Interactions between rostral and caudal cortical motor areas in the rat

Abstract

In rats, forelimb movements can be evoked from two distinct cortical regions, the rostral (RFA) and the caudal (CFA) forelimb areas. RFA and CFA have numerous reciprocal connections, and their projections reach several common targets, which allows them to interact at multiple levels of the motor axis. Lesions affecting these areas result in profound and persistent deficits, supporting their essential role for the production of arm and hand movements. Whereas rats are widely used to study motor control and recovery following lesions, little is known as to how cortical motor areas in this model interact to generate movements. To study interactions between RFA and CFA, we used paired-pulse protocols with intracortical microstimulation techniques (ICMS). A conditioning stimulus (C) in RFA was applied simultaneously, or before a test stimulus (T) in CFA. The impact of RFA conditioning on CFA outputs was quantified by recording electromyographic signals (EMG) signals from the contralateral arm muscles. We found that stimulation of RFA substantially modulates the intensity of CFA outputs while only mildly affecting the latency. In general, the effect of RFA conditioning changed from predominantly facilitatory to inhibitory with increasing delays between the C and the T stimulus. However, inspection of individual cortical sites revealed that RFA has a wide range of influence on CFA outputs with each interstimulation delay we used. Our results show that RFA has powerful and complex modulatory effects on CFA outputs that can allow it to play a major role in the cortical control of forelimb movements.

Combinatorial Motor Training Results in Functional Reorganization of Remaining Motor Cortex after Controlled Cortical Impact in Rats

“…[46][47][48] In rats, CMC and RMC have many reciprocal connections 47 and are tightly coupled in driving movement production. 49 RMC has strong modulatory effects on CMC 50 and is likely to have a key role in the resolution of upper-extremity impairments, as has been found in other injury models 10,41 and in human and primate studies. [51][52][53] In standard ICMS studies, forelimb movements can be evoked at £60 uA.…”

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

“…Therefore, it is possible that the slightly delayed sink in layer 5 was generated by synaptic inputs from layer 2/3 neurons in the RFA rather than by direct inputs from the CFA. Given the fact that layer 5 neurons in M2 project to the thalamus, striatum and back to M1/ S1 (Ueta et al, 2013(Ueta et al, , 2014Manita et al, 2015), the neural information conveyed to the RFA might be used to produce the topdown signals necessary for optimal perceptual behavior (Smith et al, 2010;Deffeyes et al, 2015;Manita et al, 2015).…”

“…The cerebello-thalamo-cortical circuit has been implicated in a variety of sensorimotor functions, including somatosensory integration (Manzoni, 2007), the control of continuous movements and externally guided movements (Elsinger et al, 2006;Schnitzler et al, 2006;Lewis et al, 2007). Therefore, it is possible that sensory signals relayed to the RFA from the CFA could play a role in modulating susceptibility to inputs from the cerebellum, which, in turn, would contribute to the optimization and correction of ongoing movements during motor skill learning (Smith et al, 2010;Deffeyes et al, 2015).…”

“…In an anatomical sense, the CFA and RFA in rats are considered to be analogous to the primary motor cortex and the premotor and/or supplementary motor cortices, respectively, in primates (Rouiller et al ., ; Wang & Kurata, ; Mohammed & Jain, ). 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, ).…”

Thalamic afferents to prefrontal cortices from ventral motor nuclei in decision‐making

“…Similarly, by recording cortical antidromic activity driven by cortical stimulation, Arbuthnott et al (1990) described that [a] "network of terminal axons is seen in layer 1 as far back as the injection site [AP À5.5], as far anterior as the frontal pole and as far lateral as the rhinal sulcus in which areas the caudal-most fibers are regularly found". These areas in rats (Neafsey et al, 1986) and mice (Tennant et al, 2011;Deffeyes et al, 2015) include the typically extensive motor associated cortical areas including forelimb and hindlimb regions and prefrontal cortical regions. Rubio-Garrido et al (2009) report that a small deposit of biotinylated dextran amine on the cortical surface backfilled approximately 150 neurons in VM whose axon arbors can be observed in layer 1 in the frontal pole anterior to the middle cerebral artery.…”