Toshi Nakajima

Covert representation of second-next movement in the pre-supplementary motor area of monkeys.

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.

The Suppression of Beta Oscillations in the Primate Supplementary Motor Complex Reflects a Volatile State During the Updating of Action Sequences

The medial motor areas play crucial but flexible roles in the temporal organizations of multiple movements. The beta oscillation of local field potentials is the predominant oscillatory activity in the motor areas, but the manner in which increases and decreases in beta power contribute to updating of multiple action plans is not yet fully understood. In the present study, beta and high-gamma activities in the supplementary motor area (SMA) and pre-SMA of monkeys were analyzed during performance of a bimanual motor sequence task that required updating and maintenance of the memory of action sequences. Beta power was attenuated during early delay periods of updating trials but was increased during maintenance trials, while there was a reciprocal increase in high-gamma power during updating trials. Moreover, transient attenuation of beta power during maintenance trials resulted in the erroneous selection of an action sequence. Therefore, it was concluded that the suppression of beta power during the early delay period reflects volatility of neural representation of the action sequence. This neural representation would be properly updated to the appropriate instructed action sequence via increases in high-gamma power in updating trials whereas it would be erroneously updated without the appropriate updating signal in maintenance trials.

Two-Dimensional Representation of Action and Arm-Use Sequences in the Presupplementary and Supplementary Motor Areas

The medial frontal cortex has been thought to be crucially involved in temporal structuring of behavior in monkeys and humans. We examined neuronal activity in the supplementary and presupplementary motor areas of monkeys to investigate how the nervous system deals with the coding of 16 motor sequences resulting from multiple actions involving bilateral use of the arms. We first found in both areas that this behavioral demand resulted in attribute-based representation of individual motor acts, reflecting functional (action) or anatomical (right/left arm) attributes. Actions were frequently represented according to a body-axis-centered reference frame (supination or pronation) regardless of the arm to be used. Moreover, behavioral sequences were primarily represented with respect to the action- or arm-use sequence rather than the sequence of individual movements. We propose that the two-dimensional attribute-based sequence representation provides a robust and efficient means of processing multiple behavioral sequences.

Neuronal Activity in the Prefrontal Cortex During Performance of a Dual Task Consisting of a Main- and An Interrupting-Task

To investigate the neuronal mechanism of multi-tasking, we recorded neuronal activity in the prefrontal cortex (PFC) and the dorsal premotor cortex (PMd) while monkeys performed a dual task consisting of a main-task and an interruption. We found PFC neurons responded selectively to either the interruption or resumption to the main-task. PMd neurons showed sustained activity related to preparation for the main-task. Accordingly, we hypothesized a model in which the PFC controls a dual task by providing biasing signals to downstream systems.

Arm-use dependent lateralization of gamma and beta oscillations in primate medial motor areas

The neurons in the motor cortex show lateralization depending on the arm to use. To investigate if local field potential (LFP) oscillations change with contralateral and ipsilateral arm use, we analyzed the power of LFP in supplementary motor areas (SMA) and pre-SMA while animals performed a delayed-response arm use task under visual guidance and memory-based. LFP power changed with the laterality of the arm use, but it was frequency dependent. Specifically, power in the gamma range increased during contralateral arm use, while beta power increased with ipsilateral arm use. Subsequently, we confirmed that the frequency-dependent laterality was true also for the memory-driven movements. Our data therefore suggest that gamma oscillation is linked to the local neuronal activities in the contralateral hemisphere, and beta oscillation is related to withholding undesired arm movements by suppression of the local neuronal activities of the ipsilateral hemisphere.

Intended arm use influences interhemispheric correlation of β-oscillations in primate medial motor areas

To investigate the role of interhemispheric β-synchronization in the selection of motor effectors, we trained two monkeys to memorize and perform multiple two-movement sequences that included unimanual repetition and bimanual switching. We recorded local field potentials simultaneously in the bilateral supplementary motor area (SMA) and pre-SMA to examine how the β-power in both hemispheres and the interhemispheric relationship of β-oscillations depend on the prepared sequence of arm use. We found a significant ipsilateral enhancement of β-power for bimanual switching trials in the left hemisphere and an enhancement of β-power in the right SMA while preparing for unimanual repetition. Furthermore, interhemispheric synchrony in the SMA was significantly more enhanced while preparing unimanual repetition than while preparing bimanual switching. This enhancement of synchrony was detected in terms of β-phase but not in terms of modulation of β-power. Furthermore, the assessment of the interhemispheric phase difference revealed that the β-oscillation in the hemisphere contralateral to the instructed arm use significantly advanced its phase relative to that in the ipsilateral hemisphere. There was no arm use-dependent shift in phase difference in the pairwise recordings within each hemisphere. Both neurons with and without arm use-selective activity were phase-locked to the β-oscillation. These results imply that the degree of interhemispheric phase synchronization as well as phase differences and oscillatory power in the β-band may contribute to the selection of arm use depending on the behavioral conditions of sequential arm use.NEW & NOTEWORTHY We addressed interhemispheric relationships of β-oscillations during bimanual coordination. While monkeys prepared to initiate movement of the instructed arm, β-oscillations in the contralateral hemisphere showed a phase advance relative to the other hemisphere. Furthermore, the sequence of arm use influenced β-power and the degree of interhemispheric phase synchronization. Thus the dynamics of interhemispheric phases and power in β-oscillations may contribute to the specification of motor effectors in a given behavioral context.

The effect of interrupting a memory-guided sequential motor task on neuronal activity in the dorsal premotor area

Common marmosets (Callithrix jacchus) have been used in biomedical research because of their high fertility, biosafety, ease of handling, and low cost of breeding when compared to other non-human primates. Recently, common marmosets have attracted a great deal of attention from researchers as experimental primates to investigate cognitive and social behavior. In addition, the recent success in the generation of transgenic marmosets with germline transmission has made common marmosets as highly important experimental primate models for human mental and nervous diseases, such as Alzheimer’s and Parkinson’s diseases. Although the working memory function is one of the most important brain functions to assess symptoms of patients with mental and nervous disease, there are, so far, no convenient ways to assess the working memory function in common marmosets. Therefore, we trained marmosets in a visual delayed matching-to-sample task, which has been widely used to assess the working memory function in monkeys as well as human patients. In the delayed matching-to-sample task, a warning signal was presented on a monitor. After the marmoset touched the warning signal, the warning signal was disappeared and then a sample stimulus was presented. After touching the sample stimulus, the stimulus was disappeared and a delay period followed. Then, a new stimulus and the sample stimulus were simultaneously presented on the monitor. The marmoset was required to touch the sample stimulus to get a reward. If the percent correct exceeded 80% in each of the five consecutive sessions under a 0.5sec delay condition, we regarded that the marmoset successfully learned the task. Five out of eight marmosets learned the delayed matching-to-sample task. We examined the performance of the five marmosets with 0.5-, 2.0-, 4.0-, 8.0-, and 16.0-sec delays. Here we will compare their working memory function with those of other animals previously reported. Research fund: the Strategic Research Program for Brain Sciences from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Laterality of Gamma-Oscillations in Primate Supplementary Motor Area During Performance of Visually-Guided Movements

The neurons in the motor cortex show lateralization depending on the arm to use. To investigate if local field potential (LFP) oscillations change with contralateral and ipsilateral arm use, we analyzed the power of LFP in supplementary motor areas (SMA) and pre-SMA while animals performed a delayed-response arm use task. LFP power changed with the laterality of the arm use, but that it was frequency dependent. Specifically, power in the gamma range increased during contralateral arm use, while beta power increased with ipsilateral arm use. Our data therefore suggest that lateralized movement is executed by gamma oscillations and unit activities in the contralateral hemisphere, and is modulated by beta frequency activities in the ipsilateral hemisphere.

Cue-Dependent Modulation of Synchrony in Primates’ Medial Motor Areas

Although β oscillations are the representative brain activity in sensorimotor areas and the basal ganglia, how they coordinate activities of multiple structures in the brain is poorly understood. To examine the coordination of the activities of the pre-supplementary motor area (pre-SMA) and the SMA through β oscillations, we recorded local field potentials simultaneously in these areas while monkeys performed a motor task. Examination of inter-area phase difference revealed that the pre-SMA became phase-advanced in β oscillations relative to the SMA when a visual cue signaled initiation of a trial. The strength of phase synchrony decreased markedly while the monkeys were visually instructed about the movement to be performed and was strengthened when the monkeys repeated the movements they had performed in the previous trial. These results suggest that visual input initializes the dynamic state of the pre-SMA and SMA when a trial starts. Additionally, sensory signals seem to be acquired and motor plans formed via modulation of the strength of inter-area synchrony of β oscillations.

Neuronal activity related to switching of arm use and action during performance of a bimanual sequential motor task

P2-g12 Multisynaptic inputs from the basal ganglia (BG) to rostrocaudally distinct sectors of the dorsal premotor cortex (PMd) in macaques Eiji Hoshi 1 , Yosuke Saga 1, Daisuke Takahara 2,3,4, Yoshihiro Hirata 2,3, Kenichi Inoue 2,3, Shigehiro Miyachi 5, Atsushi Nambu 4, Jun Tanji 1, Masahiko Takada 2,3 1 Tamagawa Univ Brain Sci Inst 2 Dept System Neurosci, Tokyo Metropolitan Inst for Neurosci 3 Systems Neurosci Sect, Primate Res Inst, Kyoto Univ 4 Div System Neurophysiol, National Inst for Physiological Sci 5 Cognitive Neurosci Sect, Primate Res Inst, Kyoto Univ