Different Modulation of Common Motor Information in Rat Primary and Secondary Motor Cortices

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.

High‐order motor cortex in rats receives somatosensory inputs from the primary motor cortex via cortico‐cortical pathways

“…Consistent with this hypothesis, the RFA modulates descending output signals from the CFA but the CFA does not modulate signals from the RFA (Deffeyes et al ., ). Furthermore, the activity patterns of RFA neurons in rodents are influenced by changes in their internal state, such as attention and motivation (Saiki et al ., ), as has been reported in the premotor cortex of monkeys (Roesch & Olson, ).…”

“…Two independent forelimb motor areas have been identified in the rodent motor cortex; the caudal forelimb area (CFA) in the primary motor cortex (M1) and the rostral forelimb area (RFA) in the secondary motor cortex (M2; Neafsey & Sievert, 1982;Young et al, 2011;Tennant et al, 2011). Both of these areas are reciprocally connected by cortico-cortical connections (Rouiller et al, 1993;Wang & Kurata, 1998;Ueta et al, 2014) and are thought to be involved in forelimb-related motor functions, including motor execution and motor skill learning (Kleim et al, 1998(Kleim et al, , 2004Tennant et al, 2012;Brown & Teskey, 2014;Saiki et al, 2014).…”

Large‐scale analysis reveals populational contributions of cortical spike rate and synchrony to behavioural functions

“…; Saiki et al . ). We defined task‐related and non‐task‐related neurons using our task relevance index and the total number of spikes (Table A ; see Methods).…”

“…; RFA: 3.5 ± 0.5 mm anterior, 2.0 ± 0.5 mm lateral, Hyland, ; Saiki et al . ). The hole was covered with silicone sealant (Dent Silicone‐V, Regular, Shofu, Kyoto, Japan) until recording started.…”

“…In some experiments, these coordinates were confirmed by checking forelimb movements or EMG activities in the contralateral forelimb in response to intracortical microstimulation (ICMS; about −20 to −120 μA, 50 pulses at 100 Hz or sustained pulses; SEN 8203, Nihon Kohden, Tokyo, Japan) (Saiki et al . ). For multiple single‐unit recording, a 16‐channel silicon probe (A2×2‐tet‐3mm‐150‐150‐121/312; NeuroNexus, Ann Arbor, MI, USA; 2 shanks × 2 tetrode‐like sites, at 150 μm intervals) was placed on the brain surface in the skull hole, and then covered with 2% agarose (Agarose‐HGT; Nacalai Tesque, Kyoto, Japan) and paraffin wax (Nacalai Tesque) to prevent drying.…”