Differential spinal projections from the forelimb areas of the rostral and caudal subregions of primary motor cortex in the cat

Jh, Martin

doi:10.1007/bf00228094

Cited by 54 publications

(53 citation statements)

References 53 publications

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“…Different M1 regions can contact selective interneuronal populations. For example, rostral M1 projections are ventrally biased, compared with caudal M1, and the only subregion with connectivity to C3-C4 propriospinal neurons (Martin, 1996;Alstermark and Ohlson, 2000). Our findings suggest an even more subtle organization, in which neighboring territories have interdigitated terminations.…”

Section: Multiple Functional Corticospinal Tractsmentioning

confidence: 71%

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

Chakrabarty¹,

Shulman²,

Martin³

2009

Journal of Neuroscience

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Corticospinal tract (CST) connections to spinal interneurons are conserved across species. We identified spinal interneuronal populations targeted by the CST in the cervical enlargement of the cat during development. We focused on the periods before and after laminar refinement of the CST terminations, between weeks 5 and 7. We used immunohistochemistry of choline acetyltransferase (ChAT), calbindin, calretinin, and parvalbumin to mark interneurons. We first compared interneuron marker distribution before and after CST refinement. ChAT interneurons increased, while calbindin interneurons decreased during this period. No significant changes were noted in parvalbumin and calretinin. We next used anterograde labeling to determine whether the CST targets different interneuron populations before and after the refinement period. Before refinement, the CST terminated sparsely where calbindin interneurons were located and spared ChAT interneurons. After refinement, the CST no longer terminated in calbindin-expressing areas but did so where ChAT interneurons were located. Remarkably, early CST terminations were dense where ChAT interneurons later increased in numbers. Finally, we determined whether corticospinal system activity was necessary for the ChAT and calbindin changes. We unilaterally inactivated M1 between weeks 5 and 7 by muscimol infusion. Inactivation resulted in a distribution of calbindin and ChAT in spinal gray matter regions where the CST terminates that resembled the immature more than mature pattern. Our results show that the CST plays a crucial role in restructuring spinal motor circuits during development, possibly through trophic support, and provide strong evidence for the importance of connections with key spinal interneuron populations in development of motor control functions.

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Section: Multiple Functional Corticospinal Tractsmentioning

confidence: 71%

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

Chakrabarty¹,

Shulman²,

Martin³

2009

Journal of Neuroscience

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“…There have been prior suggestions in cats, monkeys, and humans that the forelimb representation in M1 contains rostral and caudal subdivisions (25)(26)(27)(28)(29)(30). These subdivisions have been distinguished based on various features such as receptor binding, afferent inputs, motor outputs, patterns of activation, and the effects of lesions.…”

Section: Discussionmentioning

confidence: 99%

Subdivisions of primary motor cortex based on cortico-motoneuronal cells

Rathelot

Strick

2009

Proc. Natl. Acad. Sci. U.S.A.

511

462

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We used retrograde transneuronal transport of rabies virus from single muscles of rhesus monkeys to identify cortico-motoneuronal (CM) cells in the primary motor cortex (M1) that make monosynaptic connections with motoneurons innervating shoulder, elbow, and finger muscles. We found that M1 has 2 subdivisions. A rostral region lacks CM cells and represents an ''old'' M1 that is the standard for many mammals. The descending commands mediated by corticospinal efferents from old M1 must use the integrative mechanisms of the spinal cord to generate motoneuron activity and motor output. In contrast, a caudal region of M1 contains shoulder, elbow, and finger CM cells. This region represents a ''new'' M1 that is present only in some higher primates and humans. The direct access to motoneurons afforded by CM cells enables the newly recognized M1 to bypass spinal cord mechanisms and sculpt novel patterns of motor output that are essential for highly skilled movements.motor system ͉ movement ͉ rabies virus ͉ cerebral cortex ͉ spinal cord T he primary motor cortex (M1) is a major source of descending motor commands for voluntary movement. These commands originate, in part, from corticospinal (CST) neurons in cortical layer V, which have axons that descend to the spinal cord. CST neurons can be divided into 2 general types. One type has axons that terminate in the intermediate zone of the spinal cord, where they contact spinal interneurons. Some of these interneurons make connections with motoneurons and mediate part of the descending commands for movement. The second type of CST neuron has axons that terminate in the ventral horn of the spinal cord, where they make monosynaptic connections with motoneurons. These CST neurons are termed corticomotoneuronal (CM) cells. CM cells, because of their direct connection with motoneurons, are thought to have a special role in the generation and control of highly skilled movements (1). We used retrograde transneuronal transport of rabies virus from single muscles of the shoulder, elbow, and finger to define the overall distribution of CM cells in M1 of rhesus monkeys. Here, we report the surprising observation that CM cells are almost entirely restricted to a caudal region of M1. Thus, M1 can be anatomically subdivided into a region that has direct control over motor output and a separate region that influences motor output only indirectly through spinal cord mechanisms. ResultsLocation of CM Cells. In 2 rhesus monkeys, we injected virus into the spinodeltoid (SpD) muscle, which assists in retraction of the shoulder. In another 2 monkeys, we injected virus into the lateral head of the triceps (lTri), which assists in elbow extension [for experimental details of each animal, see supporting information (SI) Table S1]. We also include additional analyses of material from a prior study, in which we injected virus into 3 different intrinsic and extrinsic finger muscles (2). In all of these experiments, the survival time after virus injection was set to allow retrograde transneuronal trans...

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“…We made penetrations within the lateral portion of area 4␥ (Ghosh 1997;Hassler and Muhs-Clement 1964), a zone extending from about 2 mm caudal, 5 mm rostral, and 2 mm lateral to the cruciate sulcus. This is the forelimb representation (Armstrong and Drew 1985;Chakrabarty and Martin 2000;Keller 1993;Pappas and Strick 1981) and it projects densely to the cervical enlargement in kittens and adult cats (Ghosh 1997;Li and Martin 2000;Martin 1996). To ensure that we thoroughly explored the forelimb zone, in all experiments we examined the region until we encountered a consistent band of ineffective sites or nonforelimb sites, indicating the limits of excitable forelimb motor cortex.…”

Section: Icms Protocolmentioning

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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Differential spinal projections from the forelimb areas of the rostral and caudal subregions of primary motor cortex in the cat

Cited by 54 publications

References 53 publications

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

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

Subdivisions of primary motor cortex based on cortico-motoneuronal cells

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

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