUSIONS: Studies of Bálint's syndrome have provided unique evidence on neural substrates for attention, perception, and visuomotor control. Future studies should address possible underlying psychoanatomical mechanisms at "bottom up" and "top down" levels, and should specifically consider visual working memory and attention (including object based attention) as well as systems for identification of object structure and depth from binocular stereopsis, kinetic depth, motion parallax, eye movement signals, and other cues.     

Relationship between selected orientation rest frame, circular vection and space motion sickness

Space motion sickness (SMS) and spatial orientation and motion perception disturbances occur in 70-80% of astronauts. People select "rest frames" to create the subjective sense of spatial orientation. In microgravity, the astronaut's rest frame may be based on visual scene polarity cues and on the internal head and body z axis (vertical body axis). The data reported here address the following question: Can an astronaut's orientation rest frame be related and described by other variables including circular vection response latencies and space motion sickness? The astronaut's microgravity spatial orientation rest frames were determined from inflight and postflight verbal reports. Circular vection responses were elicited by rotating a virtual room continuously at 35 degrees/s in pitch, roll and yaw with respect to the astronaut. Latency to the onset of vection was recorded from the time the crew member opened their eyes to the onset of vection. The astronauts who used visual cues exhibited significantly shorter vection latencies than those who used internal z axis cues. A negative binomial regression model was used to represent the observed total SMS symptom scores for each subject for each flight day. Orientation reference type had a significant effect, resulting in an estimated three-fold increase in the expected motion sickness score on flight day 1 for astronauts who used visual cues. The results demonstrate meaningful classification of astronauts' rest frames and their relationships to sensitivity to circular vection and SMS. Thus, it may be possible to use vection latencies to predict SMS severity and duration.