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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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Related in: MedlinePlus

Direction preference of Push-/Pull-type activity in CFA and RFA neurons.A) Relative spike rate during forelimb movement in an opposite direction (pull for push, and visa versa) in Push- (left) and Pull-type (right) groups of RS (upper) and FS (lower) subtypes in each area. In Push-type groups, spike rate was first normalized with the peak activity during push movements in individual neurons, and then, they were sorted by the amplitude of relative spike rate for pull movements (large to small). Pull-type groups were analyzed in a similar way. In this analysis, neurons were included in both Push- and Pull-type groups if they showed significant Push-type activity as well as Pull-type activity. B) Spike-rate changes in the Push- and Pull-type groups of RS and FS subtypes (orange, CFA; green, RFA; triangles, RS; circles, FS). Averaged spike rate during push or pull movements (SRPUSH, SRPULL) was plotted against baseline spike rate in the lever hold period (SRHOLD) for individual neurons (left and middle in each group). Cumulative probability analysis (right) shows the distribution of direction preference index [DPI: (SRPULL − SRPUSH)/(SRPULL + SRPUSH)] in the CFA and RFA neurons.
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pone-0098662-g004: Direction preference of Push-/Pull-type activity in CFA and RFA neurons.A) Relative spike rate during forelimb movement in an opposite direction (pull for push, and visa versa) in Push- (left) and Pull-type (right) groups of RS (upper) and FS (lower) subtypes in each area. In Push-type groups, spike rate was first normalized with the peak activity during push movements in individual neurons, and then, they were sorted by the amplitude of relative spike rate for pull movements (large to small). Pull-type groups were analyzed in a similar way. In this analysis, neurons were included in both Push- and Pull-type groups if they showed significant Push-type activity as well as Pull-type activity. B) Spike-rate changes in the Push- and Pull-type groups of RS and FS subtypes (orange, CFA; green, RFA; triangles, RS; circles, FS). Averaged spike rate during push or pull movements (SRPUSH, SRPULL) was plotted against baseline spike rate in the lever hold period (SRHOLD) for individual neurons (left and middle in each group). Cumulative probability analysis (right) shows the distribution of direction preference index [DPI: (SRPULL − SRPUSH)/(SRPULL + SRPUSH)] in the CFA and RFA neurons.

Mentions: It is known that individual neurons in the motor cortex often have a preference for one direction of movement [3]. We examined the preferred direction (push or pull) in each neuron that showed a significant peak activity during push and/or pull movements (Push- and Pull-type activity, respectively). As shown in Fig. 4A, about one-third to one-half of the Push-type group of RS neurons in the CFA and RFA exhibited phasic activations in both push and pull directions, and others exhibited no activation or phasic inactivation in the opposite (pull) direction. These Push-type RS neurons showed no populational differences between the CFA and RFA in the spike-rate change from hold to push (Fig. 4B; SRPUSH − SRHOLD: CFA-RS 0.42±0.33 in Δlog(spike rate), n = 51; RFA-RS 0.32±0.22, n = 41; t-test p>0.07) and from hold to pull (SRPULL − SRHOLD: CFA-RS 0.18±0.32; RFA-RS 0.15±0.26; p>0.6). Similarly, the Pull-type RS neurons showed no differences between the CFA and RFA in spike-rate changes (SRPUSH − SRHOLD: CFA-RS 0.12±0.22, n = 62; RFA-RS 0.08±0.24, n = 88; p>0.4; SRPULL − SRHOLD: CFA-RS 0.25±0.19; RFA-RS 0.31±0.27; p>0.1). On the other hand, most of the FS neurons in the CFA and RFA exhibited phasic activations in both directions (Fig. 4A), and there were no populational differences between the two areas in spike rate changes (Fig. 4B; for Push-type/Pull-type FS neurons (in this order), SRPUSH − SRHOLD: CFA-FS 0.29±0.15/0.16±0.13, n = 29/18; RFA-FS 0.34±0.29/0.09±0.13, n = 9/12; p>0.6/0.1; SRPULL - SRHOLD: CFA-FS 0.27±0.21/0.19±0.09; RFA-FS 0.24±0.25/0.25±0.18; p>0.7/0.3). Furthermore, the direction preference itself was also similar in the CFA and RFA neurons (Fig. 4B; Push-type RS neurons, CFA-RS −0.31±0.34 in DPI, RFA-RS −0.21±0.34, KS-test, p>0.2; Push-type FS neurons, CFA-FS −0.01±0.24, RFA-FS 0.00±0.21, p>0.7; Pull-type FS neurons, CFA-FS 0.00±0.18, RFA-FS 0.18±0.30, p>0.4), except for one group (Pull-type RS neurons, CFA-RS 0.23±0.27, RFA-RS 0.32±0.35, KS-test p<0.05; note it was not significant with a t-test, p>0.08). These observations suggest that the functional activity of RFA neurons resembles that of CFA neurons in both temporal and spatial aspects of motor information.


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)

Direction preference of Push-/Pull-type activity in CFA and RFA neurons.A) Relative spike rate during forelimb movement in an opposite direction (pull for push, and visa versa) in Push- (left) and Pull-type (right) groups of RS (upper) and FS (lower) subtypes in each area. In Push-type groups, spike rate was first normalized with the peak activity during push movements in individual neurons, and then, they were sorted by the amplitude of relative spike rate for pull movements (large to small). Pull-type groups were analyzed in a similar way. In this analysis, neurons were included in both Push- and Pull-type groups if they showed significant Push-type activity as well as Pull-type activity. B) Spike-rate changes in the Push- and Pull-type groups of RS and FS subtypes (orange, CFA; green, RFA; triangles, RS; circles, FS). Averaged spike rate during push or pull movements (SRPUSH, SRPULL) was plotted against baseline spike rate in the lever hold period (SRHOLD) for individual neurons (left and middle in each group). Cumulative probability analysis (right) shows the distribution of direction preference index [DPI: (SRPULL − SRPUSH)/(SRPULL + SRPUSH)] in the CFA and RFA neurons.
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Related In: Results  -  Collection

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

pone-0098662-g004: Direction preference of Push-/Pull-type activity in CFA and RFA neurons.A) Relative spike rate during forelimb movement in an opposite direction (pull for push, and visa versa) in Push- (left) and Pull-type (right) groups of RS (upper) and FS (lower) subtypes in each area. In Push-type groups, spike rate was first normalized with the peak activity during push movements in individual neurons, and then, they were sorted by the amplitude of relative spike rate for pull movements (large to small). Pull-type groups were analyzed in a similar way. In this analysis, neurons were included in both Push- and Pull-type groups if they showed significant Push-type activity as well as Pull-type activity. B) Spike-rate changes in the Push- and Pull-type groups of RS and FS subtypes (orange, CFA; green, RFA; triangles, RS; circles, FS). Averaged spike rate during push or pull movements (SRPUSH, SRPULL) was plotted against baseline spike rate in the lever hold period (SRHOLD) for individual neurons (left and middle in each group). Cumulative probability analysis (right) shows the distribution of direction preference index [DPI: (SRPULL − SRPUSH)/(SRPULL + SRPUSH)] in the CFA and RFA neurons.
Mentions: It is known that individual neurons in the motor cortex often have a preference for one direction of movement [3]. We examined the preferred direction (push or pull) in each neuron that showed a significant peak activity during push and/or pull movements (Push- and Pull-type activity, respectively). As shown in Fig. 4A, about one-third to one-half of the Push-type group of RS neurons in the CFA and RFA exhibited phasic activations in both push and pull directions, and others exhibited no activation or phasic inactivation in the opposite (pull) direction. These Push-type RS neurons showed no populational differences between the CFA and RFA in the spike-rate change from hold to push (Fig. 4B; SRPUSH − SRHOLD: CFA-RS 0.42±0.33 in Δlog(spike rate), n = 51; RFA-RS 0.32±0.22, n = 41; t-test p>0.07) and from hold to pull (SRPULL − SRHOLD: CFA-RS 0.18±0.32; RFA-RS 0.15±0.26; p>0.6). Similarly, the Pull-type RS neurons showed no differences between the CFA and RFA in spike-rate changes (SRPUSH − SRHOLD: CFA-RS 0.12±0.22, n = 62; RFA-RS 0.08±0.24, n = 88; p>0.4; SRPULL − SRHOLD: CFA-RS 0.25±0.19; RFA-RS 0.31±0.27; p>0.1). On the other hand, most of the FS neurons in the CFA and RFA exhibited phasic activations in both directions (Fig. 4A), and there were no populational differences between the two areas in spike rate changes (Fig. 4B; for Push-type/Pull-type FS neurons (in this order), SRPUSH − SRHOLD: CFA-FS 0.29±0.15/0.16±0.13, n = 29/18; RFA-FS 0.34±0.29/0.09±0.13, n = 9/12; p>0.6/0.1; SRPULL - SRHOLD: CFA-FS 0.27±0.21/0.19±0.09; RFA-FS 0.24±0.25/0.25±0.18; p>0.7/0.3). Furthermore, the direction preference itself was also similar in the CFA and RFA neurons (Fig. 4B; Push-type RS neurons, CFA-RS −0.31±0.34 in DPI, RFA-RS −0.21±0.34, KS-test, p>0.2; Push-type FS neurons, CFA-FS −0.01±0.24, RFA-FS 0.00±0.21, p>0.7; Pull-type FS neurons, CFA-FS 0.00±0.18, RFA-FS 0.18±0.30, p>0.4), except for one group (Pull-type RS neurons, CFA-RS 0.23±0.27, RFA-RS 0.32±0.35, KS-test p<0.05; note it was not significant with a t-test, p>0.08). These observations suggest that the functional activity of RFA neurons resembles that of CFA neurons in both temporal and spatial aspects of motor information.

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
Related in: MedlinePlus