Activity of neurons in putamen during active and passive movements of wrist

Abstract

Recent studies have shown that many neurons in the basal ganglia have patterns of activity that are closely related to various parameters of active movements of the arm. The topographical distribution of these cells suggests that they are influenced by afferents from primary motor and sensory areas of the cerebral cortex. Although there is abundant evidence that information from peripheral receptors is relayed to the basal ganglia, relatively little information is available on whether neurons related to active movement are influenced by peripheral inputs. The present study was undertaken to provide information on this problem by comparing responses of putamen neurons to active and passive movements of the wrist. Two monkeys were trained to place their hand in a manipulandum and actively extend and flex their wrist against opposing torque loads. Additionally, they were trained to accept 1) passive step displacements of the wrist by the experimenter, which were comparable in amplitude, duration, and velocity to active movements, and 2) brief rapid displacements generated by a pulse of torque applied to the manipulandum by a motor. An extensive electromyographic (EMG) study was made prior to unit recording to characterize patterns of muscle activity during active and passive movements. A sample of 82 neurons was isolated in the putamen on the basis of a phasic burst of spikes associated with active movement of the wrist. Most (80%) of these cells showed directionally specific responses. The onset latency of unit firing in 91% of the cells lagged behind the onset of EMG activity in forearm agonist muscles. Phasic unit discharge during active movement increased with increasing opposing torque loads in 59% of the sample. The rate-torque curves for most of these cells were curvilinear (plateau occurred at heavy torque loads), although some cells showed a linear relationship. A comparison of these neuronal activity patterns with EMG activity-torque curves suggests that most of the cells were related to activity in forearm muscles and not to activity in proximal or axial muscles. The functional significance of these findings is interpreted in light of recent physiological and anatomic studies of the basal ganglia. A substantial proportion (44%) of the units that were related to active wrist movements showed an excitatory response during passive step displacements of the wrist in the absence of phasic EMG activity.(ABSTRACT TRUNCATED AT 400 WORDS)

Loss of Lever Press-Related Firing of Rat Striatal Forelimb Neurons after Repeated Sessions in a Lever Pressing Task

“…Thus, the observed partial reductions in force and distance as a function of session number do not explain the absence of time-locked firing in later sessions. Furthermore, ϳ50% of striatal forelimb neurons are load-related (Crutcher and DeLong, 1984;Liles, 1985). This leaves only 50% of the estimated one-third of our sample (i.e., the neurons related to depression of the lever) in question, further restricting any explanatory power of this argument.…”

“…Therefore, declining force or distance could have contributed to the decline in S:B for only an estimated one-third of the neurons studied. Second, firing rates of load-related or distance-related striatal forelimb neurons are reduced, not eliminated by, reductions in force (Crutcher and DeLong, 1984b;Liles, 1985) or distance (Kimura, 1990) of forelimb movement. Thus, the observed partial reductions in force and distance as a function of session number do not explain the absence of time-locked firing in later sessions.…”

“…Although clearly "movement-related," their properties indicate certain dissociations from movement. Firing of most neurons (type IIb of Kimura, 1990) lags behind the onset of electromyogram (EMG) activity of arm muscles (Crutcher and DeLong, 1984b;Liles, 1985;Kimura, 1990), so that any major role in movement initiation is unlikely. The parameter most frequently correlated with firing is the direction of movement, but in half the cases, firing shows no relation to load (Crutcher and DeLong, 1984b;Liles, 1985;Alexander, 1987).…”

“…Firing of most neurons (type IIb of Kimura, 1990) lags behind the onset of electromyogram (EMG) activity of arm muscles (Crutcher and DeLong, 1984b;Liles, 1985;Kimura, 1990), so that any major role in movement initiation is unlikely. The parameter most frequently correlated with firing is the direction of movement, but in half the cases, firing shows no relation to load (Crutcher and DeLong, 1984b;Liles, 1985;Alexander, 1987). Firing also occurs during passive movement and cutaneous stimulation (Crutcher and DeLong, 1984a;Liles, 1985;West et al, 1990;Carelli and West, 1991).…”

“…The parameter most frequently correlated with firing is the direction of movement, but in half the cases, firing shows no relation to load (Crutcher and DeLong, 1984b;Liles, 1985;Alexander, 1987). Firing also occurs during passive movement and cutaneous stimulation (Crutcher and DeLong, 1984a;Liles, 1985;West et al, 1990;Carelli and West, 1991). These properties suggest a role in integrating signals involved in ongoing movement, such as somatosensory feedback and /or efference copy, transmitted via the corticostriatal system (Kato and Kimura, 1992).…”