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Shintaro Funahashi

Publications and source records attributed to Shintaro Funahashi.

9 recordsLinked to original sources

Contributions of prefrontal cue-, delay-, and response-period activity to the decision process of saccade direction in a free-choice ODR task.

To examine how the dorsolateral prefrontal cortex (DLPFC) contributes to the decision process of the saccade direction, we recorded single-neuron activity while two monkeys performed two oculomotor delayed-response (ODR) tasks. In an ordinary ODR task, monkeys were required to make a memory-guided saccade to the cue location after a 3-s delay. In a self-selection version of the ODR task (S-ODR), four identical visual cues were presented simultaneously at the cue period, and monkeys were required to make a saccade toward any one of four directions after a 3-s delay. By comparing the same neuron's activity between two tasks, we found (1) neurons having directional cue-period activity in the ODR task did not show directionally selective activity in the S-ODR task, (2) neurons having directional pre-saccadic activity showed highly similar directional preferences in two tasks and exhibited temporal coupling between the onset of pre-saccadic activity and the initiation of saccadic eye movements, (3) neurons with directional delay-period activity in the ODR task exhibited similar directional preferences and showed gradual increase in the strength of the directional selectivity toward the end of the delay period in the S-ODR task. These results suggest that directional delay-period activity contributes to the decision process of the saccade direction in the S-ODR task, while directional cue-period and pre-saccadic activities do not. The gradual increase of the directional selectivity in delay-period activity might correspond to neural correlates of the decision process of the saccade direction in the S-ODR task.

Action Potentials↗

Reward-period activity in primate dorsolateral prefrontal and orbitofrontal neurons is affected by reward schedules.

Reward-period activity observed in the dorsolateral prefrontal cortex (DLPFC) and the orbitofrontal cortex (OFC) is thought to represent the detection of reward delivery. To investigate whether this activity plays the same role in these areas, we examined this activity under different reward schedules and whether the reward schedule has similar effects on this activity in each of these areas. A monkey performed an oculomotor delayed-response (ODR) task under two reward schedules. In the ODR-1 schedule, the monkey received a large amount of reward only after four successful trials, whereas in the ODR-2 schedule, it received a small amount of reward after every successful trial. Although reward-period activity was observed in both areas, more neurons exhibited this activity in the OFC. Reward-period activity was modulated by the proximity to reward delivery in both areas and this feature was observed more frequently in the OFC. The onset time of this activity also gradually advanced depending on the proximity to reward delivery. Moreover, many OFC neurons with this activity responded to free reward delivery. These results indicate that reward-period activity in the OFC represents the detection of reward delivery and that the gradual change in the magnitude and the onset time of this activity represents the expectation of reward delivery. Similar features of reward-period activity were observed in DLPFC neurons, although a significant number of DLPFC neurons did not respond to free reward delivery and no advance was observed in the onset time of this activity. These results suggest that reward-period activity in the DLPFC participates in whether or not correct performance was achieved. Thus, although similar reward-period activity was observed in both areas, the activity in the OFC represents the detection of reward delivery and is affected by the monkey's motivational state, whereas that in the DLPFC seems to participate in monitoring whether or not the necessary performance is achieved.

Action Potentials↗

Population vector analysis of primate prefrontal activity during spatial working memory.

Population vectors were used to examine information represented by a population of prefrontal activity and its temporal change during spatial working memory processes while monkeys performed ODR and R-ODR tasks. In the ODR task, monkeys made a saccade to the cue location after the delay, whereas in the R-ODR task, they made a saccade 90 degrees clockwise from the cue location. We first constructed population vectors using cue- and response-period activity. The directions of population vectors were similar to the cue directions and the saccade target directions, respectively, indicating that population vectors correctly represented information regarding directions of visual cues and saccade targets. We then calculated population vectors during a 250 ms time-window from the cue presentation to the end of the response period. In the ODR task, all population vectors were directed toward the cue direction. However, in the R-ODR task, the population vector gradually rotated during the delay period from the cue direction to the saccade direction. These results indicate that spatial information represented by a population of prefrontal activity can be shown as the direction of the population vector and that its temporal change during spatial working memory tasks can be depicted as the temporal change of the vector's direction.

Animals↗

Neuronal activity throughout the primate mediodorsal nucleus of the thalamus during oculomotor delayed-responses. I. Cue-, delay-, and response-period activity.

The thalamic mediodorsal nucleus (MD) has strong reciprocal connections with the dorsolateral prefrontal cortex (DLPFC), suggesting that the MD, like the DLPFC, participates in higher cognitive functions. To examine MD's participation in cognitive functions, we analyzed the characteristics of task-related activities sampled homogeneously from the MD while two monkeys performed a spatial working memory task using oculomotor responses. Of 141 task-related MD neurons, 26, 53, and 84% exhibited cue-, delay-, and response-period activity, respectively. Most of cue- and response-period activities showed phasic excitation, and most of delay-period activity showed tonic sustained activation. Among neurons with response-period activity, 74% exhibited presaccadic activity. Most cue-period, delay-period, and presaccadic activities were directional, whereas most postsaccadic activity was omni-directional. A significant contralateral bias in the best directions was present in cue-period and presaccadic activity. However, such bias was not present in delay-period activity, although most neurons had a best direction toward the contralateral visual field. We compared these characteristics with those observed in DLPFC neurons. Response-period activity was more frequently observed in the MD (84%) than in the DLPFC (56%). The directional selectivity and bias of task-related activities and the ratios of pre- and postsaccadic activities were different between MD and DLPFC. These results indicate that the MD participates in higher cognitive functions such as spatial working memory. However, the manner in which these two structures participate in these processes differs, in that the MD participates more in motor control aspects compared with the DLPFC.

Animals↗

Neuronal activity throughout the primate mediodorsal nucleus of the thalamus during oculomotor delayed-responses. II. Activity encoding visual versus motor signal.

We collected single-neuron activity from the mediodorsal (MD) nucleus of the thalamus, examined the information that was represented by task-related activity during performance of a spatial working memory task, and compared the present results with those obtained in the dorsolateral prefrontal cortex (DLPFC). We used two oculomotor delayed-response (ODR) tasks. In the ordinary ODR task, monkeys were required to make a memory-guided saccade to the location where a visual cue had been presented 3 s previously, whereas in the rotatory ODR task, they were required to make a memory-guided saccade 90 degrees clockwise from the cue direction. By comparing the best directions of the same task-related activity between the two tasks, we could determine whether this activity represented the cue location or the saccade direction. All cue-period activity represented the cue location. In contrast, 56% of delay-period activity represented the cue location and 41% represented the saccade direction. Almost all response-period activity represented the saccade direction. These results indicate that task-related MD activity represents either visual or motor information, suggesting that the MD participates in sensory-to-motor information processing. However, a greater proportion of delay- and response-period activities represented the saccade direction in the MD than in the DLPFC, indicating that more MD neurons participate in prospective information processing than DLPFC neurons. These results suggest that although functional interactions between the MD and DLPFC are crucial to cognitive functions such as working memory, there is a difference in how the MD and DLPFC participate in these functions.

Animals↗

Neural mechanisms of spatial working memory: contributions of the dorsolateral prefrontal cortex and the thalamic mediodorsal nucleus.

The dorsolateral prefrontal cortex (DLPFC) has been known to play an important role in working memory. Neurophysiological studies have revealed that delay period activity observed in the DLPFC is a neural correlate of the temporary storage mechanism for information and that this activity represents either retrospective or prospective information, although the majority represents retrospective information. However, the DLPFC is not the only brain area related to working memory. The analysis of neural activity in the thalamic mediodorsal (MD) nucleus reveals that the MD also participates in working memory. Although similar task-related activities were observed in the MD, the directional bias of these activities and the proportion of presaccadic activity are different between the MD and the DLPFC. These results indicate that, although the MD participates in working memory, the way it participates in this process is different between these two areas, in that the MD participates more in motor control aspects than the DLPFC does.

Animals↗

Prefrontal delay-period activity is affected by visual cues presented outside the memory field.

To examine interactions between primate prefrontal neurons having memory fields, we examined whether primate prefrontal delay-period activity produced by a visual cue presented inside the neuron's memory field is affected by an additional visual cue presented inside or outside the memory field in 39 prefrontal neurons. Delay-period activity was either diminished (43%) or enhanced (16%) when an additional cue was presented at a certain area in the visual field. Since functional interactions among neighboring prefrontal neurons were present, these modulation could be caused by the interactions between neurons having memory fields in different positions.

Animals↗

Prefrontal task-related activity representing visual cue location or saccade direction in spatial working memory tasks.

To examine what kind of information task-related activity encodes during spatial working memory processes, we analyzed single-neuron activity in the prefrontal cortex while two monkeys performed two different oculomotor delayed-response (ODR) tasks. In the standard ODR task, monkeys were required to make a saccade to the cue location after a 3-s delay, whereas in the rotatory ODR (R-ODR) task, they were required to make a saccade 90 degrees clockwise from the cue location after the 3-s delay. By comparing the same task-related activities in these two tasks, we could determine whether such activities encoded the location of the visual cue or the direction of the saccade. One hundred twenty one neurons exhibited task-related activity in relation to at least one task event in both tasks. Among them, 41 neurons exhibited directional cue-period activity, most of which encoded the location of the visual cue. Among 56 neurons with directional delay-period activity, 86% encoded the location of the visual cue, whereas 13% encoded the direction of the saccade. Among 57 neurons with directional response-period activity, 58% encoded the direction of the saccade, whereas 35% encoded the location of the visual cue. Most neurons whose response-period activity encoded the location of the visual cue also exhibited directional delay-period activity that encoded the location of the visual cue as well. The best directions of these two activities were identical, and most of these response-period activities were postsaccadic. Therefore this postsaccadic activity can be considered a signal to terminate unnecessary delay-period activity. Population histograms encoding the location of the visual cue showed tonic sustained activation during the delay period. However, population histograms encoding the direction of the saccade showed a gradual increase in activation during the delay period. These results indicate that the transformation from visual input to motor output occurs in the dorsolateral prefrontal cortex. The analysis using population histograms suggests that this transformation occurs gradually during the delay period.

Animals↗

Information processes in the primate prefrontal cortex in relation to working memory processes.

Working memory is a mechanism for short-term active storage of information as well as for processing stored information. Although evidence for neuronal mechanisms of temporary storage of information has accumulated for the prefrontal cortex, little is known about neuronal mechanisms for processing information. To understand how information is processed by prefrontal neurons, we first need to know what information is represented by single-neuron activity, and then examine how information represented by single-neuron activity or a population of activities changes along the temporal sequence of the trial. By examining task-related single-neuron activities while monkeys performed various working memory tasks, delay-period activity observed in the prefrontal cortex is considered to be a neuronal correlate of the mechanism for temporary active storage of information. Delay-period activity represents a variety of information including the spatial position and the physical feature of the stimulus, the forthcoming behavioral response, the quality of reward that the subject would receive, the difference of the task, or the rule of the task. Although delay-period activity could represent this variety of information, the information represented by delay-period activity is only the information relevant for task performance. In addition, using complex conditional tasks, delay-period activity has been shown to represent several kinds of information simultaneously. Based on these results, we examined how information represented by a population of prefrontal activities changes along the temporal sequence of the trial. Using two kinds of oculomotor delayed-response tasks, we first identified what information each task-related activity represents. Then, using population vector analysis, we could not only visualize information represented by a population of prefrontal activities, but also demonstrate the temporal change of information represented by a population of prefrontal activities. These attempts are important to understand information processes for working memory.

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