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, 103 (30), 11370-5

A Form of Motor Cortical Plasticity That Correlates With Recovery of Function After Brain Injury

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A Form of Motor Cortical Plasticity That Correlates With Recovery of Function After Brain Injury

Dhakshin Ramanathan et al. Proc Natl Acad Sci U S A.

Abstract

To investigate functional mechanisms underlying cortical motor plasticity in the intact and injured brain, we used "behaviorally relevant," long-duration intracortical microstimulation. We now report the existence of complex, multijoint movements revealed with a 500-msec duration intracortical stimulation in rat motor cortex. A consistent topographic distribution of these complex motor patterns is present across the motor cortex in naïve rats. We further document the plasticity of these complex movement patterns after focal cortical injury, with a significant expansion of specific complex movement representations in response to rehabilitative training after injury. Notably, the degree of functional recovery attained after cortical injury and rehabilitation correlates significantly with a specific feature of map reorganization, the ability to reexpress movement patterns disrupted by the initial injury. This evidence suggests the existence of complex movement representations in the rat motor cortex that exhibit plasticity after injury and rehabilitation, serving as a relevant predictor of functional recovery.

Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.
Fig. 1.
Complex movements elicited by long-duration microstimulation. (AC) Three types of complex movements evoked by long-duration stimulation within motor cortex. Complex movements elicited by long-duration microstimulation occur across multiple joints. (A) Reaching movement characterized by rostral displacement of the elbow and shoulder, without change in wrist configuration. (B) Retraction characterized by caudal displacement of the elbow and forepaw. (C) Grasping movement characterized by contraction of all digit joints simultaneously.
Fig. 2.
Fig. 2.
Coordinated sequence of complex movements elicited by prolonged simulation in rostral forelimb area of motor cortex. (A) Coordinated sequence of reach, grasp, and retract movements elicited by a single 500-msec stimulus within the rostral portion of the motor cortex. (B and C) Illustrated, using a digitized kinematic analysis, are the temporal sequence of this complex movement. Repeated stimulation at the same site elicited the same sequence of complex movements.
Fig. 3.
Fig. 3.
Comparison of cortical motor maps derived by using short-duration (30 msec) and long-duration (500 msec) intracortical microstimulation. (A) Representative motor map of forelimb motor cortex derived by using a short-duration (30-msec) microstimulation paradigm. Two regions of classic forelimb cortex, caudal forelimb area and rostral forelimb area, are separated by intervening neck-responsive sites. Distal forelimb movements (wrist) are elicited generally in lateral caudal forelimb areas. (B) Representative motor map derived by using the long-duration (500 msec) ICMS paradigm, demonstrating complex movement representations. Complex movements elicited by the prolonged stimulation paradigm include reaching, grasping, and retractions. Stimulation in rostral forelimb areas elicited complex sequences of movements such as grasp-retract or reach-grasp (shown as split squares in the figures). (C) Cumulative distribution of complex movement patterns in 11 naïve animals. The distribution of complex movements demonstrates a clear topography across motor cortex: Retractions are elicited by stimulation within lateral caudal forelimb area, reaches by stimulation spanning medial aspects of caudal and rostral forelimb areas, and grasps by stimulation within rostral motor cortex. Complex movement combinations are elicited by stimulation within rostral forelimb area (black squares).
Fig. 4.
Fig. 4.
Focal brain injury and rehabilitative training are associated with significant plasticity of complex movement representations. (A) Characteristic topography of complex movements in intact animals: Retractions are located laterally, reaches are medial, and grasps and complex movement sequences are rostral. (B and C) After a lesion targeting the lateral aspect of the caudal forelimb area, forelimb movements can no longer be elicited in and around the lesion site. (B) Moreover, rehabilitated animals exhibit a significant expansion of complex movements (outlined) within undamaged rostral forelimb area relative both to naïve control rats (A) and to nonrehabilitated, lesioned animals (C). (D) Quantification of plasticity within the RFA demonstrates that rehabilitative training after a lesion results in significant expansion of complex movement sequences (reach-grasp, grasp-retract, and reach-grasp-retract) above both naïve controls and nonrehabilitated controls (ANOVA, P < 0.01; Fisher’s post hoc between rehab vs. nonrehab, P < 0.01; Fisher’s post hoc between rehab vs. prelesion control, P < 0.01). (E) The area encoding retraction movements is significantly reduced by 67% after the lesion in nonrehabilitated animals (ANOVA, P < 0.001; Fisher’s post hoc, P < 0.0001). Notably, rehabilitative training significantly increased the area of cortex encoding retraction movements (P < 0.05 compared with nonrehabilitated animals), partially restoring the specific loss of retraction movements imposed by the lesion. Paralleling the extent of behavioral recovery, the area encoding retraction movements in rehabilitated animals recovers to 64% of intact controls. (F) The area of cortex encoding stimulus-evoked retraction movements significantly correlates with the degree of functional recovery in rehabilitated animals (R2 = 0.46, P < 0.05). No significant correlation was found between the cortical area encoding reaching or grasping movements and functional recovery (data not shown).

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