The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and the frontal eye fields in owl monkeys

Abstract

Microstimulation and anatomical techniques were combined to reveal the organization and interhemispheric connections of motor cortex in owl monkeys. Movements of body parts were elicited with low levels of electrical stimulation delivered with microelectrodes over a large region of precentral cortex. Movements were produced from three physiologically defined cortical regions. The largest region, the primary motor field, M‐I, occupied a 4‐6mm strip of cortex immediately rostral to area 3a. M‐I represented body movements from tail to mouth in a grossly somatotopic mediolateral cortical sequence. Specific movements were usually represented at more than one location, and often at as many as six or seven separate locations within M‐I. Although movements related to adjoining joints typically were elicited from adjacent cortical sites, movements of nonadjacent joints also were produced by stimulation of adjacent sites. Thus, both sites producing wrist movements and sites producing shoulder movements were found next to sites producing digit movements. Movements of digits of the forepaw were evoked at several locations including a location rostral to or within cortex representing the face. Overall, the somatotopic organization did not completely correspond to previous concepts of M‐I in that it was neither a single topographic representation, nor two serial or mirror symmetric representations, nor a “nesting about joints” representation. Instead, M‐I is more adequately described as a mosaic of regions, each representing movements of a restricted part of the body, with multiple representations of movements that tend to be somatotopically related. A second pattern of representation of body movements, the supplementary motor area (SMA), adjoined the rostromedial border of M‐I. SMA represented the body from tail to face in a caudorostral cortical sequence, with the most rostral portion related to eye movements. Movements elicited, by near‐threshold levels of current were often restricted to a single muscle or joint, as in M‐I, and the same movement was sometimes multiply represented. Typically, more intense stimulating currents were required for evoking movements in. SMA than in M‐I. A third motor region, the frontal eye field (FEF), bordered the representation of eyelids and face in M‐I. Eye movements elicited from this cortex consisted of rapid horizontal and downward deviation of gaze into the contralateral visual hemifield. In five experiments, motor maps were obtained after frontal cortex of the opposite hemisphere had been multiply injected with horseradish peroxidase to reveal callosal connections. In these experiments, the frontal lobes were flattened, sectioned parallel to the surface, and treated for horseradish peroxidase. Electrode penetrations and previously placed microlesions were used to relate surface‐view patterns of callosal connections to the motor maps. Both SMA and FEF had dense and rather uniform distributions of callosal connections. M‐I had an uneven distribution of interhemispheric connections, with the rostral half of M‐I having generally more dense and evenly distributed connections than the caudal half. Within the caudal half of M‐I, sparse callosal connections were found in cortex related to distal forelimb and hindlimb movements. Two dense adjoining patches of terminations in the midportions of rostral and caudal halves of M‐I were both related to movements of the trunk and shoulder. While many of the multiple sites producing movements of the distal limbs were in cortex with sparse callosal connections, some were in cortex with moderate to dense callosal connections. Likewise, sites producing movements of proximal body parts were both in cortex with dense callosal connections and cortex with sparse callosal connections.