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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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Behavioral task performance.A) A schematic of the forelimb movement task and recording sites for the two motor cortices. Rats held (for 1 s) and pulled a spout-lever to acquire reward water in a head-fixed condition. Multineuronal activity was recorded from the caudal and rostral forelimb areas (CFA and RFA) [primary and secondary motor cortices (M1 and M2), respectively] during task performance. Upper right: electrode tracks (arrowheads; layer 5) for the CFA and RFA recordings in Nissl-stained sections. See Materials and Methods for details. B) Lever trajectory and electromyogram (EMG) activity in right forelimb. Top: lever and EMG traces for several trials. Bottom: averaged EMG power aligned with the end of push or the onset of pull movements (vertical lines). C) Behavioral task performance. Top: hold time until the lever pull onset in response to cue tone presentation after the hold period (1 s) in a rat. Black and gray colors indicate correct and error trial responses, respectively. Bottom: peak distribution of hold time in all of the rats.
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pone-0098662-g001: Behavioral task performance.A) A schematic of the forelimb movement task and recording sites for the two motor cortices. Rats held (for 1 s) and pulled a spout-lever to acquire reward water in a head-fixed condition. Multineuronal activity was recorded from the caudal and rostral forelimb areas (CFA and RFA) [primary and secondary motor cortices (M1 and M2), respectively] during task performance. Upper right: electrode tracks (arrowheads; layer 5) for the CFA and RFA recordings in Nissl-stained sections. See Materials and Methods for details. B) Lever trajectory and electromyogram (EMG) activity in right forelimb. Top: lever and EMG traces for several trials. Bottom: averaged EMG power aligned with the end of push or the onset of pull movements (vertical lines). C) Behavioral task performance. Top: hold time until the lever pull onset in response to cue tone presentation after the hold period (1 s) in a rat. Black and gray colors indicate correct and error trial responses, respectively. Bottom: peak distribution of hold time in all of the rats.

Mentions: As established previously [40], we first trained the rats to perform a simple forelimb movement task (Fig. 1A), in which they had to manipulate a ''spout-lever'' with their right forelimb in a head-fixed condition. They spontaneously started each trial of this task by pushing the spout-lever forward and holding it for a short period (''hold period'') with the right forelimb. The hold period was extended from 0 ms up to 1,000 ms (final) in a step-by-step manner according to the total number of success trials. After the hold period was completed, a cue sound was briefly presented to them (10 kHz pure tone for 300 ms). If they pulled the spout-lever toward their mouth (holding position, 0–3 mm; licking position, 6–9 mm from the front end) in response to the cue presentation, then they were allowed to lick the spout-lever to drink 0.1% saccharin water (5 or 10 µl) as a reward. The reward was accurately dispensed from the tip of spout-lever by a micropump with a 200–800 ms delay (100 ms steps at random). The reward delivery period was followed by a short inter-trial interval (200–800 ms). Unless they held the spout-lever throughout the hold period, or unless they pulled it correctly within 5,300 ms (or 500 ms for Go trials in Go/No-go discrimination) after the cue onset, the rats were not rewarded (error trial) and had another attempt after the inter-trial interval. The rats typically learned the forelimb movement task within three days (2–5 hours a day) very efficiently using our automatic multi-rat task-training system (O'hara & Co., Ltd., Japan). Once the rats completed the operant learning of the forelimb movement task, they underwent a second surgery under anesthesia, and a tiny hole (1.0 to 1.5 mm in diameter) was made in the skull and dura mater above the left CFA (1.0±1.0 mm anterior, 2.5±1.0 mm lateral from bregma; mostly in the center of this area) or RFA (3.5±0.2 mm anterior, 2.4±0.2 mm lateral from bregma). These coordinates were determined by intracortical microstimulation (ICMS; −50 to −100 µA, 50 pulses at 100 Hz) to evoke reliable movement from the contralateral forelimb in our preliminary experiments (data not shown). In some cases, it was confirmed by the ICMS after a recording experiment (8–10 rats in each area). The hole was covered with silicon sealant (DentSilicone-V, Shofu, Japan). On the following day, they were transferred to a single behavioral experiment system (O'hara & Co., Ltd.) for final behavioral and electrophysiological 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)

Behavioral task performance.A) A schematic of the forelimb movement task and recording sites for the two motor cortices. Rats held (for 1 s) and pulled a spout-lever to acquire reward water in a head-fixed condition. Multineuronal activity was recorded from the caudal and rostral forelimb areas (CFA and RFA) [primary and secondary motor cortices (M1 and M2), respectively] during task performance. Upper right: electrode tracks (arrowheads; layer 5) for the CFA and RFA recordings in Nissl-stained sections. See Materials and Methods for details. B) Lever trajectory and electromyogram (EMG) activity in right forelimb. Top: lever and EMG traces for several trials. Bottom: averaged EMG power aligned with the end of push or the onset of pull movements (vertical lines). C) Behavioral task performance. Top: hold time until the lever pull onset in response to cue tone presentation after the hold period (1 s) in a rat. Black and gray colors indicate correct and error trial responses, respectively. Bottom: peak distribution of hold time in all of the rats.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0098662-g001: Behavioral task performance.A) A schematic of the forelimb movement task and recording sites for the two motor cortices. Rats held (for 1 s) and pulled a spout-lever to acquire reward water in a head-fixed condition. Multineuronal activity was recorded from the caudal and rostral forelimb areas (CFA and RFA) [primary and secondary motor cortices (M1 and M2), respectively] during task performance. Upper right: electrode tracks (arrowheads; layer 5) for the CFA and RFA recordings in Nissl-stained sections. See Materials and Methods for details. B) Lever trajectory and electromyogram (EMG) activity in right forelimb. Top: lever and EMG traces for several trials. Bottom: averaged EMG power aligned with the end of push or the onset of pull movements (vertical lines). C) Behavioral task performance. Top: hold time until the lever pull onset in response to cue tone presentation after the hold period (1 s) in a rat. Black and gray colors indicate correct and error trial responses, respectively. Bottom: peak distribution of hold time in all of the rats.
Mentions: As established previously [40], we first trained the rats to perform a simple forelimb movement task (Fig. 1A), in which they had to manipulate a ''spout-lever'' with their right forelimb in a head-fixed condition. They spontaneously started each trial of this task by pushing the spout-lever forward and holding it for a short period (''hold period'') with the right forelimb. The hold period was extended from 0 ms up to 1,000 ms (final) in a step-by-step manner according to the total number of success trials. After the hold period was completed, a cue sound was briefly presented to them (10 kHz pure tone for 300 ms). If they pulled the spout-lever toward their mouth (holding position, 0–3 mm; licking position, 6–9 mm from the front end) in response to the cue presentation, then they were allowed to lick the spout-lever to drink 0.1% saccharin water (5 or 10 µl) as a reward. The reward was accurately dispensed from the tip of spout-lever by a micropump with a 200–800 ms delay (100 ms steps at random). The reward delivery period was followed by a short inter-trial interval (200–800 ms). Unless they held the spout-lever throughout the hold period, or unless they pulled it correctly within 5,300 ms (or 500 ms for Go trials in Go/No-go discrimination) after the cue onset, the rats were not rewarded (error trial) and had another attempt after the inter-trial interval. The rats typically learned the forelimb movement task within three days (2–5 hours a day) very efficiently using our automatic multi-rat task-training system (O'hara & Co., Ltd., Japan). Once the rats completed the operant learning of the forelimb movement task, they underwent a second surgery under anesthesia, and a tiny hole (1.0 to 1.5 mm in diameter) was made in the skull and dura mater above the left CFA (1.0±1.0 mm anterior, 2.5±1.0 mm lateral from bregma; mostly in the center of this area) or RFA (3.5±0.2 mm anterior, 2.4±0.2 mm lateral from bregma). These coordinates were determined by intracortical microstimulation (ICMS; −50 to −100 µA, 50 pulses at 100 Hz) to evoke reliable movement from the contralateral forelimb in our preliminary experiments (data not shown). In some cases, it was confirmed by the ICMS after a recording experiment (8–10 rats in each area). The hole was covered with silicon sealant (DentSilicone-V, Shofu, Japan). On the following day, they were transferred to a single behavioral experiment system (O'hara & Co., Ltd.) for final behavioral and electrophysiological 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
Related in: MedlinePlus