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, 103 (21), 8257-62

Muscle Representation in the Macaque Motor Cortex: An Anatomical Perspective

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Muscle Representation in the Macaque Motor Cortex: An Anatomical Perspective

Jean-Alban Rathelot et al. Proc Natl Acad Sci U S A.

Abstract

How are the neurons that directly influence the motoneurons of a muscle distributed in the primary motor cortex (M1)? To answer this classical question we used retrograde transneuronal transport of rabies virus from single muscles of macaques. This enabled us to define cortico-motoneuronal (CM) cells that make monosynaptic connections with the motoneurons of the injected muscle. We examined the distribution of CM cells that project to motoneurons of three thumb and finger muscles. We found that the CM cells for these digit muscles are restricted to the caudal portion of M1, which is buried in the central sulcus. Within this region of M1, CM cells for one muscle display a remarkably widespread distribution and fill the entire mediolateral extent of the arm area. In fact, CM cells for digit muscles are found in regions of M1 that are known to contain the shoulder representation. The cortical territories occupied by CM cells for different muscles overlap extensively. Thus, we found no evidence for a focal representation of single muscles in M1. Instead, the overlap and intermingling among the different populations of CM cells may be the neural substrate to create a wide variety of muscle synergies. We found two additional surprising results. First, 15-16% of the CM cells originate from area 3a, a region of primary somatosensory cortex. Second, the size range of CM cells includes both "fast" and "slow" pyramidal tract neurons. These observations are likely to lead to dramatic changes in views about the function of the CM system.

Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.
Fig. 1.
Retrograde transneuronal transport of rabies virus from single muscles. When rabies virus is injected into a single digit muscle, it is transported in the retrograde direction to infect the motoneurons (i.e., first-order neurons) that innervate the muscle. Then virus is transported transneuronally in the retrograde direction to label all those second-order neurons that synapse on the infected motoneurons. These include dorsal root ganglion cells that supply group Ia muscle spindle afferents, spinal cord interneurons, and cortical neurons in layer V (CM cells). At longer survival times, virus can undergo another stage of retrograde transneuronal transport and label all those third-order neurons that synapse on the infected second-order neurons. For example, virus can move from second-order neurons in layer V to third-order neurons in layer III. Similarly, virus can move from second-order interneurons in the spinal cord to third-order cortical neurons in layer V. DRG, dorsal root ganglion cell; Int, interneuron; Mn, motoneuron; 1, first-order neuron; 2, second-order neuron; 3, third-order neuron.
Fig. 2.
Fig. 2.
CM cells infected with rabies. (A) CM cells in layer V labeled by retrograde transneuronal transport of rabies from an injection of virus into ADP. Dotted lines indicate the borders between cortical layers. (B) CM cells of different size in layer V taken from the box in A. Arrows indicate the location of lightly labeled neurons.
Fig. 3.
Fig. 3.
Maps of CM cells that innervate the motoneurons for digit muscles. Each panel displays flattened maps of CM cells (small round symbols) labeled after injections of rabies into ADP (JA25), ABPL (JA30), or EDC (JA3). See Fig. 7 and ref. for details about the construction of these maps. Small arrows are placed at the area 4/6 border and the area 4/3a border. ArS, arcuate sulcus; CS, central sulcus; M, medial; R, rostral; SPcS, superior precentral sulcus.
Fig. 4.
Fig. 4.
Maps of cortical stimulation and maps of CM cells. (A) Finger representation. The small filled circles indicate sites where intracortical stimulation evoked finger movements. The size of a circle is inversely related to the threshold for evoking movement (see the key at the lower right). The solid line at the right is the bottom of the central sulcus. Vertical dashed lines mark various borders. The large dashed circle surrounds a medial region containing the lowest threshold sites for shoulder movements (see B). (B) Shoulder representation. The small filled circles indicate sites where intracortical stimulation evoked shoulder movements. (C) Location of CM cells innervating digit motoneurons. The results from injections of rabies virus into ADP (Fig. 3 Top) and into EDC (Fig. 3 Bottom) have been overlapped to create this figure. Note that the most medial CM cells for digit muscles are located in a region where stimulation evoked shoulder movements at low threshold (dashed circle). The scale for all maps is shown in C. [Reproduced with permission from Kwan et al. (19) (Copyright 1978, American Physiological Society).]
Fig. 5.
Fig. 5.
Size of CM cells. The graphs show the size of CM cells in M1 labeled after virus transport from ADP (Top), ABPL (Middle), and EDC (Bottom). Cell size in these graphs represents the average of a cell's maximum and minimum diameter (see Methods for details).

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