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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 amplitude changes in Pull-type activity for intentional and incidental pulls in RFA-RS neurons.A) Populational changes in normalized spike rate in the Pull-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), the No-go cue (middle), and incidental pull (right) in No-go trials]. Horizontal bars (b and b') correspond to the time windows shown in Fig. 5C. Vertical error bars indicate s.d. values for CFA-RS (orange) and RFA-RS (green) neurons. Note that RFA-RS neurons showed a larger s.d. value during incidental pulls than CFA-RS neurons, and also that no change was observed in response to the No-go cue presentation. B) Left: averaged spike rates of Pull-type activity (significant in Go trials) during intentional pulls (SRGo PULL, corresponding to Fig. 5C, b) and during incidental pulls (SRNo-go PULL, corresponding to b') for individual CFA-RS (orange, filled triangles) and RFA-RS neurons (green). Open triangles represent those with statistical significance only in the No-go trials (corresponding to Fig. 5C, d' and d). Middle: relative Pull-type activity that was normalized with the baseline spike rate (SRGo HOLD) in the same neurons that are shown in the left. Right: cumulative probability analysis of the distribution of normalized spike rates during incidental pulls (b') in the CFA-RS and RFA-RS neurons. The Pull-type activity of RFA-RS neurons was increased or decreased more extensively than that of CFA-RS neurons. Arrowheads indicate representative neurons that were simultaneously recorded from CFA (orange) or from RFA (green). C) Left: larger Pull-type activity changes were found in the RFA-RS neurons than in the CFA-RS neurons across varying extended hold periods [1.0–1.6 s from the No-go (extension) cue to reward delivery]. Right: Pull-type activities in two representative neurons for CFA (a) and RFA (b), indicated by polylines in the left panel.
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pone-0098662-g007: Large amplitude changes in Pull-type activity for intentional and incidental pulls in RFA-RS neurons.A) Populational changes in normalized spike rate in the Pull-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), the No-go cue (middle), and incidental pull (right) in No-go trials]. Horizontal bars (b and b') correspond to the time windows shown in Fig. 5C. Vertical error bars indicate s.d. values for CFA-RS (orange) and RFA-RS (green) neurons. Note that RFA-RS neurons showed a larger s.d. value during incidental pulls than CFA-RS neurons, and also that no change was observed in response to the No-go cue presentation. B) Left: averaged spike rates of Pull-type activity (significant in Go trials) during intentional pulls (SRGo PULL, corresponding to Fig. 5C, b) and during incidental pulls (SRNo-go PULL, corresponding to b') for individual CFA-RS (orange, filled triangles) and RFA-RS neurons (green). Open triangles represent those with statistical significance only in the No-go trials (corresponding to Fig. 5C, d' and d). Middle: relative Pull-type activity that was normalized with the baseline spike rate (SRGo HOLD) in the same neurons that are shown in the left. Right: cumulative probability analysis of the distribution of normalized spike rates during incidental pulls (b') in the CFA-RS and RFA-RS neurons. The Pull-type activity of RFA-RS neurons was increased or decreased more extensively than that of CFA-RS neurons. Arrowheads indicate representative neurons that were simultaneously recorded from CFA (orange) or from RFA (green). C) Left: larger Pull-type activity changes were found in the RFA-RS neurons than in the CFA-RS neurons across varying extended hold periods [1.0–1.6 s from the No-go (extension) cue to reward delivery]. Right: Pull-type activities in two representative neurons for CFA (a) and RFA (b), indicated by polylines in the left panel.

Mentions: We obtained multineuronal recordings [39], [41], [43] from individual neurons in the output layer(s) of CFA or RFA while the rats were performing the forelimb movement task or Go/No-go response task. A 16-channel, two-shank or four-shank silicon probe with one or two tetrode-like arrangements in each shank (A2×2-tet-3 mm-150-150-121/312 or A4×1-tet-3 mm-150-121/312; NeuroNexus Technologies, USA) was inserted vertically up to 1,250 µm deep (putative layer 5; cf. Supplementary Fig. 7a of our previous report [39]) into the CFA or RFA, at least one hour before the start of recording experiment. The multichannel signals were amplified with an amplifier (MEG-6116, Nihon Kohden, Japan; or FA-32, Multi Channel Systems, Germany; final gain, 1000 or 2000; band-pass filter, 0.5 Hz to 10 kHz) through a lab-made preamplifier (voltage-follower, gain 1), and digitized at 20 kHz with a 32-channel hard-disc recorder (LX-120, TEAC, Japan). The position of spout-lever was continuously tracked by an angle encoder throughout the behavioral experiments. The EMG activity of the right forelimb was obtained by an amplifier with its head-stage (EX4-400, Dagan, USA; gain, 1000; band-pass filter, 0.3 Hz to 10 kHz) in some experiments.


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 amplitude changes in Pull-type activity for intentional and incidental pulls in RFA-RS neurons.A) Populational changes in normalized spike rate in the Pull-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), the No-go cue (middle), and incidental pull (right) in No-go trials]. Horizontal bars (b and b') correspond to the time windows shown in Fig. 5C. Vertical error bars indicate s.d. values for CFA-RS (orange) and RFA-RS (green) neurons. Note that RFA-RS neurons showed a larger s.d. value during incidental pulls than CFA-RS neurons, and also that no change was observed in response to the No-go cue presentation. B) Left: averaged spike rates of Pull-type activity (significant in Go trials) during intentional pulls (SRGo PULL, corresponding to Fig. 5C, b) and during incidental pulls (SRNo-go PULL, corresponding to b') for individual CFA-RS (orange, filled triangles) and RFA-RS neurons (green). Open triangles represent those with statistical significance only in the No-go trials (corresponding to Fig. 5C, d' and d). Middle: relative Pull-type activity that was normalized with the baseline spike rate (SRGo HOLD) in the same neurons that are shown in the left. Right: cumulative probability analysis of the distribution of normalized spike rates during incidental pulls (b') in the CFA-RS and RFA-RS neurons. The Pull-type activity of RFA-RS neurons was increased or decreased more extensively than that of CFA-RS neurons. Arrowheads indicate representative neurons that were simultaneously recorded from CFA (orange) or from RFA (green). C) Left: larger Pull-type activity changes were found in the RFA-RS neurons than in the CFA-RS neurons across varying extended hold periods [1.0–1.6 s from the No-go (extension) cue to reward delivery]. Right: Pull-type activities in two representative neurons for CFA (a) and RFA (b), indicated by polylines in the left panel.
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pone-0098662-g007: Large amplitude changes in Pull-type activity for intentional and incidental pulls in RFA-RS neurons.A) Populational changes in normalized spike rate in the Pull-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), the No-go cue (middle), and incidental pull (right) in No-go trials]. Horizontal bars (b and b') correspond to the time windows shown in Fig. 5C. Vertical error bars indicate s.d. values for CFA-RS (orange) and RFA-RS (green) neurons. Note that RFA-RS neurons showed a larger s.d. value during incidental pulls than CFA-RS neurons, and also that no change was observed in response to the No-go cue presentation. B) Left: averaged spike rates of Pull-type activity (significant in Go trials) during intentional pulls (SRGo PULL, corresponding to Fig. 5C, b) and during incidental pulls (SRNo-go PULL, corresponding to b') for individual CFA-RS (orange, filled triangles) and RFA-RS neurons (green). Open triangles represent those with statistical significance only in the No-go trials (corresponding to Fig. 5C, d' and d). Middle: relative Pull-type activity that was normalized with the baseline spike rate (SRGo HOLD) in the same neurons that are shown in the left. Right: cumulative probability analysis of the distribution of normalized spike rates during incidental pulls (b') in the CFA-RS and RFA-RS neurons. The Pull-type activity of RFA-RS neurons was increased or decreased more extensively than that of CFA-RS neurons. Arrowheads indicate representative neurons that were simultaneously recorded from CFA (orange) or from RFA (green). C) Left: larger Pull-type activity changes were found in the RFA-RS neurons than in the CFA-RS neurons across varying extended hold periods [1.0–1.6 s from the No-go (extension) cue to reward delivery]. Right: Pull-type activities in two representative neurons for CFA (a) and RFA (b), indicated by polylines in the left panel.
Mentions: We obtained multineuronal recordings [39], [41], [43] from individual neurons in the output layer(s) of CFA or RFA while the rats were performing the forelimb movement task or Go/No-go response task. A 16-channel, two-shank or four-shank silicon probe with one or two tetrode-like arrangements in each shank (A2×2-tet-3 mm-150-150-121/312 or A4×1-tet-3 mm-150-121/312; NeuroNexus Technologies, USA) was inserted vertically up to 1,250 µm deep (putative layer 5; cf. Supplementary Fig. 7a of our previous report [39]) into the CFA or RFA, at least one hour before the start of recording experiment. The multichannel signals were amplified with an amplifier (MEG-6116, Nihon Kohden, Japan; or FA-32, Multi Channel Systems, Germany; final gain, 1000 or 2000; band-pass filter, 0.5 Hz to 10 kHz) through a lab-made preamplifier (voltage-follower, gain 1), and digitized at 20 kHz with a 32-channel hard-disc recorder (LX-120, TEAC, Japan). The position of spout-lever was continuously tracked by an angle encoder throughout the behavioral experiments. The EMG activity of the right forelimb was obtained by an amplifier with its head-stage (EX4-400, Dagan, USA; gain, 1000; band-pass filter, 0.3 Hz to 10 kHz) in some experiments.

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