Afferent and efferent connections of the dorsolateral precentral gyrus (area 4, hand/arm region) in the macaque monkey, with comparisons to area 8

The afferent and efferent connections of the dorsolateral precentral gyrus, the primary motor cortex for control of the upper extremity, were studied by using the retrograde and anterograde capabilities of the horseradish peroxidase (HRP) technique in three adult macaque monkey that had received HRP gel implants in this cortical region. Reciprocal corticocortical connections were observed primarily with the supplementary motor area (SMA) in medial premotor area 6 and dorsal bank of the cingulate sulcus, postarcuate area 6 cortex, dorsal cingulate cortex (area 24), superior parietal lobule (area 5, PE/PEa), and inferior parietal lobule (area 7b, PF/PFop, including the secondary somatosensory SII region). In these heavily labeled regions, the associationl intrahemispheric afferents originated primarily from small and medium sized pyramidal cells in layer III, but also from layer V. The SMA projections were columnar in organization. Intrahemispheric afferents from contralateral homologous and nonhomologous frontal and cingulate cortices also originated predominatly from layer III, but the connections from contralateral area 4 were almost exclusively from layer III. The bilateral connections with premotor frontal area 6 and cingulate cortices were not observed with parietal regions; i.e., only ipsilateral intrahemispheric parietal corticocortical connections were observed. There were no significant connections with prearcuate area 8 or the granular frontal (prefrontal) cortex. Subcortical afferents originated primarily from the nucleus basalis of Meynert, dorsal claustrum, ventral lateral (VLo and VLc), area X, ventral posterolateral pars oralis (VPLo), central lateral and centromedian thalamic nuclei, lateral hypothalamus, pedunculopontine nucleus, locus ceruleus and subceruleus, and superior central and dorsal raphe nuclei. Lesser numbers of retrogradely labeled neurons were observed in the nucleus of the diagonal band, mediodorsal (MD), paracentral, and central superior lateral thalamic nuclei, nucleus limitans, nucleus annularis, and the mesencephalic and pontine reticular formation. Subcortical efferent projections were observed to be almost exclusively ipsilateral to the putamen, dorsal claustrum, VL/X/VPLo, central lateral (CL) and centromedian (CM) thalamic nuclei, thalamic reticular nucleus, paralaminar MD, nucleus of the posterior commissure extending into the lateral intermediate superior colliculus, nucleus of Darkschewitsch, parvicellular and magnocellular red nucleus, lateral subthalamic nucleus, pedunculopontine nucleus, peduncular nucleus of the basilar pontine gray, nucleus reticularis tegmenti pontis, and to the mesencephalic, pontine, and medullary reticular formation. There was a bilateral projection to the lateral reticular nucleus and to a lesser extent to the inferior olivary nucleus, and the possibility of light projections to the cuneate and medial vestibular nuclei and to the nucleus intercalatus above the hypoglossal nucleus. Projections to the cervical spinal cord terminated primarily in contralateral laminae VII and IX and to a lesser extent to the ipsilateral medial ventral horn. The connections are discussed in terms of their possible role in voluntary movements of the upper extremity and are compared to previous studies of the connections of prefrontal cortex and frontal eye field (area 8), a primary oculomotor region, in an effort to better understand the anatomical basis for the coordination of hand and eye movements.