Biphasic plasticity of dendritic fields in layer V motor neurons in response to motor learning

Abstract

Motor learning is associated with plastic reorganization of neural networks in primary motor cortex (M1) that advances through stages. An initial increment in spine formation is followed by pruning and maturation one week after training ended. A similar biphasic course was described for the size of the forelimb representation in M1. This study investigates the evolution of the dendritic architecture in response to motor skill training using Golgy-Cox silver impregnation in rat M1. After learning of a unilateral forelimb-reaching task to plateau performance, an increase in dendritic length of layer V pyramidal neurons (i.e. motor neurons) was observed that peaked one month after training ended. This increment in dendritic length reflected an expansion of the distal dendritic compartment. After one month dendritic arborization shrinks even though animals retain task performance. This pattern of evolution was observed for apical and basal dendrites alike -although the increase in dendritic length occurs faster in basal than in apical dendrites. Dendritic plasticity in response to motor training follows a biphasic course with initial expansion and subsequent shrinkage. This evolution takes fourth as long as the biphasic reorganization of spines or motor representations. AbstractMotor learning is associated with plastic reorganization of neural networks in primary motor cortex (M1) that advances through stages. Dendritic spines grow initially followed by pruning and maturation approximately one week after training ended. A similar biphasic course was described for the size of the forelimb representation in M1. This study investigates the evolution of the dendritic architecture in response to motor skill training using Golgy-Cox silver impregnation in rat M1. After learning of a unilateral forelimb-reaching task to plateau performance, an increase in dendritic length of layer V pyramidal neurons (i.e. motor neurons) was observed that peaked one month after training ended. This increment in dendritic length reflected an expansion of the distal dendritic compartment. After one month dendritic arborization shrinks even though animals retain task performance. This pattern of evolution was observed for apical and basal dendrites alike -although the increase in dendritic length occurs faster in basal than in apical dendrites. Dendritic plasticity in response to motor training follows a biphasic course with initial expansion and subsequent shrinkage. This evolution takes fourth as long as the biphasic reorganization of spines or motor representations.3

Circuit Mechanisms of Sensorimotor Learning

“…Motor learning has also been shown to cause an increase in the density of incoming axonal projections (Sampaio-Baptista et al, 2013) as well as an elaboration of the dendritic arbor of M1 neurons (Gloor et al, 2015; Greenough et al, 1985). Furthermore, dendritic spines on M1 pyramidal cells increase in number during the early stages of learning (Fu et al, 2012; Peters et al, 2014; Xu et al, 2009), indicating the formation of new putative synaptic sites.…”

Learning in the Rodent Motor Cortex

“…A later study went on to demonstrate that these dendritic arborization changes are restricted to neurons that are likely involved in the learned movement—in this case, the corticospinal neurons that project to the distal forelimb–associated level of the spinal cord, presumably because of the skilled grasping required in reaching tasks (Wang et al 2011). The increase in dendritic fields is not permanent, however, but instead returns to the prelearning level after learning has taken place, although the performance of the skilled movement is retained (Gloor et al 2015). This transient, learning-related dendritic expansion hints at two potentially crucial features of motor learning.…”

The Motor Cortex Is Involved in the Generation of Classically Conditioned Eyelid Responses in Behaving Rabbits

“…For example, an increase in dendritic length of layer V pyramidal neurons as a result of the acquisition of a motor reaching task has been described (Gloor et al, 2015). These cortical plasticity processes taking place in distal dendrites are dependent on proper NMDA-specific glutamate receptor functions (Hasan et al, 2013).…”

“…In fact, few past (Aou et al, 1992;Birt et al, 2003) or recent (Hasan et al, 2013) studies have addressed the involvement of this key cortical structure in the acquisition of this particular type of associative learning. However, the MC has a well defined and repeated representation of facial muscles (Huang et al, 1988;Morecraft et al, 2001;Müri, 2016), and traditionally has been assumed to be one of the main neural sites involved in the acquisition and proper performance of new motor abilities (Evarts et al, 1983;Doyon and Benali, 2005;Monfils et al, 2005;Brecht et al, 2013;Gloor et al, 2015;Hayashi-Takagi et al, 2015;Kaufman et al, 2015). In fact, MC dynamic activities have been described as interacting with cerebellar and striatal contributions to different types of motor sequence learning (Houk et al, 1996;Hikosaka et al, 2002;Penhune and Steele, 2012;Santos et al, 2015).…”