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Jun Tanji

Publications and source records attributed to Jun Tanji.

At least 19 recordsLinked to original sources

Categorization of behavioural sequences in the prefrontal cortex.

Although it has long been thought that the prefrontal cortex of primates is involved in the integrative regulation of behaviours, the neural architecture underlying specific aspects of cognitive behavioural planning has yet to be clarified. If subjects are required to remember a large number of complex motor sequences and plan to execute each of them individually, categorization of the sequences according to the specific temporal structure inherent in each subset of sequences serves to facilitate higher-order planning based on memory. Here we show, using these requirements, that cells in the lateral prefrontal cortex selectively exhibit activity for a specific category of behavioural sequences, and that categories of behaviours, embodied by different types of movement sequences, are represented in prefrontal cells during the process of planning. This cellular activity implies the generation of neural representations capable of storing structured event complexes at an abstract level, exemplifying the development of macro-structured action knowledge in the lateral prefrontal cortex.

Action Potentials↗

Activity in the lateral prefrontal cortex reflects multiple steps of future events in action plans.

To achieve a behavioral goal in a complex environment, we must plan multiple steps of motor behavior. On planning a series of actions, we anticipate future events that will occur as a result of each action and mentally organize the temporal sequence of events. To investigate the involvement of the lateral prefrontal cortex (PFC) in such multistep planning, we examined neuronal activity in the PFC of monkeys performing a maze task that required the planning of stepwise cursor movements to reach a goal. During the preparatory period, PFC neurons reflected each of all forthcoming cursor movements, rather than arm movements. In contrast, in the primary motor cortex, most neuronal activity reflected arm movements but little of cursor movements during the preparatory period, as well as during movement execution. Our data suggest that the PFC is involved primarily in planning multiple future events that occur as a consequence of behavioral actions.

Animals↗

Binary-coded monitoring of a behavioral sequence by cells in the pre-supplementary motor area.

To regulate the temporal structure of a series of behavioral sequences involving multiple actions, it is essential to monitor the progress of the entire behavioral process. To identify the involvement of three cortical motor areas in monitoring behavioral sequences, we examined neuronal activity while monkeys sequentially performed a series of motor tasks in accordance with a predetermined behavioral schedule that included a numerical structure. We found that neurons in the pre-supplementary motor area exhibited activity that appeared to monitor the performance of the behavioral trials in a binary-coded manner. One-half of the activity represented odd-numbered trials within a behavioral sequence, whereas the other one-half represented even-numbered trials. Such neuronal activity, resembling the operation of binary counting elements widely used for constructing artificial computing devices, was rare in the supplementary motor area or in the primary motor cortex.

Action Potentials↗

Differential involvement of neurons in the dorsal and ventral premotor cortex during processing of visual signals for action planning.

We examined neuronal activity in the dorsal and ventral premotor cortex (PMd and PMv, respectively) to explore the role of each motor area in processing visual signals for action planning. We recorded neuronal activity while monkeys performed a behavioral task during which two visual instruction cues were given successively with an intervening delay. One cue instructed the location of the target to be reached, and the other indicated which arm was to be used. We found that the properties of neuronal activity in the PMd and PMv differed in many respects. After the first cue was given, PMv neuron response mostly reflected the spatial position of the visual cue. In contrast, PMd neuron response also reflected what the visual cue instructed, such as which arm to be used or which target to be reached. After the second cue was given, PMv neurons initially responded to the cue's visuospatial features and later reflected what the two visual cues instructed, progressively increasing information about the target location. In contrast, the activity of the majority of PMd neurons responded to the second cue with activity reflecting a combination of information supplied by the first and second cues. Such activity, already reflecting a forthcoming action, appeared with short latencies (<400 ms) and persisted throughout the delay period. In addition, both the PMv and PMd showed bilateral representation on visuospatial information and motor-target or effector information. These results further elucidate the functional specialization of the PMd and PMv during the processing of visual information for action planning.

Animals↗

Design of a head fixation device for experiments in behaving monkeys.

We have designed a new device for head fixation of behaving monkeys. The fixation device consists of a duralumin head ring mounted with four screw holders. It is firmly fixed to the animal's skull with four stainless steel screw pins. The head ring is then attached to a primate chair in any desirable position and angle using a set of adjustable plates. The device has been used for behavioral training that requires accurate gaze monitoring and for recording single-unit activity over a several-month period. The advantage of our device is that it is simple to use; it can be attached readily without major surgical procedures and it can be quickly removed when experiments are not running. This head fixation system is suitable for behavioral experiments and single-unit recording studies. It may also be applicable for studies on functional imaging of the macaque brain, by constructing it of non-magnetic materials.

Action Potentials↗

Representation of immediate and final behavioral goals in the monkey prefrontal cortex during an instructed delay period.

We examined neuronal activity in the lateral prefrontal cortex of monkeys performing a path-planning task in a maze that required the planning of actions in multiple steps. The animals received an instruction that prompted them to prepare to move a cursor in the maze stepwise from a starting position to a goal position by operating manipulanda with either arm. During a delay period in which the animal prepared to start the first of three cursor movements to approach the pre-instructed goal, we identified two types of neuronal activity: the first type reflected the position within the maze to which the animal intended to move the cursor as an initial step (an immediate goal) and the second type reflected the position within the maze that was to be captured as a final goal. Neither type reflected motor responses. We propose that these two types of neuronal activity are neuronal correlates that represent immediate and ultimate behavioral goals. This finding implicates the prefrontal cortex in governing goal-oriented sequential behavior rather than sensorimotor transformation.

Algorithms↗

Neurons in the rostral cingulate motor area monitor multiple phases of visuomotor behavior with modest parametric selectivity.

We examined the cellular activity in the rostral cingulate motor area (CMAr) with respect to multiple behavioral factors that ranged from the retrieval and processing of associative visual signals to the planning and execution of instructed actions. We analyzed the neuronal activity in monkeys while they performed a behavioral task in which 2 visual instruction cues were given successively with an intervening delay. One cue instructed the location of the target to be reached; the other cue instructed which arm was to be used. After a second delay, the monkey received a motor-set cue to be prepared to initiate the motor task in accordance with instructions. Finally, after a GO signal, the monkey reached for the instructed target with the instructed arm. We found that the activity of neurons in the CMAr changed profoundly throughout the behavioral task, which suggested that the CMAr participated in each of the behavioral processing steps. However, the neuronal activity was only modestly selective for the spatial location of the visual signal. We also found that selectivity for the instructional information delivered with the signals (target location and arm use) was modest. Furthermore, during the motor-set and movement periods, few CMAr neurons exhibited selectivity for such motor parameters as the location of the target or the arm to be used. The abundance and robustness of the neuronal activity within the CMAr that reflected each step of the behavioral task and the modest selectivity of the same cells for sensorimotor parameters are strikingly different from the preponderance of selectivity that we have observed in other frontal areas. Based on these results, we propose that the CMAr participates in monitoring individual behavioral events to keep track of the progress of required behavioral tasks. On the other hand, CMAr activity during motor planning may reflect the emergence of a general intention for action.

Action Potentials↗

Prefrontal cortical cells projecting to the supplementary eye field and presupplementary motor area in the monkey.

We examined the location and spatial distribution of prefrontal cortical (PF) cells projecting to the supplementary eye field (SEF) and presupplementary motor area (pre-SMA) using a double retrograde-labeling technique in monkeys (Macaca fuscata). The SEF and pre-SMA were physiologically identified based on the findings of intracortical microstimulation and single cell recordings. Two fluorescent tracers, diamidino yellow and fast blue, were injected into the SEF and pre-SMA of each monkey. Retrogradely labeled cells in the PF were plotted with an automated plotting system. The cells projecting to the SEF and pre-SMA were mainly distributed in the upper and lower banks of the principal sulcus (area 46), with little overlap. Cells projecting to the SEF, but not to the pre-SMA, were observed in areas 8a, 8b, 9, 12, and 45. These findings suggest that the SEF and pre-SMA receive different sets of information from the PF cells.

Action Potentials↗

Involvement of the ventral premotor cortex in controlling image motion of the hand during performance of a target-capturing task.

The ventral premotor cortex (PMv) has been implicated in the visual guidance of movement. To examine whether neuronal activity in the PMv is involved in controlling the direction of motion of a visual image of the hand or the actual movement of the hand, we trained a monkey to capture a target that was presented on a video display using the same side of its hand as was displayed on the video display. We found that PMv neurons predominantly exhibited premovement activity that reflected the image motion to be controlled, rather than the physical motion of the hand. We also found that the activity of half of such direction-selective PMv neurons depended on which side (left versus right) of the video image of the hand was used to capture the target. Furthermore, this selectivity for a portion of the hand was not affected by changing the starting position of the hand movement. These findings suggest that PMv neurons play a crucial role in determining which part of the body moves in which direction, at least under conditions in which a visual image of a limb is used to guide limb movements.

Animals↗

Differential roles of neuronal activity in the supplementary and presupplementary motor areas: from information retrieval to motor planning and execution.

We explored functional differences between the supplementary and presupplementary motor areas (SMA and pre-SMA, respectively) systematically with respect to multiple behavioral factors, ranging from the retrieval and processing of associative visual signals to the planning and execution of target-reaching movement. We analyzed neuronal activity while monkeys performed a behavioral task in which two visual instruction cues were given successively with a delay: one cue instructed the location of the reach target, and the other instructed arm use (right or left). After a second delay, the monkey received a motor-set cue to be prepared to make the reaching movement as instructed. Finally, after a GO signal, it reached for the instructed target with the instructed arm. We found the following apparent differences in activity: 1) neuronal activity preceding the appearance of visual cues was more frequent in the pre-SMA; 2) a majority of pre-SMA neurons, but many fewer SMA neurons, responded to the first or second cue, reflecting what was shown or instructed; 3) in addition, pre-SMA neurons often reflected information combining the instructions in the first and second cues; 4) during the motor-set period, pre-SMA neurons preferentially reflected the location of the target, while SMA neurons mainly reflected which arm to use; and 5) when executing the movement, a majority of SMA neurons increased their activity and were largely selective for the use of either the ipsilateral or contralateral arm. In contrast, the activity of pre-SMA neurons tended to be suppressed. These findings point to the functional specialization of the two areas, with respect to receiving associative cues, information processing, motor behavior planning, and movement execution.

Animals↗

Cingulate cortical cells projecting to monkey frontal eye field and primary motor cortex.

We compared the distribution of cingulate cortical cells projecting to the frontal eye field (FEF) and primary motor cortex (MI) using a multiple retrograde labeling technique. Two fluorescent tracers were injected into physiologically identified FEF and MI in each monkey. The location of cells projecting to the forelimb area of MI served to identify the rostral (CMAr) and caudal (CMAc) cingulate motor areas. We found two foci of cells projecting to the FEF: rostral (CEFr) and caudal (CEFc) cingulate eye field. The CEFr was located rostral to the CMAr, while the CEFc was located rostro-ventral to the CMAc. Cells projecting to the FEF and MI scarcely overlapped, indicating that each area receives different sets of information from the cingulate cortex.

Amidines↗

Participation of the primate presupplementary motor area in sequencing multiple saccades.

The aim of this study was to investigate whether, and how, the presupplementary motor area (pre-SMA) is involved in the organization of oculomotor sequence. We trained two monkeys to perform three center-out saccades in six different orders. Each sequence consisted of a block of eight trials, initially with visual instruction (4 trials) and then from memory (4 trials). During memory-guided performance of sequential saccades, approximately 75% of task-related neuronal activity was selective for, or influenced by, the numerical position of saccades within each sequence (rank order). Neurons tuned for the direction of saccades were in the minority. We also found that 22% of sampled neurons increased their activity preferentially at a transitional period when monkeys were in the process of renewal of required saccade sequences. These data indicate that the pre-SMA is involved in the organization of oculomotor sequence, particularly in representing rank-order information and in updating sequence information. Together with previous reports on the participation of the pre-SMA in sequencing of multiple arm movements, we propose here that this area may contribute to cognitive aspects of sequential behavioral control, in an effector-independent manner.

Animals↗

Area-selective neuronal activity in the dorsolateral prefrontal cortex for information retrieval and action planning.

We compared how neurons in the dorsal and ventral regions of the dorsolateral prefrontal cortex (dl-PFC) participate in processing 2 sets of sensory signals, given at intervals, to generate plans for future actions. For the first set of visual signals, neurons in the ventral region of dl-PFC responded preferentially to the visuospatial properties of the signal, whereas neurons in the dorsal region of dl-PFC were involved primarily in retrieving information from the signal, such as the location of the target or which arm to use. For the second set of visual signals, most ventral dl-PFC neurons reflected either the sensory properties of the signals or the information retrieved from each signal. By contrast, dorsal neurons were involved more in integrating information about the target location and which arm to use to reach the target, thereby generating information that could be used to plan future actions. Thus sensorimotor transformations in the dorsolateral PFC appear to be time-variant and region-selective.

Animals↗

Functional specialization in dorsal and ventral premotor areas.

The premotor cortex (PM) in the bilateral lateral hemisphere of nonhuman primates and the human has been implicated in the sensorial guidance of movements. This is in contrast to more medial motor areas that are involved more in the temporal structuring of movements based on memorized information. The PM is further subdivided into dorsal (PMd) and ventral (PMv) parts. In this chapter, we describe our attempts to find differences in the use of these two areas in a nonhuman primate for programming future motor actions based on visual signals. We show that neurons in the PMv are involved primarily in receiving visuospatial signals and in specifying the spatial location of the target to be reached. In contrast, neurons in the PMd are involved more in integrating information about which arm to use and the target to be reached. Thus, PMd neurons are more implicated than those of the PMv in the preparation for a future motor action.

Afferent Pathways↗

Integration of temporal order and object information in the monkey lateral prefrontal cortex.

Generation of information about the temporal order of events is essential for the control of memory-based behavioral tasks. We studied cellular activity in the lateral prefrontal cortex (LPFC) in two monkeys that were required to remember the temporal order in which visual objects were presented. In this report, we focus on cellular activity in response to the sequential appearance of three different objects. We identified cells that responded selectively to physical properties (color and shape) of objects (23%) in the ventral part of the LPFC and cells for which activity was selective for the numerical position (rank order) of objects (44%) in the dorsal part of the LPFC. We also identified cells for which activity was selective for both the physical properties and rank order of objects (30%). The third type of cells, distributed in the ventral LPFC, seems of importance in integrating the two categories of information, i.e., physical and temporal information about the occurrences of objects to construct sequential order information. Furthermore, we identified a distinct group of cells that exhibited selectivity for the sequence of presentation of the three objects. Our findings suggest that LPFC cells are involved in encoding temporal sequences of events when such information is required for planning forthcoming motor behavior.

Animals↗

Contrasting neuronal activity in the supplementary and frontal eye fields during temporal organization of multiple saccades.

The organization of a series of actions into an appropriate temporal order is of particular importance in the voluntary control of motor behavior. Previous reports have emphasized the importance of medial motor areas for the temporal organization of movements. The aim of this study was to compare the neuronal activity in the supplementary and frontal eye fields (SEF and FEF) during sequential performance of multiple saccades to clarify the role of the two cortical oculomotor areas in the temporal organization of saccades based on memorized information. We analyzed neuronal activity while monkeys performed three saccades to peripheral targets in orders that were instructed and memorized. We found that activity that reflected saccade sequence or the numerical position of a saccade within a sequence (rank) was more prevalent in the SEF, whereas activity reflecting saccade direction was more dominant in the FEF. Furthermore, a sizeable number of SEF neurons exhibited an increase in activity when the animals were required to discard a current sequence and compose a novel sequence. We propose that the SEF is primarily involved in the process of planning, decoding, and updating saccade sequences, whereas the FEF plays a major role in determining the direction of forthcoming saccades.

Animals↗

Representation of the temporal order of visual objects in the primate lateral prefrontal cortex.

Recollecting a past episode involves remembering the temporal order of events. We studied cellular activity in the lateral prefrontal cortex (PFC) of two monkeys that were required to remember the temporal order in which visual objects appeared and to reach for each object in the same order after a delay. Here, we report the cellular activity in the lateral PFC, focusing on the delay period. We found that 43% of the delay-period activity was selective for the sequence in which the visual objects were presented during the cue period. While the majority of cellular activity was selective for multiple sequences, some cells (31%) were selective for only one of six sequences. Our findings show that PFC cells are involved in holding temporal order information when that information is necessary for planning forthcoming motor behavior.

Animals↗