Activity-Dependent Plasticity Improves M1 Motor Representation and Corticospinal Tract Connectivity

Abstract

Chakrabarty S, Friel KM, Martin JH. Activity-dependent plasticity improves M1 motor representation and corticospinal tract connectivity. J Neurophysiol 101: 1283-1293, 2009. First published December 17, 2008 doi:10.1152/jn.91026.2008. Motor cortex (M1) activity between postnatal weeks 5 and 7 is essential for normal development of the corticospinal tract (CST) and visually guided movements. Unilateral reversible inactivation of M1, by intracortical muscimol infusion, during this period permanently impairs development of the normal dorsoventral distribution of CST terminations and visually guided motor skills. These impairments are abrogated if this M1 inactivation is followed by inactivation of the contralateral, initially active M1, from weeks 7 to 11 (termed alternate inactivation). This later period is when the M1 motor representation normally develops. The purpose of this study was to determine the effects of alternate inactivation on the motor representation of the initially inactivated M1. We used intracortical microstimulation to map the left M1 1 to 2 mo after the end of left M1 muscimol infusion. We compared representations in the unilateral inactivation and alternate inactivation groups. Alternate inactivation converted the sparse proximal M1 motor representation produced by unilateral inactivation to a complete and high-resolution proximal-distal representation. The motor map was restored by week 11, the same age that our present and prior studies demonstrated that alternate inactivation restored CST spinal connectivity. Thus M1 motor map developmental plasticity closely parallels plasticity of CST spinal terminations. After alternate inactivation reestablished CST connections and the motor map, an additional 3 wk was required for motor skill recovery. Since motor map recovery preceded behavioral recovery, our findings suggest that the representation is necessary for recovering motor skills, but additional time, or experience, is needed to learn to take advantage of the restored CST connections and motor map. I N T R O D U C T I O NThe primary motor cortex (M1) motor representation develops postnatally. In kittens, the representation, which is examined using intracortical microstimulation (ICMS), is expressed by postnatal week 7 (Bruce and Tatton 1980; Chakrabarty and Martin 2000). Between weeks 7 and 11, the number of sites where ICMS produces a response (i.e., effective sites) increases, ICMS response thresholds decrease, and forelimb joint diversity increases (Chakrabarty and Martin 2000). Motor map development occurs after the critical period for establishing the normal pattern of corticospinal tract (CST) connectivity with spinal circuits, which is between weeks 5 and 7 (Martin 2005). This is when M1 activity is essential for normal development of the CST and visually guided movements. Unilateral reversible inactivation of M1, by intracortical muscimol infusion, during this period affects development of the CST on both the silenced and active sides. The silenced CST fails to develop the normal p...

Activity-Dependent Codevelopment of the Corticospinal System and Target Interneurons in the Cervical Spinal Cord

“…By PW12 all forelimb joints are represented at low current thresholds. The presence of an M1 motor map later in development and maturity correlates with skilled limb control (Monfils et al, 2005;Chakrabarty et al, 2009). Our finding that the CST targets cholinergic interneuron populations with strong ChAT expression after the CST refinement period provides an important spinal substrate for map development.…”

“…Furthermore, M1 activity blockade between PW5 and PW7 produces aberrant dorsal CST projections (Friel and Martin, 2005) that are outside the field of most ChAT neurons, impairing M1 motor map development ) and limb control . Interventions that return CST terminations to more ventral laminae, restores the M1 motor map and limb control Salimi et al, 2008;Chakrabarty et al, 2009). Our findings provide strong support for the importance of development of the spinal connections of the CST to particular interneuronal populations as a key event in shaping of the M1 motor map and expression of CS system motor functions.…”

Postnatal Development of a Segmental Switch Enables Corticospinal Tract Transmission to Spinal Forelimb Motor Circuits

“…These changes in spinal organization of the CS system contralateral to the inactivation are associated with M1 motor map (Chakrabarty et al, 2009b) and motor control impairments (Martin et al, 2000; Martin et al, 2004; Friel et al, 2007). We next asked if this inactivation also limits development of effective segmental CST transmission to ventral motor circuits.…”

Do sensorimotor β-oscillations maintain muscle synergy representations in primary motor cortex?

“…It is well established that skilled movements are not possible until after the establishment of corticospinal connectivity. Indeed, in cats there is tight correlation between onset of corticospinal connectivity, formation of M1 muscle representations, and skilled movement performance, all of which are dependent on M1 neural activity [68][69][70]. Continued protein synthesis, which is known to depend on various factors including neuronal activity, is also crucial for M1 motor map maintenance, synaptic transmission, and skilled movement performance in adult rats [71].…”