scholarly journals Compound stimuli reveal the structure of visual motion selectivity in macaque MT neurons

2019 ◽  
Author(s):  
Andrew D Zaharia ◽  
Robbe L T Goris ◽  
J Anthony Movshon ◽  
Eero P Simoncelli

AbstractMotion selectivity in primary visual cortex (V1) is approximately separable in orientation, spatial frequency, and temporal frequency (“frequency-separable”). Models for area MT neurons posit that their selectivity arises by combining direction-selective V1 afferents whose tuning is organized around a tilted plane in the frequency domain, specifying a particular direction and speed (“velocity-separable”). This construction explains “pattern direction selective” MT neurons, which are velocity-selective but relatively invariant to spatial structure, including spatial frequency, texture and shape. Surprisingly, when tested with single drifting gratings, most MT neurons’ responses are fit equally well by models with either form of separability. However, responses to plaids (sums of two moving gratings) tend to be better described as velocity-separable, especially for pattern neurons. We conclude that direction selectivity in MT is primarily computed by summing V1 afferents, but pattern-invariant velocity tuning for complex stimuli may arise from local, recurrent interactions.Significance StatementHow do sensory systems build representations of complex features from simpler ones? Visual motion representation in cortex is a well-studied example: the direction and speed of moving objects, regardless of shape or texture, is computed from the local motion of oriented edges. Here we quantify tuning properties based on single-unit recordings in primate area MT, then fit a novel, generalized model of motion computation. The model reveals two core properties of MT neurons — speed tuning and invariance to local edge orientation — result from a single organizing principle: each MT neuron combines afferents that represent edge motions consistent with a common velocity, much as V1 simple cells combine thalamic inputs consistent with a common orientation.

2005 ◽  
Vol 94 (6) ◽  
pp. 4156-4167 ◽  
Author(s):  
Daniel Zaksas ◽  
Tatiana Pasternak

Neurons in cortical area MT have localized receptive fields (RF) representing the contralateral hemifield and play an important role in processing visual motion. We recorded the activity of these neurons during a behavioral task in which two monkeys were required to discriminate and remember visual motion presented in the ipsilateral hemifield. During the task, the monkeys viewed two stimuli, sample and test, separated by a brief delay and reported whether they contained motion in the same or in opposite directions. Fifty to 70% of MT neurons were activated by the motion stimuli presented in the ipsilateral hemifield at locations far removed from their classical receptive fields. These responses were in the form of excitation or suppression and were delayed relative to conventional MT responses. Both excitatory and suppressive responses were direction selective, but the nature and the time course of their directionality differed from the conventional excitatory responses recorded with stimuli in the RF. Direction selectivity of the excitatory remote response was transient and early, whereas the suppressive response developed later and persisted after stimulus offset. The presence or absence of these unusual responses on error trials, as well as their magnitude, was affected by the behavioral significance of stimuli used in the task. We hypothesize that these responses represent top-down signals from brain region(s) accessing information about stimuli in the entire visual field and about the behavioral state of the animal. The recruitment of neurons in the opposite hemisphere during processing of behaviorally relevant visual signals reveals a mechanism by which sensory processing can be affected by cognitive task demands.


2016 ◽  
Vol 115 (6) ◽  
pp. 2705-2720 ◽  
Author(s):  
Helena X. Wang ◽  
J. Anthony Movshon

Neurons in area MT/V5 of the macaque visual cortex encode visual motion. Some cells are selective for the motion of oriented features (component direction-selective, CDS); others respond to the true direction of complex patterns (pattern-direction selective, PDS). There is a continuum of selectivity in MT, with CDS cells at one extreme and PDS cells at the other; we compute a pattern index that captures this variation. It is unknown how a neuron's pattern index is related to its other tuning characteristics. We therefore analyzed the responses of 792 MT cells recorded in the course of other experiments from opiate-anesthetized macaque monkeys, as a function of the direction, spatial frequency, drift rate, size, and contrast of sinusoidal gratings and of the direction and speed of random-dot textures. We also compared MT responses to those of 718 V1 cells. As expected, MT cells with higher pattern index tended to have stronger direction selectivity and broader direction tuning to gratings, and they responded better to plaids than to gratings. Strongly PDS cells also tended to have smaller receptive fields and stronger surround suppression. Interestingly, they also responded preferentially to higher drift rates and higher speeds of moving dots. The spatial frequency preferences of PDS cells depended strongly on their preferred temporal frequencies, whereas these preferences were independent in component-selective cells. Pattern direction selectivity is statistically associated with many response properties of MT cells but not strongly associated with any particular property. Pattern-selective signals are thus available in association with most other signals exported by MT.


2019 ◽  
Author(s):  
Marie Tolkiehn ◽  
Simon R. Schultz

AbstractOrientation tuning in mouse primary visual cortex (V1) has long been reported to have a random or “salt-and-pepper” organisation, lacking the structure found in cats and primates. Laminar in-vivo multi-electrode array recordings here reveal previously elusive structure in the representation of visual patterns in the mouse visual cortex, with temporo-nasally drifting gratings eliciting consistently highest neuronal responses across cortical layers and columns, whilst upward moving gratings reliably evoked the lowest activities. We suggest this bias in direction selectivity to be behaviourally relevant as objects moving into the visual field from the side or behind may pose a predatory threat to the mouse whereas upward moving objects do not. We found furthermore that direction preference and selectivity was affected by stimulus spatial frequency, and that spatial and directional tuning curves showed high signal correlations decreasing with distance between recording sites. In addition, we show that despite this bias in direction selectivity, it is possible to decode stimulus identity and that spatiotemporal features achieve higher accuracy in the decoding task whereas spike count or population counts are sufficient to decode spatial frequencies implying different encoding strategies.Significance statementWe show that temporo-nasally drifting gratings (i.e. opposite the normal visual flow during forward movement) reliably elicit the highest neural activity in mouse primary visual cortex, whereas upward moving gratings reliably evoke the lowest responses. This encoding may be highly behaviourally relevant, as objects approaching from the periphery may pose a threat (e.g. predators), whereas upward moving objects do not. This is a result at odds with the belief that mouse primary visual cortex is randomly organised. Further to this biased representation, we show that direction tuning depends on the underlying spatial frequency and that tuning preference is spatially correlated both across layers and columns and decreases with cortical distance, providing evidence for structural organisation in mouse primary visual cortex.


1992 ◽  
Vol 67 (6) ◽  
pp. 1437-1446 ◽  
Author(s):  
P. Girard ◽  
P. A. Salin ◽  
J. Bullier

1. Behavioral results in the monkey and clinical studies in human show remarkable residual visual capacities after a lesion of area V1. Earlier work by Rodman et al. demonstrated that visual activity can be recorded in the middle temporal area (MT) of the macaque monkey several weeks after a complete lesion of V1. These authors also tested the effect of a reversible block of area V1 on the visual responses of a small number of neurons in area MT and showed that most of these cells remain visually responsive. From the results of that study, however, it is difficult to assess the contribution of area 17 to the receptive-field selectivity of area MT neurons. To address this question, we have quantitatively measured the effects of a reversible inactivation of area 17 on the direction selectivity of MT neurons. 2. A circular part of the opercular region of area V1 was reversibly inactivated by cooling with a Peltier device. A microelectrode was positioned in the lower layers of V1 to control the total inactivation of that area. Eighty percent of the sites recorded in the retinotopically corresponding region of MT during inactivation of V1 were found to be visually responsive. The importance of the effect was assessed by calculating the blocking index (0 for no effect, 1 for complete inactivation). Approximately one-half of the quantitatively studied neurons gave a blocking index below 0.6, illustrating the strong residual responses recorded in many neurons. 3. Receptive-field properties were examined with multihistograms. It was found that, during inactivation of V1, the preferred direction changed for most neurons but remained close to the preferred direction or to its opposite in the control situation. During inactivation of V1, the average tuning curve of neurons became broader mostly because of strong reductions in the response to directions close to the preferred and nonpreferred. Very little change was observed in the responses for directions at 90 degrees to the optimal. These results are consistent with a model in which direction selectivity is present without an input from V1 but is reinforced by the spatial organization of this excitatory input. 4. Residual responses were found to be highly dependent on the state of anesthesia because they were completely abolished by the addition of 0.4-0.5% halothane to the ventilation gases. Finally, visual responses were recorded in area MT several hours after an acute lesion of area 17.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 11 (2) ◽  
pp. 295-306 ◽  
Author(s):  
J. McLean ◽  
L. A. Palmer

AbstractThe amplitude spectra of simple cells in areas 17 and 18 were estimated in two and three dimensions (2–D and 3–D) using drifting sinusoidal gratings. In 2–D, responses were sampled with 16 x 16 resolution in spatial and temporal frequency at the optimal orientation. In 3–D, responses were sampled with 12 x 12 x 10 resolution in spatial frequency, orientation, and temporal frequency. For 45/50 cells studied, the spatial attributes of the receptive fields (RFs) were independent of temporal frequency except for a scale factor. The five exceptions to this general finding could be described as follows: For four area 17 cells, responses in the null direction increased with temporal frequency, reducing direction selectivity. For one area 18 cell, the optimal spatial frequency increased with temporal frequency and vice versa. The 2–D discrete Fourier transform was applied to all of the estimated amplitude spectra assuming zero spatial and temporal phase. These transforms were compared with the results of first-order reverse correlations as described in the previous paper (McLean et al., 1994). Direction selective cells exhibited excitatory subregions that were obliquely oriented in space-time in both the raw correlation data and inverse transforms of the spectral data. The slopes of the subregions found in these two measures were highly correlated. Direction indices obtained from space and frequency domain measures were comparable. We demonstrate that the spectral response profiles of most simple cells are aligned with the coordinate axes in frequency domain. That is, they may be considered one-quadrant separable, suggesting that these cells are not velocity tuned per se, but are tuned for spatiotemporal frequency. The spectral bandwidth establishes the range of velocities to which these cells will respond. These findings are consistent with the one-quadrant separability constraint of linear quadrature models. We conclude that most simple cells perform as roughly linear filters in two dimensions of space and time.


1984 ◽  
Vol 52 (6) ◽  
pp. 1106-1130 ◽  
Author(s):  
T. D. Albright

We recorded from single neurons in the middle temporal visual area (MT) of the macaque monkey and studied their direction and orientation selectivity. We also recorded from single striate cortex (V1) neurons in order to make direct comparisons with our observations in area MT. All animals were immobilized and anesthetized with nitrous oxide. Direction selectivity of 110 MT neurons was studied with three types of moving stimuli: slits, single spots, and random-dot fields. All of the MT neurons were found to be directionally selective using one or more of these stimuli. MT neurons exhibited a broad range of direction-tuning bandwidths to all stimuli (minimum = 32 degrees, maximum = 186 degrees, mean = 95 degrees). On average, responses were strongly unidirectional and of similar magnitude for all three stimulus types. Orientation selectivity of 89 MT neurons was studied with stationary flashed slits. Eighty-three percent were found to be orientation selective. Overall, orientation-tuning bandwidths were significantly narrower (mean = 64 degrees) than direction-tuning bandwidths for moving stimuli. Moreover, responses to stationary-oriented stimuli were generally smaller than those to moving stimuli. Direction selectivity of 55 V1 neurons was studied with moving slits; orientation selectivity of 52 V1 neurons was studied with stationary flashed slits. In V1, compared with MT, direction-tuning bandwidths were narrower (mean = 68 degrees). Moreover, V1 responses to moving stimuli were weaker, and bidirectional tuning was more common. The mean orientation-tuning bandwidth in V1 was also significantly narrower than that in MT (mean = 52 degrees), but the responses to stationary-oriented stimuli were of similar magnitude in the two areas. We examined the relationship between optimal direction and optimal orientation for MT neurons and found that 61% had an orientation preference nearly perpendicular to the preferred direction of motion, as is the case for all V1 neurons. However, another 29% of MT neurons had an orientation preference roughly parallel to the preferred direction. These observations, when considered together with recent reports claiming sensitivity of some MT neurons to moving visual patterns (39), suggest specific neural mechanisms underlying pattern-motion sensitivity in area MT. These results support the notion that area MT represents a further specialization over area V1 for stimulus motion processing. Furthermore, the marked similarities between direction and orientation tuning in area MT in macaque and owl monkey support the suggestion that these areas are homologues.


1998 ◽  
Vol 79 (3) ◽  
pp. 1481-1493 ◽  
Author(s):  
Michael R. Ibbotson ◽  
Colin W. G. Clifford ◽  
Richard F. Mark

Ibbotson, Michael R., Colin W. G. Clifford, and Richard F. Mark. Adaptation to visual motion in directional neurons of the nucleus of the optic tract. J. Neurophysiol. 79: 1481–1493, 1998. Extracellular recordings of action potentials were made from directional neurons in the nucleus of the optic tract (NOT) of the wallaby, Macropus eugenii, while stimulating with moving sine-wave gratings. When a grating was moved at a constant velocity in the preferred direction through a neuron's receptive field, the firing rate increased rapidly and then declined exponentially until reaching a steady-state level. The decline in response is called motion adaptation. The rate of adaptation increased as the temporal frequency of the drifting grating increased, up to the frequency that elicited the maximum firing rate. Beyond this frequency, the adaptation rate decreased. When the adapting grating's spatial frequency was varied, such that response magnitudes were significantly different, the maximum adaptation rate occurred at similar temporal frequencies. Hence the temporal frequency of the stimulus is a major parameter controlling the rate of adaptation. In most neurons, the temporal frequency response functions measured after adaptation were shifted to the right when compared with those obtained in the unadapted state. Further insight into the adaptation process was obtained by measuring the responses of the cells to grating displacements within one frame (10.23 ms). Such impulsive stimulus movements of less than a one-quarter cycle elicited a response that rose rapidly to a maximum and then declined exponentially to the spontaneous firing rate in several seconds. The level of adaptation was demonstrated by observing how the time constants of the exponentials varied as a function of the temporal frequency of a previously presented moving grating. When plotted as functions of adapting frequency, time constants formed a U-shaped curve. The shortest time constants occurred at similar temporal frequencies, regardless of changes in spatial frequency, even when the change in spatial frequency resulted in large differences in response magnitude during the adaptation period. The strongest adaptation occurred when the adapting stimulus moved in the neuron's preferred direction. Stimuli that moved in the antipreferred direction or flickered had an adapting influence on the responses to subsequent impulsive movements, but the effect was far smaller than that elicited by preferred direction adaptation. Adaptation in one region of the receptive field did not affect the responses elicited by subsequent stimulation in nonoverlapping regions of the field. Adaptation is a significant property of NOT neurons and probably acts to expand their temporal resolving power.


2001 ◽  
Vol 85 (1) ◽  
pp. 187-196 ◽  
Author(s):  
James W. Bisley ◽  
Daniel Zaksas ◽  
Tatiana Pasternak

We applied electrical stimulation to physiologically identified sites in macaque middle temporal area (MT) to examine its role in short-term storage of recently encoded information about stimulus motion. We used a behavioral task in which monkeys compared the directions of two moving random-dot stimuli, sample and test, separated by a 1.5-s delay. Four sample directions were used for each site, and the animals had to indicate whether the direction of motion in the sample was the same as or different to the direction of motion in the test. We found that the effect of stimulation of the same directional column in MT depended on the behavioral state of the animal. Although stimulation had strong effects when applied during the encoding and the storage components of the task, these effects were not equivalent. Stimulation applied during the presentation of the sample produced signals interpreted by the monkeys as directional motion. However, the same stimulation introduced during the period of storage no longer produced signals interpreted as unambiguous directional information. We conclude that the directional information used by the monkeys in the working memory task is likely to be provided by neurons in MT, and the use of this information appears to be dependent on the portion of the task during which stimulation was delivered. Finally, the disruptive effects of stimulation during the delay suggest that MT neurons not only participate in the encoding of visual motion information but also in its storage by either maintaining an active connection with the circuitry involved in storage or being an integral component of that circuitry.


2018 ◽  
Vol 30 (12) ◽  
pp. 3355-3392 ◽  
Author(s):  
Jonathan Vacher ◽  
Andrew Isaac Meso ◽  
Laurent U. Perrinet ◽  
Gabriel Peyré

A common practice to account for psychophysical biases in vision is to frame them as consequences of a dynamic process relying on optimal inference with respect to a generative model. The study presented here details the complete formulation of such a generative model intended to probe visual motion perception with a dynamic texture model. It is derived in a set of axiomatic steps constrained by biological plausibility. We extend previous contributions by detailing three equivalent formulations of this texture model. First, the composite dynamic textures are constructed by the random aggregation of warped patterns, which can be viewed as three-dimensional gaussian fields. Second, these textures are cast as solutions to a stochastic partial differential equation (sPDE). This essential step enables real-time, on-the-fly texture synthesis using time-discretized autoregressive processes. It also allows for the derivation of a local motion-energy model, which corresponds to the log likelihood of the probability density. The log likelihoods are essential for the construction of a Bayesian inference framework. We use the dynamic texture model to psychophysically probe speed perception in humans using zoom-like changes in the spatial frequency content of the stimulus. The human data replicate previous findings showing perceived speed to be positively biased by spatial frequency increments. A Bayesian observer who combines a gaussian likelihood centered at the true speed and a spatial frequency dependent width with a “slow-speed prior” successfully accounts for the perceptual bias. More precisely, the bias arises from a decrease in the observer's likelihood width estimated from the experiments as the spatial frequency increases. Such a trend is compatible with the trend of the dynamic texture likelihood width.


2007 ◽  
Vol 24 (1) ◽  
pp. 53-64 ◽  
Author(s):  
B.G. OUELLETTE ◽  
K. MINVILLE ◽  
D. BOIRE ◽  
M. PTITO ◽  
C. CASANOVA

In the cat, the analysis of visual motion cues has generally been attributed to the posteromedial lateral suprasylvian cortex (PMLS) (Toyama et al., 1985; Rauschecker et al., 1987; Rauschecker, 1988; Kim et al., 1997). The responses of neurons in this area are not critically dependent on inputs from the primary visual cortex (VC), as lesions of VC leave neuronal response properties in PMLS relatively unchanged (Spear & Baumann, 1979; Spear, 1988; Guido et al., 1990b). However, previous studies have used a limited range of visual stimuli. In this study, we assessed whether neurons in PMLS cortex remained direction-selective to complex motion stimuli following a lesion of VC, particularly to complex random dot kinematograms (RDKs). Unilateral aspiration of VC was performed on post-natal days 7–9. Single unit extracellular recordings were performed one year later in the ipsilateral PMLS cortex. As in previous studies, a reduction in the percentage of direction selective neurons was observed with drifting sinewave gratings. We report a previously unobserved phenomenon with sinewave gratings, in which there is a greater modulation of firing rate at the temporal frequency of the stimulus in animals with a lesion of VC, suggesting an increased segregation of ON and OFF sub-regions. A significant portion of neurons in PMLS cortex were direction selective to simple (16/18) and complex (11/16) RDKs. However, the strength of direction selectivity to both stimuli was reduced as compared to normals. The data suggest that complex motion processing is still present, albeit reduced, in PMLS cortex despite the removal of VC input. The complex RDK motion selectivity is consistent with both geniculo-cortical and extra-geniculate thalamo-cortical pathways in residual direction encoding.


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