The Transition from Development to Motor Control Function in the Corticospinal System

Meng, Zhuo; Li, Qun; Martin, John H.

doi:10.1523/jneurosci.4313-03.2004

Cited by 56 publications

(45 citation statements)

References 34 publications

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“…We then inactivated the right M1 forelimb area between PW7 and PW11 (termed alternate inactivation; n ϭ 6 cats). This is the period when CS axon terminals develop stronger connections with spinal motor circuits (Meng and Martin, 2003;Meng et al, 2004) and when the M1 motor representation forms (Chakrabarty and Martin, 2000). Cats were perfused at the cessation of the second inactivation (PW 11; n ϭ 2) to examine the effects of alternate inactivation on CS tract axon terminations in the cervical enlargement or 1 month later (PW 15 or 16; n ϭ 4) to examine the effects of alternate inactivation on motor skills from PW10 to PW15/16 and regional CS terminations and bouton density.…”

Section: Resultsmentioning

confidence: 99%

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Bilateral Activity-Dependent Interactions in the Developing Corticospinal System

Friel¹,

Martin²

2007

J. Neurosci.

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Activity-dependent competition between the corticospinal (CS) systems in each hemisphere drives postnatal development of motor skills and stable CS tract connections with contralateral spinal motor circuits. Unilateral restriction of motor cortex (M1) activity during an early postnatal critical period impairs contralateral visually guided movements later in development and in maturity. Silenced M1 develops aberrant connections with the contralateral spinal cord whereas the initially active M1, in the other hemisphere, develops bilateral connections. In this study, we determined whether the aberrant pattern of CS tract terminations and motor impairments produced by early postnatal M1 activity restriction could be abrogated by reducing activity-dependent synaptic competition from the initially active M1 later in development. We first inactivated M1 unilaterally between postnatal weeks 5-7. We next inactivated M1 on the other side from weeks 7-11 (alternate inactivation), to reduce the competitive advantage that this side may have over the initially inactivated side. Alternate inactivation redirected aberrant contralateral CS tract terminations from the initially silenced M1 to their normal spinal territories and reduced the density of aberrant ipsilateral terminations from the initially active side. Normal movement endpoint control during visually guided locomotion was fully restored. This reorganization of CS terminals reveals an unsuspected late plasticity after the critical period for establishing the pattern of CS terminations in the spinal cord. Our findings show that robust bilateral interactions between the developing CS systems on each side are important for achieving balance between contralateral and ipsilateral CS tract connections and visuomotor control.

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Section: Resultsmentioning

confidence: 99%

“…After PW5-PW7, CS axon terminations in cats become stronger (Meng and Martin, 2003;Meng et al, 2004) and the M1 motor representation develops (Chakrabarty and Martin, 2000). This is also when the animals' repertoire of skilled movements expands (Martin and Bateson, 1985).…”

Section: Introductionmentioning

confidence: 99%

Bilateral Activity-Dependent Interactions in the Developing Corticospinal System

Friel¹,

Martin²

2007

J. Neurosci.

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“…Further studies are needed to identify the terminal innervations of contralateral CST sprouting enhanced by BMSC treatment after ischemic stroke. Because spinal motoneurons depend on synaptic transmission to receive information from propriospinal and supraspinal fibers, synaptic protein loss is also likely to contribute to the motor dysfunction (Meng et al, 2004). Synaptophysin, a presynaptic marker localized on the membrane of synaptic vesicles, is commonly used for measurement of synapse plasticity (Thiel, 1993).…”

Section: Discussionmentioning

confidence: 99%

Axonal sprouting into the denervated spinal cord and synaptic and postsynaptic protein expression in the spinal cord after transplantation of bone marrow stromal cell in stroke rats

Liu¹,

Li²,

Qu³

et al. 2007

Brain Research

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We investigated whether compensatory reinnervation in the corticospinal tract (CST) and the corticorubral tract (CRT) is enhanced by administration of bone marrow stromal cells (BMSCs) after experimental stroke. Adult male Wistar rats were subjected to permanent right middle cerebral artery occlusion (MCAo). Phosphate-buffered saline (PBS, control, n=7) or 3 × 10 6 BMSCs in PBS (n=8) were injected into a tail vein at 1 day postischemia. The CST of the left sensorimotor cortices was labeled with DiI 2 days prior to MCAo. Functional recovery was measured. Rats were sacrificed at 28 days after MCAo. The brain and spinal cord were removed and processed for vibratome sections for laser-scanning confocal analysis and paraffin sections for immunohistochemistry. Normal rats (n=4) exhibited a predominantly unilateral pattern of innervation of CST and CRT axons. After stroke, bilateral innervation occurred through axonal sprouting of the uninjured CRT and CST. Administration of BMSCs significantly increased the axonal restructuring on the de-afferented red nucleus and the denervated spinal motoneurons (p<0.05). BMSC treatment also significantly increased synaptic proteins in the denervated motoneurons. These results were highly correlated with improved functional outcome after stroke (r>0.81, p<0.01). We conclude that the transplantation of BMSCs enhance axonal sprouting and rewiring into the denervated spinal cord which may facilitate functional recovery after focal cerebral ischemia.

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“…Even though it is obvious that CST connections in the spinal cord are essential for motor map function, it has been largely overlooked since the early studies of Asanuma, Brooks, and colleagues (for review, see Asanuma 1981). After 7 wk, which is when CST spinal terminations achieve a mature laterality and laminar distribution, maturation of the density Martin 2001, 2002) and strength (Meng et al 2004) of CST spinal terminations correlate well with maturation of the M1 motor map. Early postnatal M1 inactivation blocks development of ventrally projecting CST terminations to the deep dorsal horn, intermediate zone, and ventral horn and impairs motor map development.…”

Section: M1 Motor Map Reflects Cst Spinal Termination Patternmentioning

confidence: 99%

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

Chakrabarty

Friel²,

Martin³

2009

Journal of Neurophysiology

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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...

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The Transition from Development to Motor Control Function in the Corticospinal System

Cited by 56 publications

References 34 publications

Bilateral Activity-Dependent Interactions in the Developing Corticospinal System

Bilateral Activity-Dependent Interactions in the Developing Corticospinal System

Axonal sprouting into the denervated spinal cord and synaptic and postsynaptic protein expression in the spinal cord after transplantation of bone marrow stromal cell in stroke rats

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

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