Neurons in the middle temporal visual area (MT) have been implicated in the perception of visual motion, whereas prefrontal cortex (PFC) neurons have been linked to temporary storage of sensory signals, attentional and executive control of behavior. Using a task that placed demands on both sets of neurons, we investigated their contribution to working memory for visual motion. Monkeys compared the direction of two moving random-dot stimuli, sample and test, separated by a brief memory delay. Neurons in both areas showed robust direction-selective activity during all phases of the task. During the sample, ϳ60% of task-related PFC neurons were direction selective, and this selectivity emerged 40 ms later than in MT. Unlike MT, the PFC responses to sample did not correlate with behavioral choices, but their selectivity was modulated by task demands and diminished on error trials. Reliable directional signals were found in both areas during the memory delay, but these signals were transient rather than sustained by neurons of either area. Responses to the test in both areas were modulated by the remembered sample direction, decreasing when the test direction matched the sample. This decrease arose in the PFC 100 ms later than in MT and was predictive of the forthcoming decision. Our data suggest that neurons in the two regions are functionally connected and make unique contributions to different task components. PFC neurons reflect task-related information about visual motion and represent decisions that may be based, in part, on the comparison in MT between the remembered sample and test.

We recorded the activity of middle temporal (MT) neurons in 2 monkeys while they compared the directions of motion in 2 sequentially presented random-dot stimuli, sample and test, and reported them as the same or different by pressing one of 2 buttons. We found that MT neurons were active not only in response to the sample and test stimuli but also during the 1,500-ms delay separating them. Most neurons showed a characteristic pattern of activity consisting of a small burst of firing early in the delay, followed by a period of suppression and a subsequent increase in firing rate immediately preceding the presentation of the test stimulus. In a third of the neurons, the activity early in the delay not only reflected the direction of the sample stimulus, but was also related to the range of local directions it contained. During the middle of the delay the majority of neurons were suppressed, consistent with a gating mechanism that could be used to ignore task-irrelevant stimuli. Late in the delay, most neurons showed an increase in response, probably in anticipation of the upcoming test. Throughout most of the delay there was a directional signal in the population of MT neurons, manifested by higher firing rates following the sample moving in the antipreferred direction. Whereas some of these effects may be related to sensory adaptation, others are more likely to represent a more active task-related process. These results support the hypothesis that MT neurons actively participate in the successful execution of all aspects of the task requiring processing and remembering visual motion.

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.

When asked to compare two moving stimuli separated by a delay, observers must not only identify stimulus direction but also store it in memory. We examined the properties of this storage mechanism in two macaque monkeys by sequentially presenting two random-dot stimuli, sample and test, in opposite hemifields and introducing a random-motion mask during the delay. The mask interfered with performance only at the precise location of the test, 100-200 ms after the start of the delay, and when its size and speed matched those of the remembered sample. This selective interference suggests that the representation of the motion stimulus in memory preserves its direction, speed, and size and is most fragile shortly after the completion of the encoding phase of the task. This precise preservation of sensory attributes of the motion stimulus suggests that the neural mechanisms involved in the processing of visual motion may also be involved in its storage.

We asked if the information about stimulus motion used in a visual working-memory task is localized in space. Monkeys compared the directions of two moving random-dot stimuli, sample and test, separated by a temporal delay and reported whether the stimuli moved in the same or in different directions. By presenting the two comparison stimuli in separate locations in the visual field, we determined whether information about stimulus direction was spatially localized during the storage and retrieval/comparison components of the task. Two psychophysical measures of direction discrimination provided nearly identical estimates of the critical spatial separation between sample and test stimuli that lead to a loss in threshold. Direction range thresholds measured with dot stimuli consisting of a range of local directional vectors were affected by spatial separation when a random-motion mask was introduced during the delay into the location of the upcoming test. The selective masking at the test location suggests that the information about the remembered direction was localized and available at that location. Direction difference thresholds, measured with coherently moving random dots, were also affected by separation between the two comparison stimuli. The separation at which performance was affected in both tasks increased with retinal eccentricity in parallel with the increase in receptive-field size in neurons in cortical area MT. The loss with transfer of visual information between different spatial locations suggests a contribution of cortical areas with localized receptive fields to the performance of the memory task. The similarity in the spatial scale of the storage mechanism derived psychophysically and the receptive field size of neurons in area MT suggest that MT neurons are central to this task.