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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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Different modulation of Hold- and Pull-type activities in CFA and RFA neurons.A) Intentional (original) and incidental pull movements in a Go/No-go response task. In Go trials, rats must pull the spout-lever deliberately and quickly in response to the presentation of original Go cue to win a reward (Int. pull; 'intentional pull' as a rewarding response). In No-go trials, the rats must keep holding the spout-lever during an extended hold period [1.0–1.6 s after the presentation of No-go (extension) cue]. After the correct No-go response, the rats were allowed to pull the spout-lever to lick the reward anytime (Inci. pull; 'incidental pull' as a consummatory response). Note that the same amount of reward was delivered in both trial types, but more effortful processing would be required for intentional (original) pull movements in the Go trials. B) Left: averaged lever trajectories (mean ± s.d. traces, aligned with the pull onset) for intentional (pink) and incidental (purple) pull movements in one rat (top) and in all of the 38 sessions (24 rats; bottom). Right: distribution of reaction time for intentional pulls (pink; from Go cue onset to pull onset) and incidental pulls (purple; from reward-pumping noise to pull onset) in one rat (top) and all of the rats (bottom; latency to peak). C) Functional activity aligned with the onset (0 s) of intentional pull in Go trials (1st column from the left), of the No-go cue (2nd) and of incidental pull (3rd) in No-go trials, in RS (top) and FS (bottom) subtypes of the CFA (left) and RFA (right) neurons. The spike activity that was significant in the first column (Int. pull-aligned in Go trials) was normalized across the three columns by the peak amplitude from the first column for the individual neurons, which were sorted by the peak time position in the first column (e.g., CFA-RS neurons 1–181). Below, the activity that was significant only in the No-go trials was normalized and sorted by the peak in the third (Inci. pull-aligned) column (e.g., CFA-RS neurons 1–34). Rectangles indicate time windows for Hold- (a, a', c, c') and Pull-type (b, b', d, d') activities for comparisons between Go and No-go trials. An asterisk indicates Pre-pull-type activity, which was in between the Hold- and Pull-type activities (see Fig. 6C).
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pone-0098662-g005: Different modulation of Hold- and Pull-type activities in CFA and RFA neurons.A) Intentional (original) and incidental pull movements in a Go/No-go response task. In Go trials, rats must pull the spout-lever deliberately and quickly in response to the presentation of original Go cue to win a reward (Int. pull; 'intentional pull' as a rewarding response). In No-go trials, the rats must keep holding the spout-lever during an extended hold period [1.0–1.6 s after the presentation of No-go (extension) cue]. After the correct No-go response, the rats were allowed to pull the spout-lever to lick the reward anytime (Inci. pull; 'incidental pull' as a consummatory response). Note that the same amount of reward was delivered in both trial types, but more effortful processing would be required for intentional (original) pull movements in the Go trials. B) Left: averaged lever trajectories (mean ± s.d. traces, aligned with the pull onset) for intentional (pink) and incidental (purple) pull movements in one rat (top) and in all of the 38 sessions (24 rats; bottom). Right: distribution of reaction time for intentional pulls (pink; from Go cue onset to pull onset) and incidental pulls (purple; from reward-pumping noise to pull onset) in one rat (top) and all of the rats (bottom; latency to peak). C) Functional activity aligned with the onset (0 s) of intentional pull in Go trials (1st column from the left), of the No-go cue (2nd) and of incidental pull (3rd) in No-go trials, in RS (top) and FS (bottom) subtypes of the CFA (left) and RFA (right) neurons. The spike activity that was significant in the first column (Int. pull-aligned in Go trials) was normalized across the three columns by the peak amplitude from the first column for the individual neurons, which were sorted by the peak time position in the first column (e.g., CFA-RS neurons 1–181). Below, the activity that was significant only in the No-go trials was normalized and sorted by the peak in the third (Inci. pull-aligned) column (e.g., CFA-RS neurons 1–34). Rectangles indicate time windows for Hold- (a, a', c, c') and Pull-type (b, b', d, d') activities for comparisons between Go and No-go trials. An asterisk indicates Pre-pull-type activity, which was in between the Hold- and Pull-type activities (see Fig. 6C).

Mentions: Data in the text and figures are expressed as the mean ± s.d. (unless otherwise mentioned) and sample number (n). When applicable, we used appropriate statistical tests: i.e., t-test (for data analyses in Figs. 2A, 3D (see text), 4B, 5B, 6A,B, and 7A,B), paired t-test (Fig. 5B), Kolmogorov-Smirnov (KS) test (Figs. 2C,E, 3B,D-F 4B, 6B, and 7B), two-way ANOVA (Fig. 7C), and F-test for s.d. difference (Fig. 7A,B). See Results for details.


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)

Different modulation of Hold- and Pull-type activities in CFA and RFA neurons.A) Intentional (original) and incidental pull movements in a Go/No-go response task. In Go trials, rats must pull the spout-lever deliberately and quickly in response to the presentation of original Go cue to win a reward (Int. pull; 'intentional pull' as a rewarding response). In No-go trials, the rats must keep holding the spout-lever during an extended hold period [1.0–1.6 s after the presentation of No-go (extension) cue]. After the correct No-go response, the rats were allowed to pull the spout-lever to lick the reward anytime (Inci. pull; 'incidental pull' as a consummatory response). Note that the same amount of reward was delivered in both trial types, but more effortful processing would be required for intentional (original) pull movements in the Go trials. B) Left: averaged lever trajectories (mean ± s.d. traces, aligned with the pull onset) for intentional (pink) and incidental (purple) pull movements in one rat (top) and in all of the 38 sessions (24 rats; bottom). Right: distribution of reaction time for intentional pulls (pink; from Go cue onset to pull onset) and incidental pulls (purple; from reward-pumping noise to pull onset) in one rat (top) and all of the rats (bottom; latency to peak). C) Functional activity aligned with the onset (0 s) of intentional pull in Go trials (1st column from the left), of the No-go cue (2nd) and of incidental pull (3rd) in No-go trials, in RS (top) and FS (bottom) subtypes of the CFA (left) and RFA (right) neurons. The spike activity that was significant in the first column (Int. pull-aligned in Go trials) was normalized across the three columns by the peak amplitude from the first column for the individual neurons, which were sorted by the peak time position in the first column (e.g., CFA-RS neurons 1–181). Below, the activity that was significant only in the No-go trials was normalized and sorted by the peak in the third (Inci. pull-aligned) column (e.g., CFA-RS neurons 1–34). Rectangles indicate time windows for Hold- (a, a', c, c') and Pull-type (b, b', d, d') activities for comparisons between Go and No-go trials. An asterisk indicates Pre-pull-type activity, which was in between the Hold- and Pull-type activities (see Fig. 6C).
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Related In: Results  -  Collection

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pone-0098662-g005: Different modulation of Hold- and Pull-type activities in CFA and RFA neurons.A) Intentional (original) and incidental pull movements in a Go/No-go response task. In Go trials, rats must pull the spout-lever deliberately and quickly in response to the presentation of original Go cue to win a reward (Int. pull; 'intentional pull' as a rewarding response). In No-go trials, the rats must keep holding the spout-lever during an extended hold period [1.0–1.6 s after the presentation of No-go (extension) cue]. After the correct No-go response, the rats were allowed to pull the spout-lever to lick the reward anytime (Inci. pull; 'incidental pull' as a consummatory response). Note that the same amount of reward was delivered in both trial types, but more effortful processing would be required for intentional (original) pull movements in the Go trials. B) Left: averaged lever trajectories (mean ± s.d. traces, aligned with the pull onset) for intentional (pink) and incidental (purple) pull movements in one rat (top) and in all of the 38 sessions (24 rats; bottom). Right: distribution of reaction time for intentional pulls (pink; from Go cue onset to pull onset) and incidental pulls (purple; from reward-pumping noise to pull onset) in one rat (top) and all of the rats (bottom; latency to peak). C) Functional activity aligned with the onset (0 s) of intentional pull in Go trials (1st column from the left), of the No-go cue (2nd) and of incidental pull (3rd) in No-go trials, in RS (top) and FS (bottom) subtypes of the CFA (left) and RFA (right) neurons. The spike activity that was significant in the first column (Int. pull-aligned in Go trials) was normalized across the three columns by the peak amplitude from the first column for the individual neurons, which were sorted by the peak time position in the first column (e.g., CFA-RS neurons 1–181). Below, the activity that was significant only in the No-go trials was normalized and sorted by the peak in the third (Inci. pull-aligned) column (e.g., CFA-RS neurons 1–34). Rectangles indicate time windows for Hold- (a, a', c, c') and Pull-type (b, b', d, d') activities for comparisons between Go and No-go trials. An asterisk indicates Pre-pull-type activity, which was in between the Hold- and Pull-type activities (see Fig. 6C).
Mentions: Data in the text and figures are expressed as the mean ± s.d. (unless otherwise mentioned) and sample number (n). When applicable, we used appropriate statistical tests: i.e., t-test (for data analyses in Figs. 2A, 3D (see text), 4B, 5B, 6A,B, and 7A,B), paired t-test (Fig. 5B), Kolmogorov-Smirnov (KS) test (Figs. 2C,E, 3B,D-F 4B, 6B, and 7B), two-way ANOVA (Fig. 7C), and F-test for s.d. difference (Fig. 7A,B). See Results for details.

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