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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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Basal spiking properties of CFA and RFA neurons.A) Classification of isolated units in CFA (orange) and RFA (green) into regular-spiking (RS; spike duration >0.5 ms, light colors) and fast-spiking (FS; ≤0.5 ms, dark colors) subtypes of neurons. Top: ongoing (all averaged) spike rate plotted against spike duration for individual neurons. Bottom: bimodal distribution of spike duration. Insets, typical spike waveforms for the two neuron subtypes (mean ± s.d.; calibration: 1 ms, 0.1 mV; gray bar, spike duration). B) Coefficient of variation (CV) of inter-spike intervals (ISIs) in CFA and RFA neurons. Histograms show CV distributions for RS (light) and FS (dark) subtypes. C) Cumulative probability analysis of the CV distribution shown in B. D) Temporal feature in auto-correlogram (ACG) in CFA and RFA neurons. We defined ACG bias as a median value in ACG from 0 to +100 ms (red lines in two insets). Histograms show ACG bias distributions for RS (light) and FS (dark) subtypes. E) Cumulative probability analysis of the ACG bias distribution shown in D.
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pone-0098662-g002: Basal spiking properties of CFA and RFA neurons.A) Classification of isolated units in CFA (orange) and RFA (green) into regular-spiking (RS; spike duration >0.5 ms, light colors) and fast-spiking (FS; ≤0.5 ms, dark colors) subtypes of neurons. Top: ongoing (all averaged) spike rate plotted against spike duration for individual neurons. Bottom: bimodal distribution of spike duration. Insets, typical spike waveforms for the two neuron subtypes (mean ± s.d.; calibration: 1 ms, 0.1 mV; gray bar, spike duration). B) Coefficient of variation (CV) of inter-spike intervals (ISIs) in CFA and RFA neurons. Histograms show CV distributions for RS (light) and FS (dark) subtypes. C) Cumulative probability analysis of the CV distribution shown in B. D) Temporal feature in auto-correlogram (ACG) in CFA and RFA neurons. We defined ACG bias as a median value in ACG from 0 to +100 ms (red lines in two insets). Histograms show ACG bias distributions for RS (light) and FS (dark) subtypes. E) Cumulative probability analysis of the ACG bias distribution shown in D.

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)

Basal spiking properties of CFA and RFA neurons.A) Classification of isolated units in CFA (orange) and RFA (green) into regular-spiking (RS; spike duration >0.5 ms, light colors) and fast-spiking (FS; ≤0.5 ms, dark colors) subtypes of neurons. Top: ongoing (all averaged) spike rate plotted against spike duration for individual neurons. Bottom: bimodal distribution of spike duration. Insets, typical spike waveforms for the two neuron subtypes (mean ± s.d.; calibration: 1 ms, 0.1 mV; gray bar, spike duration). B) Coefficient of variation (CV) of inter-spike intervals (ISIs) in CFA and RFA neurons. Histograms show CV distributions for RS (light) and FS (dark) subtypes. C) Cumulative probability analysis of the CV distribution shown in B. D) Temporal feature in auto-correlogram (ACG) in CFA and RFA neurons. We defined ACG bias as a median value in ACG from 0 to +100 ms (red lines in two insets). Histograms show ACG bias distributions for RS (light) and FS (dark) subtypes. E) Cumulative probability analysis of the ACG bias distribution shown in D.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0098662-g002: Basal spiking properties of CFA and RFA neurons.A) Classification of isolated units in CFA (orange) and RFA (green) into regular-spiking (RS; spike duration >0.5 ms, light colors) and fast-spiking (FS; ≤0.5 ms, dark colors) subtypes of neurons. Top: ongoing (all averaged) spike rate plotted against spike duration for individual neurons. Bottom: bimodal distribution of spike duration. Insets, typical spike waveforms for the two neuron subtypes (mean ± s.d.; calibration: 1 ms, 0.1 mV; gray bar, spike duration). B) Coefficient of variation (CV) of inter-spike intervals (ISIs) in CFA and RFA neurons. Histograms show CV distributions for RS (light) and FS (dark) subtypes. C) Cumulative probability analysis of the CV distribution shown in B. D) Temporal feature in auto-correlogram (ACG) in CFA and RFA neurons. We defined ACG bias as a median value in ACG from 0 to +100 ms (red lines in two insets). Histograms show ACG bias distributions for RS (light) and FS (dark) subtypes. E) Cumulative probability analysis of the ACG bias distribution shown in D.
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.

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