A relationship between behavioral choice and the visual responses of neurons in macaque MT

1996 ◽  
Vol 13 (1) ◽  
pp. 87-100 ◽  
Author(s):  
K. H. Britten ◽  
W. T. Newsome ◽  
M. N. Shadlen ◽  
S. Celebrini ◽  
J. A. Movshon

AbstractWe have previously documented the exquisite motion sensitivity of neurons in extrastriate area MT by studying the relationship between their responses and the direction and strength of visual motion signals delivered to their receptive fields. These results suggested that MT neurons might provide the signals supporting behavioral choice in visual discrimination tasks. To approach this question from another direction, we have now studied the relationship between the discharge of MT neurons and behavioral choice, independently of the effects of visual stimulation. We found that trial-to-trial variability in neuronal signals was correlated with the choices the monkey made. Therefore, when a directionally selective neuron in area MT fires more vigorously, the monkey is more likely to make a decision in favor of the preferred direction of the cell. The magnitude of the relationship was modest, on average, but was highly significant across a sample of 299 cells from four monkeys. The relationship was present for all stimuli (including those without a net motion signal), and for all but the weakest responses. The relationship was reduced or eliminated when the demands of the task were changed so that the directional signal carried by the cell was less informative. The relationship was evident within 50 ms of response onset, and persisted throughout the stimulus presentation. On average, neurons that were more sensitive to weak motion signals had a stronger relationship to behavior than those that were less sensitive. These observations are consistent with the idea that neuronal signals in MT are used by the monkey to determine the direction of stimulus motion. The modest relationship between behavioral choice and the discharge of any one neuron, and the prevalence of the relationship across the population, make it likely that signals from many neurons are pooled to form the data on which behavioral choices are based.

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)


1993 ◽  
Vol 69 (3) ◽  
pp. 902-914 ◽  
Author(s):  
C. L. Colby ◽  
J. R. Duhamel ◽  
M. E. Goldberg

1. The middle temporal area (MT) projects to the intraparietal sulcus in the macaque monkey. We describe here a discrete area in the depths of the intraparietal sulcus containing neurons with response properties similar to those reported for area MT. We call this area the physiologically defined ventral intraparietal area, or VIP. In the present study we recorded from single neurons in VIP of alert monkeys and studied their visual and oculomotor response properties. 2. Area VIP has a high degree of selectivity for the direction of a moving stimulus. In our sample 72/88 (80%) neurons responded at least twice as well to a stimulus moving in the preferred direction compared with a stimulus moving in the null direction. The average response to stimuli moving in the preferred direction was 9.5 times as strong as the response to stimuli moving in the opposite direction, as compared with 10.9 times as strong for neurons in area MT. 3. Many neurons were also selective for speed of stimulus motion. Quantitative data from 25 neurons indicated that the distribution of preferred speeds ranged from 10 to 320 degrees/s. The degree of speed tuning was on average twice as broad as that reported for area MT. 4. Some neurons (22/41) were selective for the distance at which a stimulus was presented, preferring a stimulus of equivalent visual angle and luminance presented near (within 20 cm) or very near (within 5 cm) the face. These neurons maintained their preference for near stimuli when tested monocularly, suggesting that visual cues other than disparity can support this response. These neurons typically could not be driven by small spots presented on the tangent screen (at 57 cm). 5. Some VIP neurons responded best to a stimulus moving toward the animal. The absolute direction of visual motion was not as important for these cells as the trajectory of the stimulus: the best stimulus was one moving toward a particular point on the face from any direction. 6. VIP neurons were not active in relation to saccadic eye movements. Some neurons (10/17) were active during smooth pursuit of a small target. 7. The predominance of direction and speed selectivity in area VIP suggests that it, like other visual areas in the dorsal stream, may be involved in the analysis of visual motion.


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.


1999 ◽  
Vol 81 (4) ◽  
pp. 1783-1794 ◽  
Author(s):  
Eyal Seidemann ◽  
William T. Newsome

Effect of spatial attention on the responses of area MT neurons. This study examines the influence of spatial attention on the responses of neurons in the middle temporal visual area (MT or V5) of extrastriate cortex. Two monkeys were trained to perform a direction-discrimination task. On each trial, two apertures of random-dot stimuli appeared simultaneously at two spatially separated locations; the monkeys were required to discriminate the direction of stimulus motion at one location while ignoring the stimulus at the other location. After extensive training, we recorded the responses of MT neurons in two configurations: 1) Both apertures placed “within” the neuron’s receptive field (RF) and 2) one aperture covering the RF while the other was presented at a “remote” location. For each unit we compared the responses to identical stimulus displays when the monkey was instructed to attend to one or the other aperture. The responses of MT neurons were 8.7% stronger, on average, when the monkey attended to the spatial location that contained motion in the “preferred” direction. Attentional effects were equal, on average, in the within RF and remote configurations. The attentional modulations began ∼300 ms after stimulus onset, gradually increased throughout the trial, and peaked near stimulus offset. An analysis of the neuronal responses on error trials suggests that the monkeys failed to attend to the appropriate spatial location on these trials. The relatively weak attentional effects that we observed contrast strikingly with recent results of Treue and Maunsell, who demonstrated very strong attentional modulations (median effect >80%) in MT in a task that shares many features with ours. Our results suggest that spatial attention alone is not sufficient to induce strong attentional effects in MT even when two competing motion stimuli appear within the RF of the recorded neuron. The difference between our results and those of Treue and Maunsell suggests that the magnitude of the attentional effects in MT may depend critically on how attention is directed to a particular stimulus and on the precise demands of the task.


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.


1991 ◽  
Vol 66 (2) ◽  
pp. 485-496 ◽  
Author(s):  
D. L. Robinson ◽  
J. W. McClurkin ◽  
C. Kertzman ◽  
S. E. Petersen

1. We recorded from single neurons in awake, trained rhesus monkeys in a lighted environment and compared responses to stimulus movement during periods of fixation with those to motion caused by saccadic or pursuit eye movements. Neurons in the inferior pulvinar (PI), lateral pulvinar (PL), and superior colliculus were tested. 2. Cells in PI and PL respond to stimulus movement over a wide range of speeds. Some of these cells do not respond to comparable stimulus motion, or discharge only weakly, when it is generated by saccadic or pursuit eye movements. Other neurons respond equivalently to both types of motion. Cells in the superficial layers of the superior colliculus have similar properties to those in PI and PL. 3. When tested in the dark to reduce visual stimulation from the background, cells in PI and PL still do not respond to motion generated by eye movements. Some of these cells have a suppression of activity after saccadic eye movements made in total darkness. These data suggest that an extraretinal signal suppresses responses to visual stimuli during eye movements. 4. The suppression of responses to stimuli during eye movements is not an absolute effect. Images brighter than 2.0 log units above background illumination evoke responses from cells in PI and PL. The suppression appears stronger in the superior colliculus than in PI and PL. 5. These experiments demonstrate that many cells in PI and PL have a suppression of their responses to stimuli that cross their receptive fields during eye movements. These cells are probably suppressed by an extraretinal signal. Comparable effects are present in the superficial layers of the superior colliculus. These properties in PI and PL may reflect the function of the ascending tectopulvinar system.


2015 ◽  
Vol 113 (5) ◽  
pp. 1545-1555 ◽  
Author(s):  
Douglas A. Ruff ◽  
Richard T. Born

Attending to a stimulus modulates the responses of sensory neurons that represent features of that stimulus, a phenomenon named “feature attention.” For example, attending to a stimulus containing upward motion enhances the responses of upward-preferring direction-selective neurons in the middle temporal area (MT) and suppresses the responses of downward-preferring neurons, even when the attended stimulus is outside of the spatial receptive fields of the recorded neurons (Treue S, Martinez-Trujillo JC. Nature 399: 575–579, 1999). This modulation renders the representation of sensory information across a neuronal population more selective for the features present in the attended stimulus (Martinez-Trujillo JC, Treue S. Curr Biol 14: 744–751, 2004). We hypothesized that if feature attention modulates neurons according to their tuning preferences, it should also be sensitive to their tuning strength, which is the magnitude of the difference in responses to preferred and null stimuli. We measured how the effects of feature attention on MT neurons in rhesus monkeys ( Macaca mulatta) depended on the relationship between features—in our case, direction of motion and binocular disparity—of the attended stimulus and a neuron's tuning for those features. We found that, as for direction, attention to stimuli containing binocular disparity cues modulated the responses of MT neurons and that the magnitude of the modulation depended on both a neuron's tuning preferences and its tuning strength. Our results suggest that modulation by feature attention may depend not just on which features a neuron represents but also on how well the neuron represents those features.


2003 ◽  
Vol 89 (1) ◽  
pp. 246-256 ◽  
Author(s):  
Jing Liu ◽  
William T. Newsome

We analyzed the functional organization of speed tuned neurons in extrastriate visual area MT. We sought to determine whether neurons tuned for particular speeds are clustered spatially and whether such spatial clusters are elongated normal to the cortical surface so as to form speed columns. Our data showed that MT neurons are indeed clustered according to preferred speed. Multiunit recordings were speed tuned, and the speed tuning of these signals was well correlated with the speed tuning of single neurons recorded simultaneously. To determine whether speed columns exist in MT, we compared the rates at which preferred speed changed in electrode tracks that traversed MT obliquely and normally to the cortical surface. If speed columns exist, the preferred speed should change at a faster rate during oblique electrode tracks. We found, however, that preferred speed changed at similar rates for either type of penetration. In the same data set, the rate of change of preferred direction and preferred disparity differed substantially in normal and oblique penetrations as expected from the known columnar organization of MT. Thus our results suggest that a columnar organization for speed tuned neurons does not exist in MT.


2016 ◽  
Author(s):  
Bastian Schledde ◽  
F. Orlando Galashan ◽  
Magdalena Przybyla ◽  
Andreas K. Kreiter ◽  
Detlef Wegener

AbstractNon-spatial selective attention is based on the notion that specific features or objects in the visual environment are effectively prioritized in cortical visual processing. Feature-based attention (FBA) in particular, is a well-studied process that dynamically and selectively enhances neurons preferentially processing the attended feature attribute (e.g. leftward motion). In everyday life, however, behavior may require high sensitivity for an entire feature dimension (e.g. motion). Yet, evidence for feature dimension-specific attentional modulation on a cellular level is lacking. We here investigate neuronal activity in macaque motion-selective medio-temporal area (MT) in an experimental setting requiring the monkeys to detect either a motion change or a color change. We hypothesized that neural activity in MT is enhanced if the task requires perceptual sensitivity to motion. Despite identical visual stimulation, we found that mean firing rates were higher in the motion task, and response variability and latency were lower as compared to the color task. This task-specific response modulation in the processing of visual motion was independent from the relation between attended and stimulating motion direction. It emerged already in the absence of visual input, and consisted of a spatially global and tuning-independent shift of the MT baseline activity. The results provide single cell support for the hypothesis of a feature dimension-specific top-down signal emphasizing the processing of an entire feature class.


2016 ◽  
Author(s):  
Liu D. Liu ◽  
Christopher C. Pack

SummaryPerceptual decisions require the transformation of raw sensory inputs into cortical representations suitable for stimulus discrimination. One of the best-known examples of this transformation involves the middle temporal area (MT) of the primate visual cortex. Area MT provides a robust representation of stimulus motion, and previous work has shown that it contributes causally to performance on motion discrimination tasks. Here we report that the strength of this contribution can be highly plastic: Depending on the recent training history, pharmacological inactivation of MT can severely impair motion discrimination, or it can have little detectable influence. Similarly, depending on training, microstimulation can bias motion perception or simply introduce noise. Further analysis of neural and behavioral data suggests that training shifts the readout of motion information between MT and lower-level cortical areas. These results show that the contribution of individual brain regions to conscious perception can shift flexibly depending on sensory experience.


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