Distinct Laterality in Forelimb-Movement Representations of Rat Primary and Secondary Motor Cortical Neurons with Intratelencephalic and Pyramidal Tract Projections

Abstract

Two distinct motor areas, the primary and secondary motor cortices (M1 and M2), play crucial roles in voluntary movement in rodents. The aim of this study was to characterize the laterality in motor cortical representations of right and left forelimb movements. To achieve this goal, we developed a novel behavioral task, the Right-Left Pedal task, in which a head-restrained male rat manipulates a right or left pedal with the corresponding forelimb. This task enabled us to monitor independent movements of both forelimbs with high spatiotemporal resolution. We observed phasic movement-related neuronal activity (Go-type) and tonic hold-related activity (Hold-type) in isolated unilateral movements. In both M1 and M2, Go-type neurons exhibited bias toward contralateral preference, whereas Hold-type neurons exhibited no bias. The contralateral bias was weaker in M2 than M1. Moreover, we differentiated between intratelencephalic (IT) and pyramidal tract (PT) neurons using optogenetically evoked spike collision in rats expressing channelrhodopsin-2. Even in identified PT and IT neurons, Hold-type neurons exhibited no lateral bias. Go-type PT neurons exhibited bias toward contralateral preference, whereas IT neurons exhibited no bias. Our findings suggest a different laterality of movement representations of M1 and M2, in each of which IT neurons are involved in cooperation of bilateral movements, whereas PT neurons control contralateral movements. In rodents, the primary and secondary motor cortices (M1 and M2) are involved in voluntary movements via distinct projection neurons: intratelencephalic (IT) neurons and pyramidal tract (PT) neurons. However, it remains unclear whether the two motor cortices (M1 vs M2) and the two classes of projection neurons (IT vs PT) have different laterality of movement representations. We optogenetically identified these neurons and analyzed their functional activity using a novel behavioral task to monitor movements of the right and left forelimbs separately. We found that contralateral bias was reduced in M2 relative to M1, and in IT relative to PT neurons. Our findings suggest that the motor information processing that controls forelimb movement is coordinated by a distinct cell population.

FreiPose: A Deep Learning Framework for Precise Animal Motion Capture in 3D Spaces

“…To this end, we divided continuous paw movements during ex-ploratory behavior into artificial trials by setting a threshold of the paw speed (for details see methods 6.3.4). In line with previous work based on instructed tasks [15], neurons in motor cortex were modulated by the movements of the contralateral but not the ipsilateral paw in a ± 333 ms window around movement onset ( Fig. 4a,b, two-sided t-test on mean normalized firing rate across population, p< 0.05).…”

Lateralized Expression of Cortical Perineuronal Nets during Maternal Experience is Dependent on MECP2

“…This idea of lateralization of function in the rodent brain has been a topic of longstanding yet of sporadic interest in the field (Glick and Ross, 1981;Kim et al, 2012;Soma et al, 2017;Wu et al, 2014). However, the underlying cellular mechanisms governing laterality are unknown.…”

Differential Changes in the Lateralized Activity of Identified Projection Neurons of Motor Cortex in Hemiparkinsonian Rats

“…Neuroimaging and electrophysiological studies in humans and monkeys have shown that unilateral movements are associated with preferred activation (lateralization) of the contralateral primary motor cortex (M1), premotor cortex (PM) and supplementary motor area (SMA; Colebatch et al, 1991; Catalan et al, 1998; Mattay et al, 1998; Solodkin et al, 2001; Kurata, 2007). However, there is a difference in the degree of lateralization among M1 and other motor areas: the preferred activation during contralateral movements in M1 contrasts with the bilateral activation of PM (Kurata, 2007; Soma et al, 2017, 2019). Imaging studies have revealed that the lateralization in the motor cortex is diminished in PD (Wu et al, 2015).…”