scholarly journals Hierarchy of direction-tuned motion adaptation in human visual cortex

2012 ◽  
Vol 107 (8) ◽  
pp. 2163-2184 ◽  
Author(s):  
Hyun Ah Lee ◽  
Sang-Hun Lee

Prolonged exposure to a single direction of motion alters perception of subsequent static or dynamic stimuli and induces substantial changes in behaviors of motion-sensitive neurons, but the origin of neural adaptation and neural correlates of perceptual consequences of motion adaptation in human brain remain unclear. Using functional magnetic resonance imaging, we measured motion adaptation tuning curves in a fine scale by probing changes in cortical activity after adaptation for a range of directions relative to the adapted direction. We found a clear dichotomy in tuning curve shape: cortical responses in early-tier visual areas reduced at around both the adapted and opposite direction, resulting in a bidirectional tuning curve, whereas response reduction in high-tier areas occurred only at around the adapted direction, resulting in a unidirectional tuning curve. We also found that the psychophysically measured adaptation tuning curves were unidirectional and best matched the cortical adaptation tuning curves in the middle temporal area (MT) and the medial superior temporal area (MST). Our findings are compatible with, but not limited to, an interpretation in which direct impacts of motion adaptation occur in both unidirectional and bidirectional units in early visual areas, but the perceptual consequences of motion adaptation are manifested in the population activity in MT and MST, which may inherit those direct impacts of adaptation from the directionally selective units.

1999 ◽  
Vol 82 (5) ◽  
pp. 2462-2475 ◽  
Author(s):  
Satoshi Eifuku ◽  
Robert H. Wurtz

Many neurons in the lateral-ventral region of the medial superior temporal area (MSTl) have a clear center surround separation in their receptive fields. Either moving or stationary stimuli in the surround modulates the response to moving stimuli in the center, and this modulation could facilitate the perceptual segmentation of a moving object from its background. Another mechanism that could facilitate such segmentation would be sensitivity to binocular disparity in the center and surround regions of the receptive fields of these neurons. We therefore investigated the sensitivity of these MSTl neurons to disparity ranging from three degrees crossed disparity (near) to three degrees uncrossed disparity (far) applied to both the center and the surround regions. Many neurons showed clear disparity sensitivity to stimulus motion in the center of the receptive field. About [Formula: see text] of 104 neurons had a clear peak in their response, whereas another [Formula: see text] had broader tuning. Monocular stimulation abolished the tuning. The prevalence of cells broadly tuned to near and far disparity and the reversal of preferred directions at different disparities observed in MSTd were not found in MSTl. A stationary surround at zero disparity simply modulated up or down the response to moving stimuli at different disparities in the receptive field (RF) center but did not alter the disparity tuning curve. When the RF center motion was held at zero disparity and the disparity of the stationary surround was varied, some surround disparities produced greater modulation of MSTl neuron response than did others. Some neurons with different disparity preferences in center and surround responded best to the relative disparity differences between center and surround, whereas others were related to the absolute difference between center and surround. The combination of modulatory surrounds and the sensitivity to relative difference between center and surround disparity make these MSTl neurons particularly well suited for the segmentation of a moving object from the background.


Cephalalgia ◽  
2010 ◽  
Vol 31 (3) ◽  
pp. 338-345 ◽  
Author(s):  
Andrea Antal ◽  
Rafael Polania ◽  
Katharina Saller ◽  
Carmen Morawetz ◽  
Carsten Schmidt-Samoa ◽  
...  

Objective: Differences between people with and without migraine on various measures of visual perception have been attributed to abnormal cortical processing due to the disease. The aim of the present study was to explore the dynamics of the basic interictal state with regard to the extrastriate, motion-responsive middle temporal area (MT-complex) with functional magnetic resonance imaging (fMRI) at 3 tesla using coherent/incoherent moving dot stimuli. Method: Twenty-four migraine patients (12 with aura [MwA], 12 without aura [MwoA]) and 12 healthy subjects participated in the study. The individual cortical folding pattern was accounted for by using a cortical matching approach. Results: In the inferior-posterior portion of the MT-complex, most likely representing MT, control subjects showed stronger bilateral activation compared to MwA and MwoA patients. Compared with healthy controls MwoA and MwA patients showed significantly stronger activation mainly at the left side in response to visual stimulation in the superior-anterior portion of the MT-complex, representing the medial-superior temporal area (MST). Conclusion: Our findings strengthen the hypothesis that hyperresponsiveness of the visual cortex in migraine goes beyond early visual areas, even in the interictal period.


2001 ◽  
Vol 85 (5) ◽  
pp. 2245-2266 ◽  
Author(s):  
A. Takemura ◽  
Y. Inoue ◽  
K. Kawano ◽  
C. Quaia ◽  
F. A. Miles

Single-unit discharges were recorded in the medial superior temporal area (MST) of five behaving monkeys. Brief (230-ms) horizontal disparity steps were applied to large correlated or anticorrelated random-dot patterns (in which the dots had the same or opposite contrast, respectively, at the two eyes), eliciting vergence eye movements at short latencies [65.8 ± 4.5 (SD) ms]. Disparity tuning curves, describing the dependence of the initial vergence responses (measured over the period 50–110 ms after the step) on the magnitude of the steps, resembled the derivative of a Gaussian, the curves obtained with correlated and anticorrelated patterns having opposite sign. Cells with disparity-related activity were isolated using correlated stimuli, and disparity tuning curves describing the dependence of these initial neuronal responses (measured over the period of 40–100 ms) on the magnitude of the disparity step were constructed ( n = 102 cells). Using objective criteria and the fuzzy c-means clustering algorithm, disparity tuning curves were sorted into four groups based on their shapes. A post hoc comparison indicated that these four groups had features in common with four of the classes of disparity-selective neurons in striate cortex, but three of the four groups appeared to be part of a continuum. Most of the data were obtained from two monkeys, and when the disparity tuning curves of all the individual neurons recorded from either monkey were summed together, they fitted the disparity tuning curve for that same animal's vergence responses remarkably well ( r 2: 0.93, 0.98). Fifty-six of the neurons recorded from these two monkeys were also tested with anticorrelated patterns, and all showed significant modulation of their activity ( P < 0.005, 1-way ANOVA). Further, when all of the disparity tuning curves obtained with these patterns from either monkey were summed together, they too fitted the disparity tuning curve for that same animal's vergence responses very well ( r 2: 0.95, 0.96). Indeed, the summed activity even reproduced idiosyncratic differences in the vergence responses of the two monkeys. Based on these and other observations on the temporal coding of events, we hypothesize that the magnitude, direction, and time course of the initial vergence velocity responses associated with disparity steps applied to large patterns are all encoded in the summed activity of the disparity-sensitive cells in MST. Latency data suggest that this activity in MST occurs early enough to play an active role in the generation of vergence eye movements at short latencies.


2011 ◽  
Vol 105 (1) ◽  
pp. 60-68 ◽  
Author(s):  
Brian Lee ◽  
Bijan Pesaran ◽  
Richard A. Andersen

Visual signals generated by self-motion are initially represented in retinal coordinates in the early parts of the visual system. Because this information can be used by an observer to navigate through the environment, it must be transformed into body or world coordinates at later stations of the visual-motor pathway. Neurons in the dorsal aspect of the medial superior temporal area (MSTd) are tuned to the focus of expansion (FOE) of the visual image. We performed experiments to determine whether focus tuning curves in area MSTd are represented in eye coordinates or in screen coordinates (which could be head, body, or world-centered in the head-fixed paradigm used). Because MSTd neurons adjust their FOE tuning curves during pursuit eye movements to compensate for changes in pursuit and translation speed that distort the visual image, the coordinate frame was determined while the eyes were stationary (fixed gaze or simulated pursuit conditions) and while the eyes were moving (real pursuit condition). We recorded extracellular responses from 80 MSTd neurons in two rhesus monkeys ( Macaca mulatta). We found that the FOE tuning curves of the overwhelming majority of neurons were aligned in an eye-centered coordinate frame in each of the experimental conditions [fixed gaze: 77/80 (96%); real pursuit: 77/80 (96%); simulated pursuit 74/80 (93%); t-test, P < 0.05]. These results indicate that MSTd neurons represent heading in an eye-centered coordinate frame both when the eyes are stationary and when they are moving. We also found that area MSTd demonstrates significant eye position gain modulation of response fields much like its posterior parietal neighbors.


2019 ◽  
Author(s):  
Tyler S Manning ◽  
Kenneth H Britten

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.


2011 ◽  
Vol 106 (2) ◽  
pp. 764-774 ◽  
Author(s):  
Ian H. Stevenson ◽  
Anil Cherian ◽  
Brian M. London ◽  
Nicholas A. Sachs ◽  
Eric Lindberg ◽  
...  

In systems neuroscience, neural activity that represents movements or sensory stimuli is often characterized by spatial tuning curves that may change in response to training, attention, altered mechanics, or the passage of time. A vital step in determining whether tuning curves change is accounting for estimation uncertainty due to measurement noise. In this study, we address the issue of tuning curve stability using methods that take uncertainty directly into account. We analyze data recorded from neurons in primary motor cortex using chronically implanted, multielectrode arrays in four monkeys performing center-out reaching. With the use of simulations, we demonstrate that under typical experimental conditions, the effect of neuronal noise on estimated preferred direction can be quite large and is affected by both the amount of data and the modulation depth of the neurons. In experimental data, we find that after taking uncertainty into account using bootstrapping techniques, the majority of neurons appears to be very stable on a timescale of minutes to hours. Lastly, we introduce adaptive filtering methods to explicitly model dynamic tuning curves. In contrast to several previous findings suggesting that tuning curves may be in constant flux, we conclude that the neural representation of limb movement is, on average, quite stable and that impressions to the contrary may be largely the result of measurement noise.


2002 ◽  
Vol 88 (6) ◽  
pp. 3469-3476 ◽  
Author(s):  
Richard J. A. Van Wezel ◽  
Kenneth H. Britten

In many sensory systems, exposure to a prolonged stimulus causes adaptation, which tends to reduce neural responses to subsequent stimuli. Such effects are usually stimulus-specific, making adaptation a powerful probe into information processing. We used dynamic random dot kinematograms to test the magnitude and selectivity of adaptation effects in the middle temporal area (MT) and to compare them to effects on human motion discrimination. After 3 s of adaptation to a random dot pattern moving in the preferred direction, MT neuronal responses to subsequent test patterns were reduced by 26% on average compared with adaptation to a static pattern. This reduction in response magnitude was largely independent of what test stimulus was presented. However, adaptation in the opposite direction changed responses less often and very inconsistently. Therefore motion adaptation systematically and profoundly affects the neurons in MT representing the adapted direction, but much less those representing the opposite direction. In human psychophysical experiments, such adapting stimuli affected direction discrimination, biasing choices away from the adaptation direction. The magnitude of this perceptual shift was consistent with the magnitude of the changes seen in area MT, if one assumes that a motion comparison step occurs after MT.


Some computational theories of motion perception assume that the first stage en route to this perception is the local estimate of image velocity. However, this assumption is not supported by data from the primary visual cortex. Its motion sensitive cells are not selective to velocity, but rather are directionally selective and tuned to spatio-temporal frequen­cies. Accordingly, physiologically based theories start with filters selec­tive to oriented spatio-temporal frequencies. This paper shows that computational and physiological theories do not necessarily conflict, because such filters may, as a population, compute velocity locally. To prove this point, we show how to combine the outputs of a class of frequency tuned filters to detect local image velocity. Furthermore, we show that the combination of filters may simulate ‘Pattern’ cells in the middle temporal area (MT), whereas each filter simulates primary visual cortex cells. These simulations include three properties of the primary cortex. First, the spatio-temporal frequency tuning curves of the in­dividual filters display approximate space-time separability. Secondly, their direction-of-motion tuning curves depend on the distribution of orientations of the components of the Fourier decomposition and speed of the stimulus. Thirdly, the filters show facilitation and suppression for responses to apparent motions in the preferred and null directions, respect­ively. It is suggested that the MT’s role is not to solve the aperture problem, but to estimate velocities from primary cortex information. The spatial integration that accounts for motion coherence may be postponed to a later cortical stage.


1988 ◽  
Vol 60 (3) ◽  
pp. 940-965 ◽  
Author(s):  
M. R. Dursteler ◽  
R. H. Wurtz

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)


2021 ◽  
Vol 118 (32) ◽  
pp. e2106235118
Author(s):  
Reuben Rideaux ◽  
Katherine R. Storrs ◽  
Guido Maiello ◽  
Andrew E. Welchman

Sitting in a static railway carriage can produce illusory self-motion if the train on an adjoining track moves off. While our visual system registers motion, vestibular signals indicate that we are stationary. The brain is faced with a difficult challenge: is there a single cause of sensations (I am moving) or two causes (I am static, another train is moving)? If a single cause, integrating signals produces a more precise estimate of self-motion, but if not, one cue should be ignored. In many cases, this process of causal inference works without error, but how does the brain achieve it? Electrophysiological recordings show that the macaque medial superior temporal area contains many neurons that encode combinations of vestibular and visual motion cues. Some respond best to vestibular and visual motion in the same direction (“congruent” neurons), while others prefer opposing directions (“opposite” neurons). Congruent neurons could underlie cue integration, but the function of opposite neurons remains a puzzle. Here, we seek to explain this computational arrangement by training a neural network model to solve causal inference for motion estimation. Like biological systems, the model develops congruent and opposite units and recapitulates known behavioral and neurophysiological observations. We show that all units (both congruent and opposite) contribute to motion estimation. Importantly, however, it is the balance between their activity that distinguishes whether visual and vestibular cues should be integrated or separated. This explains the computational purpose of puzzling neural representations and shows how a relatively simple feedforward network can solve causal inference.


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