Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain

Abstract

Cortical networks undergo adaptations during learning, including increases in dendritic complexity and spines. We hypothesized that structural elaborations during learning are restricted to discrete subsets of cells preferentially activated by, and relevant to, novel experience. Accordingly, we examined corticospinal motor neurons segregated on the basis of their distinct descending projection patterns, and their contribution to specific aspects of motor control during a forelimb skilled grasping task in adult rats. Learningmediated structural adaptations, including extensive expansions of spine density and dendritic complexity, were restricted solely to neurons associated with control of distal forelimb musculature required for skilled grasping; neurons associated with control of proximal musculature were unchanged by the experience. We further found that distal forelimb-projecting and proximal forelimbprojecting neurons are intermingled within motor cortex, and that this distribution does not change as a function of skill acquisition. These findings indicate that representations of novel experience in the adult motor cortex are associated with selective structural expansion in networks of functionally related, active neurons that are distributed across a single cortical domain. These results identify a distinct parcellation of cortical resources in support of learning.cell filling | corticospinal neurons | morphology | sensorimotor cortex P rior studies have documented alterations of neuronal structure in response to experience and learning (1-6), raising the possibility that these structural modifications might serve as a basis for long-term memory. Within randomly sampled layer V pyramidal neurons of the motor cortex, dendritic branching and arborization (1, 2) and synapse number (5, 7, 8) increase in rats undergoing skilled motor training. New spines reportedly form rapidly after training (9), are stabilized by repeated training, and can persist for extended times beyond the experience (10). Collectively, these observations support the concept that newly formed connections may provide a basis for long-term maintenance of experience.However, studies examining modifications of neuronal architecture in the context of learning and experience have not focused exclusively on neurons specifically engaged by the experience; instead, random sampling of neurons has been used across the broader cortical functional unit (e.g., forelimb motor cortex or visual cortex). To reach a greater level of understanding regarding the nature of experiential representation in the learning adult brain, it is necessary to examine structural modifications in functionally distinct subsets of neurons based on their relevance to the learning experience. In the present study, taking advantage of specific output patterns of the motor system, we attempt to achieve this level of resolution using a combination of behavioral training and retrograde filling of cortical motor neurons projecting to distinct spinal segments that act as effectors of...

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

“…However, we are confident that this limitation does not reduce the validity of this study. The learning-dependent enlargement of apical dendrites reported here is in good agreement with previous studies [4,13].…”

“…rewarding reaching attempts by application of a food pellet directly into the animals mouth) are known to induce a certain enlargement of dendrites of layer V motor neurons. However, this enlargement is significantly smaller when compared to learning groups in both, apical [4] and basal dendrites [13,14]. Furthermore, this activity-induced enlargement of dendritic trees follows a different time-course with a pruning that is present after four weeks [28].…”

“…Thus, this neuronal staining has no specificity for neurons that underwent plastic changes or were involved in the control of the trained limb. Recently, the results of earlier studies relying on Golgy-Cox staining were reproduced by Wang and colleagues [13], that used retrograde tracer injection into the cervical spinal cord to identify motor neurons that selectively control the forepaw. Training a reaching task induced an enlargement of dendritic length and number of branches only in these neurons but not in motor neurons projecting to cervical segments controlling more distal muscles of the forelimb.…”

“…The speed of this change is unknown because no measurements were conducted between day 5 and 2 months. Enlarged dendritic fields have been described two weeks after training onset [4,13,17] -a time-point at which spine density and map size already returned to baseline. The peak in dendritic arborization one month after training found here indicates a kinetic of plastic changes that is even slower than expected.…”

“…An initial increase in spine formation for example is followed by an enhanced turnover that reduces the number of spines to baseline levels [5]. Whereas this concept of biphasic reorganization has been well demonstrated for spines [5], synaptic weights [11] and motor maps [12] it is unknown whether learning-induced growth of dendritic fields [4,13,14] is a lasting phenomenon or if a pruning occurs after a delay. To address this question, we measured dendritic morphology of layer V motoneurons at different time-points (day 0, day 30 and day 60) following acquisition of a skilled reaching task in rats.…”