Peripheral nerve injury in developing rats reorganizes representation pattern in motor cortex.

Abstract

We investigated the effect of neonatal nerve lesions on cerebral motor cortex organization by comparing the cortical motor representation of normal adult rats with adult rats that had one forelimb removed on the day of birth. Mapping of cerebral neocortex with electrical stimulation revealed an altered relationship between the motor cortex and the remaining muscles. Whereas distal forelimb movements are normally elicited at the lowest threshold in the motor cortex forelimb area, the same stimuli activated shoulder and trunk muscles in experimental animals. In addition, an expanded cortical representation of intact body parts was present and there was an absence of a distinct portion of motor cortex. These data demonstrate that representation patterns in motor cortex can be altered by peripheral nerve injury during development.Genetic mechanisms expressed during development are believed to be important determinants of the functional organization of cortical areas. It is also clear that representation patterns can be modified, at least in sensory cortex. Anatomical and electrophysiological investigations of somatic sensory and visual cortices have shown that injury to peripheral receptors or even selective forms of experience in developing mammals result in expanded representations of intact parts (1-4) and concomitant changes in cortical connectivity patterns (5-9). Although developmentally induced modifications in representation patterns, intrinsic organization, or efferent connections of motor cortex could profoundly affect movement execution and control, the effect of peripheral nerve injury on these aspects of motor organization is largely unknown. In the present study we examined the effect of neonatal peripheral nerve injury on the somatic representation in the primary motor cortex (MI) in rats.Among all cerebral neocortical areas, MI appears to be most closely related to the control of muscles. MI is necessary for the independent use of muscles in skilled voluntary movements, participates in movement initiation, and is involved in the elaboration of the complex repertoire of movements observed in mammals (10, 11). Generally, MI is defined in a variety of mammals as the cortical area in which movements can be evoked at the lowest levels of electrical stimulation (12). Intracortical microstimulation (ICMS) mapping reveals a topographically ordered pattern of representation in MI; focal sites in cortex are related to one or a few closely related muscles (13). Although electrical stimulation produces artificial patterns of neural activation, it appears to reflect the functional relationship of small regions of MI with muscles, since neurons at a cortical site discharge during movements of the same muscles that are activated by ICMS at that same site (14). In rats MI is largely comprised of a cytoarchitectonically distinct frontal agranular cortical field that contains forelimb, head, and trunk representations. A portion of the immediately adjacent granular somatic sensory cortex (SI) is also included i...

Functional connectivity of the transected brachial plexus after intercostal neurotization in monkeys

“…However, this plasticity is generated by rewiring from nearby neurons and occurs in neonates. Alterations of movement representations in primary motor cortex of adult monkeys by task training or peripheral nerve lesions in rats have been shown (Donoghue and Sanes, 1987;Donoghue et al, 1990Donoghue et al, , 1992Sanes et al, 1990;Nudo and Milliken, 1996). Nevertheless, the output reorganization appeared to be restricted to cortically adjacent areas (Donoghue and Sanes, 1987;Donoghue et al, 1990Donoghue et al, , 1992Sanes et al, 1990).…”

Congenitally altered motor experience alters somatotopic organization of human primary motor cortex

“…It also differs from previous reports of deafferentation induced reorganization of M1. Rats with neonatal forelimb amputations (35) and humans with upper limb amputations during childhood (8-10) failed to demonstrate comparable large-scale changes. Because amputations in these studies were unilateral and functional compensation of the resulting deficit was not mentioned, this seems to underline the importance of exceptional foot dexterity as the driving force for our findings (further discussed below).…”

Voltage-Sensitive Dye Imaging Reveals Dynamic Spatiotemporal Properties of Cortical Activity after Spontaneous Muscle Twitches in the Newborn Rat

“…In sensory areas, they promote homotopic connections by synchronizing cortical regions receiving afferent inputs from adjacent sensory organs (Feller, 1999). In the adult rodent, close anatomical connections exist between the somatosensory and motor cortices (Donoghue and Parham, 1983;Fabri and Burton, 1991), and the motor cortex is rapidly altered by sensory input (Donoghue and Sanes, 1987;Sanes et al, 1990Sanes et al, , 1992. Depolarization from the somatosensory cortex that moves medially within the developing cortex may serve to promote the maturation of these anatomical and functional connections.…”