Kenneth H. Britten

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

We 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.

Responses of neurons in macaque MT to stochastic motion signals.

Dynamic random-dot stimuli have been widely used to explore central mechanisms of motion processing. We have measured the responses of neurons in area MT of the alert monkey while we varied the strength and direction of the motion signal in such displays. The strength of motion is controlled by the proportion of spatiotemporally correlated dots, which we term the correlation of the stimulus. For many MT cells, responses varied approximately linearly with stimulus correlation. When they occurred, nonlinearities were equally likely to be either positively or negatively accelerated. We also explored the relationship between response magnitude and response variance for these cells and found, in general agreement with other investigators, that this relationship conforms to a power law with an exponent slightly greater than 1. The variance of the cells discharge is little influenced by the trial-to-trial fluctuations inherent in our stochastic display, and is therefore likely to be of neural origin. Linear responses to these stochastic motion stimuli are predicted by simple, low-level motion models incorporating sensors having relatively broad spatial and temporal frequency tuning.

Neuronal mechanisms of motion perception.

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Effects of inferotemporal cortex lesions on form-from-motion discrimination in monkeys

SummaryThe inferotemporal cortex of primates plays a prominent role in the learning and retention of visual form discriminations. In this experiment we investigated the role of inferotemporal (IT) cortex in the discrimination of two-dimensional forms defined by motion cues. Six monkeys were trained to a criterion level of performance on two form-from-motion problems. Three of these animals received complete bilateral lesions of IT cortex, while the other three served as unoperated controls. All animals were then retrained to criterion to evaluate the effects of IT lesions on the retention of form-from-motion learning. Compared with the control group, the lesion group was significantly impaired on both problems. Following retention testing, we trained both groups of monkeys on two new form-from-motion problems to investigate the effects of IT lesions on acquisition rates for new learning. The lesion group performed well on the new problems; the learning rates of the operated and control groups were not significantly different. When forms were defined by luminance cues, monkeys with IT lesions, like those in previous studies, were impaired both for retention and for acquisition. These findings indicate that the anterograde effects of IT lesions on learning new form discriminations are less severe for forms defined by motion cues than for forms defined by luminance cues. However, the retrograde effects of IT lesions on retention are severe for forms defined by either cue.

Temporal Structure of Spike Trains from MT Neurons in the Awake Monkey

We compute the power spectrum associated with single-unit extracellular spike trains recorded in a previous study of 213 neurons in extrastriate area MT of the macaque monkey, a region that plays a major role in processing motion information. The data were recorded while monkeys performed a near-threshold direction discrimination task so that both physiological and psychophysical data could be obtained on the same set of trials [14]. (1) About half of the cells have a flat spectrum with a dip at low temporal frequencies, indicative of a Poisson process with a refractory period. (2) About half of the cells have a peak in the 25–50 Hz frequency band. (3) We show that the peak in the power spectrum is related to the cell’s tendency to fire bursts of action potentials and that the shape of the power spectrum can be described without assuming an explicit oscillatory neuronal mechanism. (4) We find no relationship between the shape of the power spectrum, in particular, the amplitude of the peak, and psychophysical measures of the monkeys’ performance on the direction discrimination task.