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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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Large reduction in Hold-type activity by an extension of the hold period in RFA-RS neurons.A) Populational changes in normalized spike rate in the Hold-type groups (significant in Go trials) of CFA-RS (orange) and RFA-RS (green) neurons [mean ± s.e.m. traces, aligned with the onset (0 s) of intentional pull in Go trials (left), No-go cue (middle), and incidental pull (right) in No-go trials]. Horizontal bars (a and a') correspond to the time windows shown in Fig. 5C. Note that the Hold-type activity of RFA-RS was lower than that of CFA-RS neurons in the No-go trials (a'), and also that no change was observed in response to the No-go cue presentation. B) Left: averaged spike rates of Hold-type activity (significant in Go trials) before intentional pull (SRGo HOLD, corresponding to Fig. 5C, a) and before incidental pull (SRNo-go HOLD, corresponding to a') for individual CFA-RS (orange, filled triangles) and RFA-RS neurons (green). Open triangles represent those with statistical significance only in No-go trials (corresponding to Fig. 5C, c' and c). Right: cumulative probability analysis of the distribution of normalized spike rates during an extended hold period in No-go trials (a') in CFA-RS and RFA-RS neurons. There was a larger reduction in the Hold-type activity in RFA-RS neurons in the extended period than that in CFA-RS neurons. C) Populational changes in normalized spike rate in Pre-pull-type groups of CFA-RS (orange; as indicated by an asterisk in Fig. 5C) and RFA-RS (green) neurons [mean ± s.e.m. traces, aligned with the onset (0 s) of Go or No-go cue (left, for Go and No-go trials, respectively) and incidental pull (right, for No-go trials)]. A horizontal bar indicates a range of intentional pulls. These types of neurons abruptly stopped a gradually increasing spike activity just prior to intentional/incidental pull movements.
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pone-0098662-g006: Large reduction in Hold-type activity by an extension of the hold period in RFA-RS neurons.A) Populational changes in normalized spike rate in the Hold-type groups (significant in Go trials) of CFA-RS (orange) and RFA-RS (green) neurons [mean ± s.e.m. traces, aligned with the onset (0 s) of intentional pull in Go trials (left), No-go cue (middle), and incidental pull (right) in No-go trials]. Horizontal bars (a and a') correspond to the time windows shown in Fig. 5C. Note that the Hold-type activity of RFA-RS was lower than that of CFA-RS neurons in the No-go trials (a'), and also that no change was observed in response to the No-go cue presentation. B) Left: averaged spike rates of Hold-type activity (significant in Go trials) before intentional pull (SRGo HOLD, corresponding to Fig. 5C, a) and before incidental pull (SRNo-go HOLD, corresponding to a') for individual CFA-RS (orange, filled triangles) and RFA-RS neurons (green). Open triangles represent those with statistical significance only in No-go trials (corresponding to Fig. 5C, c' and c). Right: cumulative probability analysis of the distribution of normalized spike rates during an extended hold period in No-go trials (a') in CFA-RS and RFA-RS neurons. There was a larger reduction in the Hold-type activity in RFA-RS neurons in the extended period than that in CFA-RS neurons. C) Populational changes in normalized spike rate in Pre-pull-type groups of CFA-RS (orange; as indicated by an asterisk in Fig. 5C) and RFA-RS (green) neurons [mean ± s.e.m. traces, aligned with the onset (0 s) of Go or No-go cue (left, for Go and No-go trials, respectively) and incidental pull (right, for No-go trials)]. A horizontal bar indicates a range of intentional pulls. These types of neurons abruptly stopped a gradually increasing spike activity just prior to intentional/incidental pull movements.

Mentions: We obtained a number of task-related CFA and RFA neurons from the 24 rats performing the Go/No-go response task (Fig. 5C; CFA-RS n = 215, RFA-RS n = 207, CFA-FS n = 47, RFA-FS n = 17). In this task situation, the No-go cue worked as an extension cue to indicate that lever hold should be extended until the reward was delivered. We failed to find any No-go-cue-specific activity in the RS and FS subtypes of the CFA and RFA (Figs. 5C, 6A, and 7A). In addition, we found no auditory response to the reward-pumping noise in Go or No-go trials (data not shown). Accordingly, these motor cortices seem to have no sensory (auditory) or cognitive function to process the Go/No-go signals in our experimental condition. We, therefore, focused on fundamental motor functions, especially the Hold- and Pull-type activities in RS neurons, with regard to the intentional and incidental pull movements. When the lever hold was extended in No-go trials, the Hold-type activity was prolonged until the incidental pull occurred (Figs. 5C and 6A). The prolonged Hold-type activity (a') was more significantly reduced in the RFA-RS neurons than in the CFA-RS neurons [Fig. 6A, right; normalized spike rate in the time window a': CFA-RS 99.7±33.2%, n = 43; RFA-RS 79.8±29.9%, n = 37; t-test p<0.005; and similarly, Fig. 6B, right, KS test p<0.03; Fig. 6B, left, SRNo-go HOLD − SRGo HOLD (including neurons with significant activity only in No-go trials): CFA-RS −0.00±0.16 in Δlog(spike rate); RFA-RS −0.09±0.19; t-test p<0.02]. Besides the Hold-type activity, Pre-pull-type activity (e.g., Fig. 5C, asterisk) showed a gradual increase in spike rate until just before the pull onset, regardless of the different behavioral situations (Fig. 6C; CFA-RS n = 16, RFA-RS n = 7), suggesting that Pre-pull-type activity is associated with motor preparation or initiation.


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)

Large reduction in Hold-type activity by an extension of the hold period in RFA-RS neurons.A) Populational changes in normalized spike rate in the Hold-type groups (significant in Go trials) of CFA-RS (orange) and RFA-RS (green) neurons [mean ± s.e.m. traces, aligned with the onset (0 s) of intentional pull in Go trials (left), No-go cue (middle), and incidental pull (right) in No-go trials]. Horizontal bars (a and a') correspond to the time windows shown in Fig. 5C. Note that the Hold-type activity of RFA-RS was lower than that of CFA-RS neurons in the No-go trials (a'), and also that no change was observed in response to the No-go cue presentation. B) Left: averaged spike rates of Hold-type activity (significant in Go trials) before intentional pull (SRGo HOLD, corresponding to Fig. 5C, a) and before incidental pull (SRNo-go HOLD, corresponding to a') for individual CFA-RS (orange, filled triangles) and RFA-RS neurons (green). Open triangles represent those with statistical significance only in No-go trials (corresponding to Fig. 5C, c' and c). Right: cumulative probability analysis of the distribution of normalized spike rates during an extended hold period in No-go trials (a') in CFA-RS and RFA-RS neurons. There was a larger reduction in the Hold-type activity in RFA-RS neurons in the extended period than that in CFA-RS neurons. C) Populational changes in normalized spike rate in Pre-pull-type groups of CFA-RS (orange; as indicated by an asterisk in Fig. 5C) and RFA-RS (green) neurons [mean ± s.e.m. traces, aligned with the onset (0 s) of Go or No-go cue (left, for Go and No-go trials, respectively) and incidental pull (right, for No-go trials)]. A horizontal bar indicates a range of intentional pulls. These types of neurons abruptly stopped a gradually increasing spike activity just prior to intentional/incidental pull movements.
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Related In: Results  -  Collection

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

pone-0098662-g006: Large reduction in Hold-type activity by an extension of the hold period in RFA-RS neurons.A) Populational changes in normalized spike rate in the Hold-type groups (significant in Go trials) of CFA-RS (orange) and RFA-RS (green) neurons [mean ± s.e.m. traces, aligned with the onset (0 s) of intentional pull in Go trials (left), No-go cue (middle), and incidental pull (right) in No-go trials]. Horizontal bars (a and a') correspond to the time windows shown in Fig. 5C. Note that the Hold-type activity of RFA-RS was lower than that of CFA-RS neurons in the No-go trials (a'), and also that no change was observed in response to the No-go cue presentation. B) Left: averaged spike rates of Hold-type activity (significant in Go trials) before intentional pull (SRGo HOLD, corresponding to Fig. 5C, a) and before incidental pull (SRNo-go HOLD, corresponding to a') for individual CFA-RS (orange, filled triangles) and RFA-RS neurons (green). Open triangles represent those with statistical significance only in No-go trials (corresponding to Fig. 5C, c' and c). Right: cumulative probability analysis of the distribution of normalized spike rates during an extended hold period in No-go trials (a') in CFA-RS and RFA-RS neurons. There was a larger reduction in the Hold-type activity in RFA-RS neurons in the extended period than that in CFA-RS neurons. C) Populational changes in normalized spike rate in Pre-pull-type groups of CFA-RS (orange; as indicated by an asterisk in Fig. 5C) and RFA-RS (green) neurons [mean ± s.e.m. traces, aligned with the onset (0 s) of Go or No-go cue (left, for Go and No-go trials, respectively) and incidental pull (right, for No-go trials)]. A horizontal bar indicates a range of intentional pulls. These types of neurons abruptly stopped a gradually increasing spike activity just prior to intentional/incidental pull movements.
Mentions: We obtained a number of task-related CFA and RFA neurons from the 24 rats performing the Go/No-go response task (Fig. 5C; CFA-RS n = 215, RFA-RS n = 207, CFA-FS n = 47, RFA-FS n = 17). In this task situation, the No-go cue worked as an extension cue to indicate that lever hold should be extended until the reward was delivered. We failed to find any No-go-cue-specific activity in the RS and FS subtypes of the CFA and RFA (Figs. 5C, 6A, and 7A). In addition, we found no auditory response to the reward-pumping noise in Go or No-go trials (data not shown). Accordingly, these motor cortices seem to have no sensory (auditory) or cognitive function to process the Go/No-go signals in our experimental condition. We, therefore, focused on fundamental motor functions, especially the Hold- and Pull-type activities in RS neurons, with regard to the intentional and incidental pull movements. When the lever hold was extended in No-go trials, the Hold-type activity was prolonged until the incidental pull occurred (Figs. 5C and 6A). The prolonged Hold-type activity (a') was more significantly reduced in the RFA-RS neurons than in the CFA-RS neurons [Fig. 6A, right; normalized spike rate in the time window a': CFA-RS 99.7±33.2%, n = 43; RFA-RS 79.8±29.9%, n = 37; t-test p<0.005; and similarly, Fig. 6B, right, KS test p<0.03; Fig. 6B, left, SRNo-go HOLD − SRGo HOLD (including neurons with significant activity only in No-go trials): CFA-RS −0.00±0.16 in Δlog(spike rate); RFA-RS −0.09±0.19; t-test p<0.02]. Besides the Hold-type activity, Pre-pull-type activity (e.g., Fig. 5C, asterisk) showed a gradual increase in spike rate until just before the pull onset, regardless of the different behavioral situations (Fig. 6C; CFA-RS n = 16, RFA-RS n = 7), suggesting that Pre-pull-type activity is associated with motor preparation or initiation.

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