366
Brain Research, i 54 (1978) 366~ ~70 i ) Elsevier/North-Holland Biomedical P,-ess
Multiple representation in the primate motor cortex
P E T E R L. STRICK and JAMES B. PRESTON Research Service, Veterans Administration and Departments oj Neurosurgery and Physh~togy, Ispsrate Medical Center. Syracuse, N. Y. ( U. S. A. (Accepted May 18th, 1978)
The classical view of somatotopic organization in the motor cortex is that a single continuous representation of body parts exists within the primary motor area. This concept of cortical representation was derived from studies in a variety of species including man, in which movements were evoked following cortical surface stimulation a~, 15,16
Woolsey et al. summarized their findings by portraying the representation in primary motor cortex as a distorted map o f the body parts in which each part had a single representation. However, they were quick to note that such a diagram did not completely represent their findings 'since in a line drawing one cannot indicate the successive overlap which is so characteristic a feature of cortical representation' (see p. 252) 16. A number of models have been proposed in an attempt to better describe the fine structure of motor cortex output 1,3,4,6, s,9, r~. It occurred to us that multiple representations of a body part might be buried within the 'successive overlap" observed in these earlier studies. This concept of cortical organization finds support from recent studies which have challenged the classical concept of a single sensory representation within the primary somatosensory cortex 1° In order to explore the possibility that multiple representations exist within area 4, we elected to map the arm area of the primary motor cortex in the squirrel monkey using intracortical microstimulation 4. We chose the squirrel monkey because none of the arm or hand m o t o r representation is buried within a sulcus in this primate 13. The results of our experiments demonstrate that the wrist and hand are represented twice in area 4. Squirrel monkeys fSaimiri sciureusJ were anesthetized with 10 mg/kg ketamine hydrogen chloride given intramuscularly and 25 mg/kg ofpentobarbitat sodium given intraperitoneally. Supplemental i.m doses of ketamine hydrogen chloride were given as needed to maintain anesthesia. A plastic cylinder was fixed over the forelimb area of the motor cortex. The cylinder was filled with warm mineral oil and formed the base of a closed chamber system 5. The m o t o r cortex was mapped using intracortical microstimulation to evoke movements of the contralateral forelimb. Glass coated, platinum-iridium micro-
367 electrodes with impendances of 0.7 to 1.5 M ~ were driven into the motor cortex approximately perpendicular to its surface. As in the Cebus monkey a, the lowest threshold points for evoking muscle contractions were located approximately 1.5 mm below the surface of the cortex. Histology has confirmed this depth to be within the Betz cell layer. Stimulation consisted of a 50-60 msec cathodal pulse train delivered at a frequency of 300-400 Hz with a pulse duration of 0.2 msec. Thresholds for evoking movements varied between 1.0 and 25/~A (in most cases below I0 #A). The effects of microstimulation were determined by muscle palpation, visual inspection, and in some cases verified by E M G recording. Microstimulation in area 4, in the region rostral to area 3a, evoked movements of the hand (thumb and fingers). A zone from which predominately wrist and radioulnar joint movements were evoked (wrist flexion and extension, wrist ulnar and radial deviation, and forearm supination and pronation) was found just rostral to the hand zone. Rostral to this wrist zone there was an abrupt transition to a zone from which thumb and finger movements were once again evoked. The presence of this second zone of hand representation in area 4 does not conform to the classical viewpoint of motor cortex representation. Although classical maps of the motor cortex demonstrate some overlap in the representation of body partsa'5, t6, the basic pattern is one in which movements of more proximal portions of the limb are evoked from points rostral to a single area of hand representation. Thus, in contrast to maps derived from surface stimulation, our microstimulation studies have demonstrated a discrete second representation for the hand. Furthermore, immediately rostral to the second hand zone lies another zone in which movements of the wrist and radioulnarjoint are again evoked. Low intensity microstimulation did not evoke additional hand movements rostral to this second wrist representation. We will call the hand and wrist zones nearest the central fissure the caudal representation and the second hand and wrist zones, which are more remote from the central fissure, the rostral representation. In general the same muscles were activated at similar threshold currents in both representations. Histological analysis of the sites of lesions marking both caudal and rostral representations demonstrated that both were located in area 4. Fig. 1 illustrates some of our findings. Figure IA depicts an oblique view of the left hemisphere of the squirrel monkey. The parallelogram outlined on the cortical surface (labeled B) represents a segment of area 4. Located within this segment is the center of the hand-wrist region, as well as the transition between caudal and rostral representations. The line of transition between the two representations was 4 mm from the central fissure in the animal illustrated. In 4 other animals the line of transition was located from 3.7 to 4.2 mm rostral to the central fissure. Fig. 1B is an enlarged view of the parallelogram labeled B in Fig. I A. Each symbol shows the site of one microelectrode penetration made in this 2 >
Brain Research, i 54 (1978) 366~ ~70 i ) Elsevier/North-Holland Biomedical P,-ess
Multiple representation in the primate motor cortex
P E T E R L. STRICK and JAMES B. PRESTON Research Service, Veterans Administration and Departments oj Neurosurgery and Physh~togy, Ispsrate Medical Center. Syracuse, N. Y. ( U. S. A. (Accepted May 18th, 1978)
The classical view of somatotopic organization in the motor cortex is that a single continuous representation of body parts exists within the primary motor area. This concept of cortical representation was derived from studies in a variety of species including man, in which movements were evoked following cortical surface stimulation a~, 15,16
Woolsey et al. summarized their findings by portraying the representation in primary motor cortex as a distorted map o f the body parts in which each part had a single representation. However, they were quick to note that such a diagram did not completely represent their findings 'since in a line drawing one cannot indicate the successive overlap which is so characteristic a feature of cortical representation' (see p. 252) 16. A number of models have been proposed in an attempt to better describe the fine structure of motor cortex output 1,3,4,6, s,9, r~. It occurred to us that multiple representations of a body part might be buried within the 'successive overlap" observed in these earlier studies. This concept of cortical organization finds support from recent studies which have challenged the classical concept of a single sensory representation within the primary somatosensory cortex 1° In order to explore the possibility that multiple representations exist within area 4, we elected to map the arm area of the primary motor cortex in the squirrel monkey using intracortical microstimulation 4. We chose the squirrel monkey because none of the arm or hand m o t o r representation is buried within a sulcus in this primate 13. The results of our experiments demonstrate that the wrist and hand are represented twice in area 4. Squirrel monkeys fSaimiri sciureusJ were anesthetized with 10 mg/kg ketamine hydrogen chloride given intramuscularly and 25 mg/kg ofpentobarbitat sodium given intraperitoneally. Supplemental i.m doses of ketamine hydrogen chloride were given as needed to maintain anesthesia. A plastic cylinder was fixed over the forelimb area of the motor cortex. The cylinder was filled with warm mineral oil and formed the base of a closed chamber system 5. The m o t o r cortex was mapped using intracortical microstimulation to evoke movements of the contralateral forelimb. Glass coated, platinum-iridium micro-
367 electrodes with impendances of 0.7 to 1.5 M ~ were driven into the motor cortex approximately perpendicular to its surface. As in the Cebus monkey a, the lowest threshold points for evoking muscle contractions were located approximately 1.5 mm below the surface of the cortex. Histology has confirmed this depth to be within the Betz cell layer. Stimulation consisted of a 50-60 msec cathodal pulse train delivered at a frequency of 300-400 Hz with a pulse duration of 0.2 msec. Thresholds for evoking movements varied between 1.0 and 25/~A (in most cases below I0 #A). The effects of microstimulation were determined by muscle palpation, visual inspection, and in some cases verified by E M G recording. Microstimulation in area 4, in the region rostral to area 3a, evoked movements of the hand (thumb and fingers). A zone from which predominately wrist and radioulnar joint movements were evoked (wrist flexion and extension, wrist ulnar and radial deviation, and forearm supination and pronation) was found just rostral to the hand zone. Rostral to this wrist zone there was an abrupt transition to a zone from which thumb and finger movements were once again evoked. The presence of this second zone of hand representation in area 4 does not conform to the classical viewpoint of motor cortex representation. Although classical maps of the motor cortex demonstrate some overlap in the representation of body partsa'5, t6, the basic pattern is one in which movements of more proximal portions of the limb are evoked from points rostral to a single area of hand representation. Thus, in contrast to maps derived from surface stimulation, our microstimulation studies have demonstrated a discrete second representation for the hand. Furthermore, immediately rostral to the second hand zone lies another zone in which movements of the wrist and radioulnarjoint are again evoked. Low intensity microstimulation did not evoke additional hand movements rostral to this second wrist representation. We will call the hand and wrist zones nearest the central fissure the caudal representation and the second hand and wrist zones, which are more remote from the central fissure, the rostral representation. In general the same muscles were activated at similar threshold currents in both representations. Histological analysis of the sites of lesions marking both caudal and rostral representations demonstrated that both were located in area 4. Fig. 1 illustrates some of our findings. Figure IA depicts an oblique view of the left hemisphere of the squirrel monkey. The parallelogram outlined on the cortical surface (labeled B) represents a segment of area 4. Located within this segment is the center of the hand-wrist region, as well as the transition between caudal and rostral representations. The line of transition between the two representations was 4 mm from the central fissure in the animal illustrated. In 4 other animals the line of transition was located from 3.7 to 4.2 mm rostral to the central fissure. Fig. 1B is an enlarged view of the parallelogram labeled B in Fig. I A. Each symbol shows the site of one microelectrode penetration made in this 2 >
