Differential Roles of Neuronal Activity in the Supplementary and Presupplementary Motor Areas: From Information Retrieval to Motor Planning and Execution

2004 ◽  
Vol 92 (6) ◽  
pp. 3482-3499 ◽  
Author(s):  
Eiji Hoshi ◽  
Jun Tanji

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.

2006 ◽  
Vol 95 (6) ◽  
pp. 3596-3616 ◽  
Author(s):  
Eiji Hoshi ◽  
Jun Tanji

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.


1998 ◽  
Vol 80 (6) ◽  
pp. 3247-3260 ◽  
Author(s):  
Keisetsu Shima ◽  
Jun Tanji

Shima, Keisetsu and Jun Tanji. Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J. Neurophysiol. 80: 3247–3260, 1998. To study the involvement of the supplementary (SMA) and presupplementary (pre-SMA) motor areas in performing sequential multiple movements that are individually separated in time, we injected muscimol, a γ-aminobutyric acid agonist, bilaterally into the part of each area that represents the forelimb. Two monkeys were trained to perform three different movements, separated by a waiting time, in four or six different orders. First, each series of movements was learned during five trials guided by visual signals that indicated the correct movements. The monkeys subsequently executed the three movements in the memorized order, without the visual signals. After the injection of muscimol (3 μl, 5 μg/μl in 10 min) into either the SMA or pre-SMA bilaterally, the animals started making errors in performing the sequence of movements correctly from memory. However, when guided with a visual signal, they could select and perform the three movements correctly. The impaired memory-based sequencing of movements worsened progressively with time until the animals could not perform the task. Yet they still could associate the visual signals with the different movements at that stage. In control experiments on two separate monkeys, we found that injections of the same amount of muscimol into either the SMA or pre-SMA did not cause problems with nonsequential reaching movement regardless of whether it was visually triggered or self-initiated. These results support the view that both the SMA and pre-SMA are crucially involved in sequencing multiple movements over time.


2000 ◽  
Vol 84 (4) ◽  
pp. 2148-2160 ◽  
Author(s):  
Keisetsu Shima ◽  
Jun Tanji

To study how neurons in the medial motor areas participate in performing sequential multiple movements that are individually separated in time, we analyzed neuronal activity in the supplementary (SMA) and presupplementary (pre-SMA) motor areas. Monkeys were trained to perform three different movements separated by waiting times, in four or six different orders. Initially each series of movements was learned during five trials guided by visual signals that indicated the correct movements. The monkeys subsequently executed the three movements in the memorized order without the visual signals. Three types of neuronal activity were of particular interest; these appeared to be crucially involved in sequencing the multiple motor tasks in different orders. First, we found activity changes that were selective for a particular sequence of the three movements that the monkeys were prepared to perform. The sequence-selective activity ceased when the monkeys initiated the first movement. Second, we found interval-selective activity that appeared in the interval between one particular movement and the next. Third, we found neuronal activity representing the rank order of three movements arranged chronologically; that is, the activity differed selectively in the process of preparing the first, second, or third movements in individual trials. The interval-selective activity was more prevalent in the SMA, whereas the rank-order selective activity was more frequently recorded in the pre-SMA. These results suggest how neurons in the SMA and pre-SMA are involved in sequencing multiple movements over time.


2005 ◽  
Vol 94 (1) ◽  
pp. 640-656 ◽  
Author(s):  
Eiji Hoshi ◽  
Hiromasa Sawamura ◽  
Jun Tanji

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.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Atsushi Chiba ◽  
Kazunori Morita ◽  
Ken-ichi Oshio ◽  
Masahiko Inase

AbstractTo investigate neuronal processing involved in the integration of auditory and visual signals for time perception, we examined neuronal activity in prefrontal cortex (PFC) of macaque monkeys during a duration discrimination task with auditory and visual cues. In the task, two cues were consecutively presented for different durations between 0.2 and 1.8 s. Each cue was either auditory or visual and was followed by a delay period. After the second delay, subjects indicated whether the first or the second cue was longer. Cue- and delay-responsive neurons were found in PFC. Cue-responsive neurons mostly responded to either the auditory or the visual cue, and to either the first or the second cue. The neurons responsive to the first delay showed activity that changed depending on the first cue duration and were mostly sensitive to cue modality. The neurons responsive to the second delay exhibited activity that represented which cue, the first or second cue, was presented longer. Nearly half of this activity representing order-based duration was sensitive to cue modality. These results suggest that temporal information with visual and auditory signals was separately processed in PFC in the early stage of duration discrimination and integrated for the final decision.


2009 ◽  
Vol 101 (4) ◽  
pp. 1883-1889 ◽  
Author(s):  
Toshi Nakajima ◽  
Ryosuke Hosaka ◽  
Hajime Mushiake ◽  
Jun Tanji

We attempted to analyze the nature of premovement activity of neurons in medial motor areas [supplementary motor area (SMA) and pre-SMA] from a perspective of coding multiple movements. Monkeys were trained to perform a series of two movements with an intervening delay: supination or pronation with either forearm. Movements were initially instructed with visual signals but had to be remembered thereafter. Although a well-known type of premovement activity representing the forthcoming movements was found in the two areas, we found an unexpected type of activity that represented a second-next movement before initiating the first of the two movements. Typically in the pre-SMA, such activity selective for the second-next movement peaked before the initiation of the first movement, decayed thereafter, and remained low in magnitude while initiating the second movement. This type of activity may tentatively hold information for the second movement while initiating the first. That information may be fed into another group of neurons that themselves build a preparatory activity required to plan the second movements. Alternatively, the activity could serve as a signal to inhibit a premature exertion of the motor command for the second movement.


2014 ◽  
Vol 281 (1785) ◽  
pp. 20133201 ◽  
Author(s):  
Federico Rossano ◽  
Marie Nitzschner ◽  
Michael Tomasello

Domestic dogs are particularly skilled at using human visual signals to locate hidden food. This is, to our knowledge, the first series of studies that investigates the ability of dogs to use only auditory communicative acts to locate hidden food. In a first study, from behind a barrier, a human expressed excitement towards a baited box on either the right or left side, while sitting closer to the unbaited box. Dogs were successful in following the human's voice direction and locating the food. In the two following control studies, we excluded the possibility that dogs could locate the box containing food just by relying on smell, and we showed that they would interpret a human's voice direction in a referential manner only when they could locate a possible referent (i.e. one of the boxes) in the environment. Finally, in a fourth study, we tested 8–14-week-old puppies in the main experimental test and found that those with a reasonable amount of human experience performed overall even better than the adult dogs. These results suggest that domestic dogs’ skills in comprehending human communication are not based on visual cues alone, but are instead multi-modal and highly flexible. Moreover, the similarity between young and adult dogs’ performances has important implications for the domestication hypothesis.


2020 ◽  
Vol 123 (5) ◽  
pp. 1727-1738 ◽  
Author(s):  
Giacomo Ariani ◽  
Young Han Kwon ◽  
Jörn Diedrichsen

Even for overlearned motor skills such as reaching, movement repetition improves performance. How brain processes associated with motor planning or execution benefit from repetition, however, remains unclear. We report the novel finding of repetition effects for sequential movements. Our results show that repetition benefits are tied to improved online planning of upcoming sequence elements. We also highlight how actual movement experience appears to be more beneficial than mental rehearsal for observing short-term repetition effects.


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