Brainstem and spinal projections of the deep cerebellar nuclei in the monkey, with observations on the brainstem projections of the dorsal column nuclei.
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Biomedical subjects
Publications and source records attributed to W T Thach.
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Conventional glass-coated Pt-Ir microelectrode technique was adapted for use in recording single unit activity in the cervical dorsal root ganglia of chronic awake behaving monkeys. The activity of one fully identified and four putative afferents from forearm muscle spindles was recorded as a trained monkey performed wrist movements, guided by a visual display, in pursuit tracking of slow predictable hold-ramp-hold target trajectories. Comparison of spindle afferent discharge with parent muscle EMG provided evidence of gamma fusimotor activity dissociated from the activity of homonymous a motoneurons. This appears to maintain a uniform pattern of afferent activity in the face of widely varying parent muscle activity.
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1. Monkeys were trained to grasp a rod movable in a horizontal arc (Fig. 1), and to hold the rod by angulation of the wrist in each of three positions (A,B, C). A maintained load was placed on the rod alternately to oppose flexion and extension. At a light signal, the monkey had to move to the next position in a prescribed sequence (ABCBABCBA, ETC.). The task was designed to dissociate, while holding in position, the following variables: 1) pattern of muscular activity in the forearm required to hold the wrist in position, determined by the direction of the load (flexor or extensor muscles); 2) position of the rod, and thus angulation of the wrist joint (A, B, and C); and 3) set for the direction of the intended next movement (flexor or extensor). These variables are subsequently referred to as MPAT, JPOS, and DSET, respectively. 2. After training, recordings were made of the EMG activity of muscles used in the task and of the discharge of single neurons in the motor cortex of the cerebrum and the interposed and dentate nuclei of the cerebellum. 3. While holding the wrist in position, EMG and interpositus behaved uniformly, with higher discharge frequency under load in one direction and lower discharge frequency under load in the opposite direction. This relation was relatively independent of the position held and of the direction of the intended next movement. Thus, interpositus and EMG both seemed best related to the MPAT variable, as opposed to JPOS and DSET variables. By contrast, neurons in motor cortex and in dentate fell into three categories: one category discharged in relation to the pattern of muscular activity (MPAT), a second to the position of the wrist (JPOS), and a third to the direction of the intended next movement (DSET). While MPAT neurons formed a distinct dissociated group, neurons that were best related to JPOS were often related to DSET, and vice versa. 4. A few of the MPAT neurons in interpositus and motor cortex were further studied by varying the magnitude (as well as the direction) of the loads. Both interpositus and motor cortex MPAT neurons changed firing frequency in relation to the magnitude of load, and though few neurons were thus studied, the relation seemed clearer for interpositus than for motor cortex. 5. Anatomically, the three types of neurons thus classified by firing pattern during the hold periods were intermixed in the arm area of motor cortex. In dentate and interpositus, those neurons thus related to the performance were localized to a narrow strip across the posterior part of both nuclei. Neurons apparently related to eye and drinking movements were located more posteriorly still, suggesting somatotopic representation.
Monkeys were trained to grasp a handle and move it in a horizontal arc to a central position by flexing or extending the wrist. A torque motor applied forces to the handle that switched at random intervals to alternately load flexor and extensor muscles. At each load switch, the handle was displaced transiently from the central position, and then moved back by the monkeys and held there steadily again. Recordings were made from cerebellar Purkinje cells (P-cells) whose simple spike (SS) activity was related to the task. The magnitude of one of the oppositely directed loads was then altered and the monkeys took about 12-100 trials with the novel load before performing as regularly as previously. During this period with one known and one novel load, some P-cells underwent increases in complex spike (CS) frequency at specific times after the load switch. This increased CS frequency would last for a similar number of trials as that taken by the monkey to adapt to the novel load before decreasing to near its previous level. Associated with the increased CS frequency ther were decreases in SS frequency that persisted after the CS frequency had decreased to near its previous level. These results are consistent with theoretical proposals that motor learning takes place in the cerebellum through changes in the strength of transmission of parallel fiber synapses on P-cells caused by the climbing fiber input. These results further suggest that climbing fiber firing causes a decrease in the strength of parallel fiber synapses.
The discharge of neurons in cerebellar dentate nucleus and cerebral motor cortex was recorded on alternate days in each of 3 monkeys in association with prompt arm movement in response to a light signal. The time of change of the discharge of each neuron in relation to arm movement was computed. The distributions of the time of change for cerebellum and cerebrum overlapped, but the cerebellar distribution was shifted slightly earlier.
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We have examined several different paradigms of adaptation and of "acquisition of skill"-skill defined as a movement specialized to meet a certain goal and gained through practice. In each paradigm, change occurs through trial-and-error performance. In some of the tasks, damage of cerebellar cortex impairs adaptation and not performance. The deficits in performance cannot explain the deficits in adaptation. In some of the tasks, the discharge of Purkinje cells and, by inference, the discharge of inferior olive cells and mossy fibers have occurred in a manner consistent with the Marr-Albus theory of motor learning. We extend the theory to show how parallel fibers could implement both the coordination of complex movements and the learning of new movements. The size of the response combinations would be proportionate to the length of parallel fibers. The mechanism proposed here would permit optimized complex movement behaviors to respond to specific behavioral contexts rapidly, stereotypically, and automatically. The mechanism would permit storage of many context-response couplings and many complex responses. The mechanism would permit privacy, individuality, and a large number of behavioral responses.