The Journal of Neuroscience, April 1997, 7(d): 101O-1 021 The Somatotopic Organization of the Supplementary Motor Area: lntracortical Microstimulation Mapping Andrew R. Mitz and Steven P. Wise Laboratory of Neurophysiology, National Institute of Mental Health, Bethesda, Maryland 20892 The somatotopic organization of the supplementary motor area @MA) is commonly held to consist of a rostrocaudal sequence of orofacial, forelimb, and hindlimb representa- tions. Recently, however, this somatotopy has been ques- tioned. Studies of regional cerebral blood flow in humans and the movements evoked by intracortical electrical stim- ulation in cynomolgus monkeys have been unable to reveal evidence of distinct orofacial, forelimb, and hindlimb rep- resentations rostrocaudally situated along the medial cortex of the hemisphere. Partly on the basis of those results, it has been suggested that the SMA functions as a nontopo- graphically organized “higher-order” motor center. The present study reexamines SMA organization by observing stimulation-evoked movements. The medial frontal cortex of 2 rhesus monkeys was mapped using a modified intra- cortical microstimulation technique. We observed a forelimb representation mainly on the medial surface of the hemi- sphere in both animals. Rostra1 or rostrolateral to the fore- limb representation, depending on the individual, we evoked orofacial movements (including eye movements). Hindlimb movements were evoked from tissue overlapping, but large- ly caudal to, the forelimb representation. Thus, we conclude that there is a clear rostrocaudal progression of orofacial, forelimb, and hindlimb movement representations in the SMA. Woolsey’s classic picture of supplementary motor area (SMA) somatotopy (Woolsey et al., 1952)hasbeenquestioned recently on the basis of both a regional cerebral blood flow study in humans(Orgogozo and Larsen, 1979) and a microstimulation study in monkeys(Macphersonet al., 1982a). In neither ofthose studies did the investigators observe any clear somatotopic or- ganization in the SMA. For example, Macpherson et al. found a “caudal concentration of hindlimb points” with micro- stimulation but concluded that their results “did not support Woolsey’s concept of a somatotopic rostrocaudal sequence of face, forelimb and hindlimb representation” (Macphersonet al., 1982a,p. 415). Despite the doubts raised by those recent microstimulation and blood flow studies, examination of neuronal discharge (Brinkman and Porter, 1979; Tanji and Kurata, 1982) and the Received June 20, 1986; revised Sept. 15, 1986; accepted Oct. 17, 1986. The authors thank William G. Benson for preparation of the histological ma- terial, and Dr. Robert E. Burke of the Laboratory of Neural Control for the use of his laboratory’s cell plotting system. Correspondence should be addressed to Andrew R. Mitz, Laboratory of Neu- rophysiology, NIH, Building 36, Room 2D10, Bethesda, MD 20892. Copyright 0 1987 Society for Neuroscience 0270-6474/87/041010-12$02.00/O pattern of corticocortical connections (Jones and Powell, 1969; Pandyaand V&nolo, 197 1; Kiinzle, 1978;Muakkassa and Strick, 1979; Godschalk et al., 1984) in various macaque species sup- port Woolsey’s view of somatotopy within the SMA. Further, the region of the SMA projecting to cervical spinal segments appears to be rostra1 to the region that projects to lumbar seg- ments (Murray and Coulter, 1981; cf. Macpherson et al., 1982a, b). However, the available data do not lead to unequivocal con- clusionsabout SMA topography. The anatomical studiescited above, with the exception of that of Godschalk et al., rely upon comparison of labeling or staining patterns among several in- dividuals in a species. Thus, it is possible to reject the anatomical evidence for SMA somatotopy on the grounds that comparing data from different individuals undermines conclusions about somatotopy, especiallyin sucha small cortical field. While the multiple label study of Godschalk et al. addresses the problem adequately from a technical perspective, relevant connectional data are reported only from 1 animal, and SMA topography wasneither the focus of their study nor wasit discussed in their report. As for physiologicalresults reporting somatotopy (Brink- man and Porter, 1979; Tanji and Kurata, 1982), these too have limitations that have allowed the adoption of a nontopographic model of SMA organization. The work of Brinkman and Porter did not include sufficient behavioral control to identify orofacial, hindlimb, and forelimb movements separately.Further, the ex- act location of their recording sites in relation to sulcal land- marks or cytoarchitectonic boundaries was inadequately pre- sented in their report. As for the work of Tanji and Kurata, since they did not systematically examine orofacial movements, their conclusionsconcerning somatotopy rested upon the dis- tinct location of neurons active before hindlimb movements and those active before forelimb movements. But the lack of a clear histological or physiological boundary between the hind- limb representationsof the primary motor cortex and SMA prevents the unequivocal identification of an SMA hindlimb representation necessary for their conclusion. It is presumablyfor the above reasons that the physiological and anatomical evidencefor SMA somatotopy has been rejected by prominent reviewers of the SMA literature (Eccles, 1982; Ecclesand Robinson, 1984; Wiesendanger and Wiesendanger, 1984; Wiesendanger, 1986).That view of the literature has con- tributed to the suggestion that the SMA functions as a nonto- pographically organized “supramotor” center (Orgogozo and Larsen, 1979;Eccles,1982;Eccles and Robinson, 1984).In view of the discrepancybetween classically accepted and more recent views of SMA organization, we decided to reinvestigatethe issue of SMA somatotopy with a method having different interpre- tational limitations than those previously applied.