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Different modulation of common motor information in rat primary and secondary motor cortices.

Saiki A, Kimura R, Samura T, Fujiwara-Tsukamoto Y, Sakai Y, Isomura Y - PLoS ONE (2014)

Bottom Line: We found virtually no major differences between CFA and RFA neurons, regardless of neuron subtypes, not only in their basal spiking properties but also in the time-course, amplitude, and direction preference of their functional activation for simple forelimb movements.However, the RFA neurons, as compared with the CFA neurons, showed obviously a greater susceptibility of their functional activation to an alteration in a behavioral situation, a 'rewarding' response that leads to reward or a 'consummatory' response that follows reward water, which might be accompanied by some internal adaptations without affecting the motor outputs.Our results suggest that, although the CFA and RFA neurons commonly process fundamental motor information to properly control forelimb movements, the RFA neurons may be functionally differentiated to integrate motor information with internal state information for an adaptation to goal-directed behaviors.

View Article: PubMed Central - PubMed

Affiliation: Brain Science Institute, Tamagawa University, Machida, Tokyo, Japan; Graduate School of Brain Sciences, Tamagawa University, Machida, Tokyo, Japan; JST CREST, Chiyoda-ku, Tokyo, Japan.

ABSTRACT
Rodents have primary and secondary motor cortices that are involved in the execution of voluntary movements via their direct and parallel projections to the spinal cord. However, it is unclear whether the rodent secondary motor cortex has any motor function distinct from the primary motor cortex to properly control voluntary movements. In the present study, we quantitatively examined neuronal activity in the caudal forelimb area (CFA) of the primary motor cortex and rostral forelimb area (RFA) of the secondary motor cortex in head-fixed rats performing forelimb movements (pushing, holding, and pulling a lever). We found virtually no major differences between CFA and RFA neurons, regardless of neuron subtypes, not only in their basal spiking properties but also in the time-course, amplitude, and direction preference of their functional activation for simple forelimb movements. However, the RFA neurons, as compared with the CFA neurons, showed obviously a greater susceptibility of their functional activation to an alteration in a behavioral situation, a 'rewarding' response that leads to reward or a 'consummatory' response that follows reward water, which might be accompanied by some internal adaptations without affecting the motor outputs. Our results suggest that, although the CFA and RFA neurons commonly process fundamental motor information to properly control forelimb movements, the RFA neurons may be functionally differentiated to integrate motor information with internal state information for an adaptation to goal-directed behaviors.

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A hypothetical model.Our schematic model of different motor functions of the primary and secondary motor cortices (M1 and M2) in voluntary movement control. See Discussion for details.
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pone-0098662-g008: A hypothetical model.Our schematic model of different motor functions of the primary and secondary motor cortices (M1 and M2) in voluntary movement control. See Discussion for details.

Mentions: Even if CFA and RFA neurons share fundamental motor functions, it is still possible that they play different roles in motor control with major changes in behavioral situation. A large change in behavioral situation would lead to some adaptive changes in internal brain state such as attention, motivation, emotion, and so on. In the second experiments, therefore, we examined whether CFA and RFA neurons differentially encode motor information for similar forelimb movements in two distinct behavioral situations in the Go/No-go response task (Fig. 5A) [40]. In Go trials, rats had to pull the spout-lever as quickly as possible in response to the Go cue presentation for reward acquisition ('intentional pull', a rewarding response); they should conduct auditory cue discrimination and make a decision for the goal-directed action. In No-go trials, they were allowed to pull the lever at will to lick the already-earned reward ('incidental pull', a consummatory response) after a completion of correct No-go response; they should need neither cue discrimination nor decision-making for this action. Operating noise of the micropump for reward delivery (reward-pumping noise) after a correct No-go response could work as another Go signal to allow an incidental pull. The reaction time of intentional pulls (from Go cue onset to pull onset; Fig. 5B, 159.7±47.6 ms) was significantly longer than that of incidental pulls (from reward-pumping noise to pull onset; 129.3±22.1 ms, t-test p<0.002), suggesting that intentional pulls may require more effortful processing for cue discrimination and decision-making for the goal-directed action, whereas incidental pulls may not require it, but may be facilitated by an attention or motivation to the earned reward. Thus, the behavioral situations were certainly different between the two trial types. In contrast, the rats performed similar pull movements in both trial-types of the Go/No-go response task (Fig. 5B; an example rat: intentional pulls 41.6±3.7% of full shift at 150 ms after the pull onset, n = 717 trials; incidental pulls 41.7±3.9%, n = 824 trials; paired t-test p>0.6; group analysis: intentional 40.2±12.2%, incidental 39.3±10.7% at 150 ms after the pull onset; N = 38 sessions from 24 rats; paired t-test p>0.4; see also EMG activity in Fig. 8C of our previous report [40]).


Different modulation of common motor information in rat primary and secondary motor cortices.

Saiki A, Kimura R, Samura T, Fujiwara-Tsukamoto Y, Sakai Y, Isomura Y - PLoS ONE (2014)

A hypothetical model.Our schematic model of different motor functions of the primary and secondary motor cortices (M1 and M2) in voluntary movement control. See Discussion for details.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4043846&req=5

pone-0098662-g008: A hypothetical model.Our schematic model of different motor functions of the primary and secondary motor cortices (M1 and M2) in voluntary movement control. See Discussion for details.
Mentions: Even if CFA and RFA neurons share fundamental motor functions, it is still possible that they play different roles in motor control with major changes in behavioral situation. A large change in behavioral situation would lead to some adaptive changes in internal brain state such as attention, motivation, emotion, and so on. In the second experiments, therefore, we examined whether CFA and RFA neurons differentially encode motor information for similar forelimb movements in two distinct behavioral situations in the Go/No-go response task (Fig. 5A) [40]. In Go trials, rats had to pull the spout-lever as quickly as possible in response to the Go cue presentation for reward acquisition ('intentional pull', a rewarding response); they should conduct auditory cue discrimination and make a decision for the goal-directed action. In No-go trials, they were allowed to pull the lever at will to lick the already-earned reward ('incidental pull', a consummatory response) after a completion of correct No-go response; they should need neither cue discrimination nor decision-making for this action. Operating noise of the micropump for reward delivery (reward-pumping noise) after a correct No-go response could work as another Go signal to allow an incidental pull. The reaction time of intentional pulls (from Go cue onset to pull onset; Fig. 5B, 159.7±47.6 ms) was significantly longer than that of incidental pulls (from reward-pumping noise to pull onset; 129.3±22.1 ms, t-test p<0.002), suggesting that intentional pulls may require more effortful processing for cue discrimination and decision-making for the goal-directed action, whereas incidental pulls may not require it, but may be facilitated by an attention or motivation to the earned reward. Thus, the behavioral situations were certainly different between the two trial types. In contrast, the rats performed similar pull movements in both trial-types of the Go/No-go response task (Fig. 5B; an example rat: intentional pulls 41.6±3.7% of full shift at 150 ms after the pull onset, n = 717 trials; incidental pulls 41.7±3.9%, n = 824 trials; paired t-test p>0.6; group analysis: intentional 40.2±12.2%, incidental 39.3±10.7% at 150 ms after the pull onset; N = 38 sessions from 24 rats; paired t-test p>0.4; see also EMG activity in Fig. 8C of our previous report [40]).

Bottom Line: We found virtually no major differences between CFA and RFA neurons, regardless of neuron subtypes, not only in their basal spiking properties but also in the time-course, amplitude, and direction preference of their functional activation for simple forelimb movements.However, the RFA neurons, as compared with the CFA neurons, showed obviously a greater susceptibility of their functional activation to an alteration in a behavioral situation, a 'rewarding' response that leads to reward or a 'consummatory' response that follows reward water, which might be accompanied by some internal adaptations without affecting the motor outputs.Our results suggest that, although the CFA and RFA neurons commonly process fundamental motor information to properly control forelimb movements, the RFA neurons may be functionally differentiated to integrate motor information with internal state information for an adaptation to goal-directed behaviors.

View Article: PubMed Central - PubMed

Affiliation: Brain Science Institute, Tamagawa University, Machida, Tokyo, Japan; Graduate School of Brain Sciences, Tamagawa University, Machida, Tokyo, Japan; JST CREST, Chiyoda-ku, Tokyo, Japan.

ABSTRACT
Rodents have primary and secondary motor cortices that are involved in the execution of voluntary movements via their direct and parallel projections to the spinal cord. However, it is unclear whether the rodent secondary motor cortex has any motor function distinct from the primary motor cortex to properly control voluntary movements. In the present study, we quantitatively examined neuronal activity in the caudal forelimb area (CFA) of the primary motor cortex and rostral forelimb area (RFA) of the secondary motor cortex in head-fixed rats performing forelimb movements (pushing, holding, and pulling a lever). We found virtually no major differences between CFA and RFA neurons, regardless of neuron subtypes, not only in their basal spiking properties but also in the time-course, amplitude, and direction preference of their functional activation for simple forelimb movements. However, the RFA neurons, as compared with the CFA neurons, showed obviously a greater susceptibility of their functional activation to an alteration in a behavioral situation, a 'rewarding' response that leads to reward or a 'consummatory' response that follows reward water, which might be accompanied by some internal adaptations without affecting the motor outputs. Our results suggest that, although the CFA and RFA neurons commonly process fundamental motor information to properly control forelimb movements, the RFA neurons may be functionally differentiated to integrate motor information with internal state information for an adaptation to goal-directed behaviors.

Show MeSH