Retinal stabilization reveals limited influence of extraretinal signals on heading tuning in the medial superior temporal area

Heading Direction ◽

Visual Areas ◽

AbstractHeading perception in primates depends heavily on visual optic-flow cues. Yet during self-motion, heading percepts remain stable even though smooth-pursuit eye movements often distort optic flow. Electrophysiological studies have identified visual areas in monkey cortex, including the dorsal medial superior temporal area (MSTd), that signal the true heading direction during pursuit. According to theoretical work, self-motion can be represented accurately by compensating for these distortions in two ways: via retinal mechanisms or via extraretinal efference-copy signals, which predict the sensory consequences of movement. Psychophysical evidence strongly supports the efference-copy hypothesis, but physiological evidence remains inconclusive. Neurons that signal the true heading direction during pursuit are found in visual areas of monkey cortex, including the dorsal medial superior temporal area (MSTd). Here we measured heading tuning in MSTd using a novel stimulus paradigm, in which we stabilize the optic-flow stimulus on the retina during pursuit. This approach isolates the effects on neuronal heading preferences of extraretinal signals, which remain active while the retinal stimulus is prevented from changing. Our results demonstrate a significant but small influence of extraretinal signals on the preferred heading directions of MSTd neurons. Under our stimulus conditions, which are rich in retinal cues, we find that retinal mechanisms dominate physiological corrections for pursuit eye movements, suggesting that extraretinal cues, such as predictive efference-copy mechanisms, have a limited role under naturalistic conditions.Significance StatementSensory systems discount stimulation caused by the animal’s own behavior. For example, eye movements cause irrelevant retinal signals that could interfere with motion perception. The visual system compensates for such self-generated motion, but how this happens is unclear. Two theoretical possibilities are a purely visual calculation or one using an internal signal of eye movements to compensate for their effects. Such a signal can be isolated by experimentally stabilizing the image on a moving retina, but this approach has never been adopted to study motion physiology. Using this method, we find that eye-movement signals have little influence on neural activity in visual cortex, while feed-forward visual calculation has a strong effect and is likely important under real-world conditions.

The Responses of VIP Neurons Are Sufficiently Sensitive to Support Heading Judgments

10.1152/jn.00401.2009 ◽

2010 ◽

Vol 103 (4) ◽

pp. 1865-1873 ◽

Cited By ~ 17

Author(s):

Tao Zhang ◽

Kenneth H. Britten

Keyword(s):

Optic Flow ◽

Discrimination Task ◽

Roc Analysis ◽

Operating Characteristic ◽

Macaque Monkey ◽

Pursuit Eye Movements ◽

Behavioral Thresholds ◽

Heading Direction ◽

Ventral Intraparietal Area ◽

The ventral intraparietal area (VIP) of the macaque monkey is thought to be involved in judging heading direction based on optic flow. We recorded neuronal discharges in VIP while monkeys were performing a two-alternative, forced-choice heading discrimination task to relate quantitatively the activity of VIP neurons to monkeys' perceptual choices. Most VIP neurons were responsive to simulated heading stimuli and were tuned such that their responses changed across a range of forward trajectories. Using receiver operating characteristic (ROC) analysis, we found that most VIP neurons were less sensitive to small heading changes than was the monkey, although a minority of neurons were equally sensitive. Pursuit eye movements modestly yet significantly increased both neuronal and behavioral thresholds by approximately the same amount. Our results support the view that VIP activity is involved in self-motion judgments.

Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST

10.1152/jn.1988.60.3.940 ◽

1988 ◽

Vol 60 (3) ◽

pp. 940-965 ◽

Cited By ~ 213

Author(s):

M. R. Dursteler ◽

R. H. Wurtz

Keyword(s):

Eye Movements ◽

Visual Field ◽

Visual Motion ◽

Ibotenic Acid ◽

Motion Processing ◽

Temporal Area ◽

Target Speed ◽

Pursuit Eye Movements ◽

Visual Motion Processing

1. Previous experiments have shown that punctate chemical lesions within the middle temporal area (MT) of the superior temporal sulcus (STS) produce deficits in the initiation and maintenance of pursuit eye movements (10, 34). The present experiments were designed to test the effect of such chemical lesions in an area within the STS to which MT projects, the medial superior temporal area (MST). 2. We injected ibotenic acid into localized regions of MST, and we observed two deficits in pursuit eye movements, a retinotopic deficit and a directional deficit. 3. The retinotopic deficit in pursuit initiation was characterized by the monkey's inability to match eye speed to target speed or to adjust the amplitude of the saccade made to acquire the target to compensate for target motion. This deficit was related to the initiation of pursuit to targets moving in any direction in the visual field contralateral to the side of the brain with the lesion. This deficit was similar to the deficit we found following damage to extrafoveal MT except that the affected area of the visual field frequently extended throughout the entire contralateral visual field tested. 4. The directional deficit in pursuit maintenance was characterized by a failure to match eye speed to target speed once the fovea had been brought near the moving target. This deficit occurred only when the target was moving toward the side of the lesion, regardless of whether the target began to move in the ipsilateral or contralateral visual field. There was no deficit in the amplitude of saccades made to acquire the target, or in the amplitude of the catch-up saccades made to compensate for the slowed pursuit. The directional deficit is similar to the one we described previously following chemical lesions of the foveal representation in the STS. 5. Retinotopic deficits resulted from any of our injections in MST. Directional deficits resulted from lesions limited to subregions within MST, particularly lesions that invaded the floor of the STS and the posterior bank of the STS just lateral to MT. Extensive damage to the densely myelinated area of the anterior bank or to the posterior parietal area on the dorsal lip of the anterior bank produced minimal directional deficits. 6. We conclude that damage to visual motion processing in MST underlies the retinotopic pursuit deficit just as it does in MT. MST appears to be a sequential step in visual motion processing that occurs before all of the visual motion information is transmitted to the brainstem areas related to pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)

MST Neuronal Responses to Heading Direction During Pursuit Eye Movements

10.1152/jn.1999.81.2.596 ◽

1999 ◽

Vol 81 (2) ◽

pp. 596-610 ◽

Cited By ~ 66

Author(s):

William K. Page ◽

Charles J. Duffy

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Visual Motion ◽

Neuronal Population ◽

Smooth Pursuit Eye Movements ◽

Neuronal Responses ◽

Temporal Area ◽

Pursuit Eye Movements ◽

Heading Direction ◽

Monkey Visual Cortex

MST neuronal responses to heading direction during pursuit eye movements. As you move through the environment, you see a radial pattern of visual motion with a focus of expansion (FOE) that indicates your heading direction. When self-movement is combined with smooth pursuit eye movements, the turning of the eye distorts the retinal image of the FOE but somehow you still can perceive heading. We studied neurons in the medial superior temporal area (MST) of monkey visual cortex, recording responses to FOE stimuli presented during fixation and smooth pursuit eye movements. Almost all neurons showed significant changes in their FOE selective responses during pursuit eye movements. However, the vector average of all the neuronal responses indicated the direction of the FOE during both fixation and pursuit. Furthermore, the amplitude of the net vector increased with increasing FOE eccentricity. We conclude that neuronal population encoding in MST might contribute to pursuit-tolerant heading perception.

Visual selectivity for heading in the macaque ventral intraparietal area

10.1152/jn.00410.2014 ◽

2014 ◽

Vol 112 (10) ◽

pp. 2470-2480 ◽

Cited By ~ 14

Author(s):

Andre Kaminiarz ◽

Anja Schlack ◽

Klaus-Peter Hoffmann ◽

Markus Lappe ◽

Frank Bremmer

Keyword(s):

Eye Movements ◽

Visual Information ◽

Flow Fields ◽

Image Motion ◽

Temporal Area ◽

Cell Responses ◽

Retinal Image Motion ◽

Ventral Intraparietal Area ◽

The patterns of optic flow seen during self-motion can be used to determine the direction of one's own heading. Tracking eye movements which typically occur during everyday life alter this task since they add further retinal image motion and (predictably) distort the retinal flow pattern. Humans employ both visual and nonvisual (extraretinal) information to solve a heading task in such case. Likewise, it has been shown that neurons in the monkey medial superior temporal area (area MST) use both signals during the processing of self-motion information. In this article we report that neurons in the macaque ventral intraparietal area (area VIP) use visual information derived from the distorted flow patterns to encode heading during (simulated) eye movements. We recorded responses of VIP neurons to simple radial flow fields and to distorted flow fields that simulated self-motion plus eye movements. In 59% of the cases, cell responses compensated for the distortion and kept the same heading selectivity irrespective of different simulated eye movements. In addition, response modulations during real compared with simulated eye movements were smaller, being consistent with reafferent signaling involved in the processing of the visual consequences of eye movements in area VIP. We conclude that the motion selectivities found in area VIP, like those in area MST, provide a way to successfully analyze and use flow fields during self-motion and simultaneous tracking movements.

The temporal dynamics of heading perception in the presence of moving objects

10.1152/jn.00866.2015 ◽

2016 ◽

Vol 115 (1) ◽

pp. 286-300 ◽

Cited By ~ 7

Author(s):

Oliver W. Layton ◽

Brett R. Fajen

Keyword(s):

Optic Flow ◽

Time Course ◽

Moving Objects ◽

Temporal Dynamics ◽

Temporal Evolution ◽

Moving Object ◽

Temporal Area ◽

Self Motion ◽

Future Path

Many forms of locomotion rely on the ability to accurately perceive one's direction of locomotion (i.e., heading) based on optic flow. Although accurate in rigid environments, heading judgments may be biased when independently moving objects are present. The aim of this study was to systematically investigate the conditions in which moving objects influence heading perception, with a focus on the temporal dynamics and the mechanisms underlying this bias. Subjects viewed stimuli simulating linear self-motion in the presence of a moving object and judged their direction of heading. Experiments 1 and 2 revealed that heading perception is biased when the object crosses or almost crosses the observer's future path toward the end of the trial, but not when the object crosses earlier in the trial. Nonetheless, heading perception is not based entirely on the instantaneous optic flow toward the end of the trial. This was demonstrated in Experiment 3 by varying the portion of the earlier part of the trial leading up to the last frame that was presented to subjects. When the stimulus duration was long enough to include the part of the trial before the moving object crossed the observer's path, heading judgments were less biased. The findings suggest that heading perception is affected by the temporal evolution of optic flow. The time course of dorsal medial superior temporal area (MSTd) neuron responses may play a crucial role in perceiving heading in the presence of moving objects, a property not captured by many existing models.

Spiral motion selective neurons in area MSTd contribute to judgments of heading

10.1152/jn.00999.2012 ◽

2014 ◽

Vol 111 (11) ◽

pp. 2332-2342 ◽

Cited By ~ 4

Author(s):

Hong Xu ◽

Pascal Wallisch ◽

David C. Bradley

Keyword(s):

Optic Flow ◽

Discrimination Task ◽

Flow Patterns ◽

Choice Probability ◽

Dorsal Part ◽

Significant Trial ◽

Temporal Area ◽

Spiral Motion ◽

Self-motion generates patterns of optic flow on the retina. Neurons in the dorsal part of the medial superior temporal area (MSTd) are selective for these optic flow patterns. It has been shown that neurons in this area that are selective for expanding optic flow fields are involved in heading judgments. We wondered how subpopulations of MSTd neurons, those tuned for expansion, rotation or spiral motion, contribute to heading perception. To investigate this question, we recorded from neurons in area MSTd with diverse tuning properties, while the animals performed a heading-discrimination task. We found a significant trial-to-trial correlation (choice probability) between the MSTd neurons and the animals' decision. Neurons in different subpopulations did not differ significantly in terms of their choice probability. Instead, choice probability was strongly related to the sensitivity of the neuron in our sample, regardless of tuning preference. We conclude that a variety of subpopulations of MSTd neurons with different tuning properties contribute to heading judgments.

Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons

10.1152/jn.1988.60.2.580 ◽

1988 ◽

Vol 60 (2) ◽

pp. 580-603 ◽

Cited By ~ 344

Author(s):

H. Komatsu ◽

R. H. Wurtz

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Visual Motion ◽

Receptive Fields ◽

Motion Processing ◽

Temporal Area ◽

Pursuit Eye Movements ◽

Visual Motion Processing ◽

Visual Areas ◽

Visual Properties

1. Among the multiple extrastriate visual areas in monkey cerebral cortex, several areas within the superior temporal sulcus (STS) are selectively related to visual motion processing. In this series of experiments we have attempted to relate this visual motion processing at a neuronal level to a behavior that is dependent on such processing, the generation of smooth-pursuit eye movements. 2. We studied two visual areas within the STS, the middle temporal area (MT) and the medial superior temporal area (MST). For the purposes of this study, MT and MST were defined functionally as those areas within the STS having a high proportion of directionally selective neurons. MST was distinguished from MT by using the established relationship of receptive-field size to eccentricity, with MST having larger receptive fields than MT. 3. A subset of these visually responsive cells within the STS were identified as pursuit cells--those cells that discharge during smooth pursuit of a small target in an otherwise dark room. Pursuit cells were found only in localized regions--in the foveal region of MT (MTf), in a dorsal-medial area of MST on the anterior bank of the STS (MSTd), and in a lateral-anterior area of MST on the floor and the posterior bank of the STS (MST1). 4. Pursuit cells showed two characteristics in common when their visual properties were studied while the monkey was fixating. Almost all cells showed direction selectivity for moving stimuli and included the fovea within their receptive fields. 5. The visual response of pursuit cells in the several areas differed in two ways. Cells in MTf preferred small moving spots of light, whereas cells in MSTd preferred large moving stimuli, such as a pattern of random dots. Cells in MTf had small receptive fields; those in MSTd usually had large receptive fields. Visual responses of pursuit neurons in MST1 were heterogeneous; some resembled those in MTf, whereas others were similar to those in MSTd. This suggests that the pursuit cells in MSTd and MST1 belong to different subregions of MST.

Clustering of Self-Motion Selectivity and Visual Response Properties in Macaque Area MSTd

10.1152/jn.90705.2008 ◽

2008 ◽

Vol 100 (5) ◽

pp. 2669-2683 ◽

Cited By ~ 20

Author(s):

Aihua Chen ◽

Yong Gu ◽

Katsumasa Takahashi ◽

Dora E. Angelaki ◽

Gregory C. DeAngelis

Keyword(s):

Receptive Field ◽

Optic Flow ◽

Correlation Technique ◽

Visual Response ◽

Temporal Area ◽

The Subject ◽

Multisensory Representation ◽

Self Motion ◽

Direction Preference

Neurons in the dorsal subdivision of the medial superior temporal area (MSTd) show directionally selective responses to both visual (optic flow) and vestibular stimuli that correspond to translational or rotational movements of the subject. Previous work has shown that MSTd neurons are clustered within the cortex according to their directional preferences for optic flow, suggesting that there may be a topographic mapping of self-motion vectors in MSTd. If MSTd provides a multisensory representation of self-motion information, then MSTd neurons may also be expected to show clustering according to their directional preferences for vestibular signals, but this has not been tested previously. We have examined clustering of vestibular signals by comparing the tuning of isolated single units (SUs) with the undifferentiated multiunit (MU) activity of several neighboring neurons recorded from the same microelectrode. We find that directional preferences for both translational and rotational vestibular stimuli, like those for optic flow, are clustered within area MSTd. MU activity often shows significant tuning for vestibular stimuli, although this MU selectivity is generally weaker for translation than for rotation. When directional tuning is observed in MU activity, the direction preference generally agrees closely with that of a simultaneously recorded SU. We also examined clustering of visual receptive field properties in MSTd by analyzing receptive field maps obtained using a reverse-correlation technique. We find that both the local directional preferences and overall spatial receptive field profiles are well clustered in MSTd. Overall, our findings have implications for how visual and vestibular signals regarding self-motion may be decoded from populations of MSTd neurons.

Pursuit Speed Compensation in Cortical Area MSTd

10.1152/jn.00002.2001 ◽

2002 ◽

Vol 88 (5) ◽

pp. 2630-2647 ◽

Cited By ~ 33

Author(s):

Krishna V. Shenoy ◽

James A. Crowell ◽

Richard A. Andersen

Keyword(s):

Eye Movements ◽

Retinal Image ◽

Visual Motion ◽

Object Motion ◽

Retinal Position ◽

Temporal Area ◽

Pursuit Eye Movements ◽

The Difference ◽

Pursuit Velocity

When we move forward the visual images on our retinas expand. Humans rely on the focus, or center, of this expansion to estimate their direction of self-motion or heading and, as long as the eyes are still, the retinal focus corresponds to the heading. However, smooth pursuit eye movements add visual motion to the expanding retinal image and displace the focus of expansion. In spite of this, humans accurately judge their heading during pursuit eye movements even though the retinal focus no longer corresponds to the heading. Recent studies in macaque suggest that correction for pursuit may occur in the dorsal aspect of the medial superior temporal area (MSTd); neurons in this area are tuned to the retinal position of the focus and they modify their tuning to partially compensate for the focus shift caused by pursuit. However, the question remains whether these neurons shift focus tuning more at faster pursuit speeds, to compensate for the larger focus shifts created by faster pursuit. To investigate this question, we recorded from 40 MSTd neurons while monkeys made pursuit eye movements at a range of speeds across simulated self- or object motion displays. We found that most MSTd neurons modify their focus tuning more at faster pursuit speeds, consistent with the idea that they encode heading and other motion parameters regardless of pursuit speed. Across the population, the median rate of compensation increase with pursuit speed was 51% as great as required for perfect compensation. We recorded from the same neurons in a simulated pursuit condition, in which gaze was fixed but the entire display counter-rotated to produce the same retinal image as during real pursuit. This condition yielded the result that retinal cues contribute to pursuit compensation; the rate of compensation increase was 30% of that required for accurate encoding of heading. The difference between these two conditions was significant ( P < 0.05), indicating that extraretinal cues also contribute significantly. We found a systematic antialignment between preferred pursuit and preferred visual motion directions. Neurons may use this antialignment to combine retinal and extraretinal compensatory cues. These results indicate that many MSTd neurons compensate for pursuit velocity, pursuit direction as previously reported and pursuit speed, and further implicate MSTd as a critical stage in the computation of egomotion.