Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements.

1. Previous studies have shown that midbrain dopamine (DA) neurons in monkeys respond to external stimuli that are used to initiate behavioral reactions. In the present study, we investigated to what extent changes in neuronal activity would occur when behavioral acts are generated internally or whether they would depend solely on external stimuli. 2. Monkeys performed self-initiated arm movements from a resting key into a covered, food-containing box at a self-chosen moment and without external preparatory or triggering signals. In a second task, the arm movement was triggered by rapid opening of the door of the food box. This stimulus was either audible and visible or only audible to the animal. Impulses of DA neurons were recorded with movable microelectrodes from the pars compacta of substantia nigra (area A9) and areas A8 and A10 and were discriminated from those of other neurons by their long duration (1.5-5.0 ms) and low spontaneous frequency (0.5-8.5 imp/s). 3. The activity of 12% of 104 DA neurons increased slowly and moderately up to 1,500 ms before the onset of individual self-initiated arm movements. Median increases amounted to 91% over background discharge rate. A further 16% of DA neurons were activated together with the onset of muscle activity and during the movement. 4. During self-initiated movements, a nonhabituating, phasic burst of impulses occurred when the monkey's hand touched a morsel of food inside the box. This response was seen in 84% of 154 neurons on the contralateral side, with median onset latency of 65 ms and duration of 160 ms. A comparable percentage of neurons responded to ipsilateral touch with similar latency and duration. 5. The touch response during self-initiated movements was absent, both on the contra- and ipsilateral sides, when the animal's hand touched the bare wire normally holding the food, when touching nonfood objects, or during tactile exploration of the empty interior of the food box. Thus responses appeared to be related to the appetitive properties of the object being touched rather than the object itself. 6. In the task employing stimulus-triggered movements, 77% of 86 DA neurons discharged a burst of impulses in response to door opening but entirely failed to respond to the touch of food in the box. The response to door opening in this task was similar to the touch response during self-initiated movements in the same neurons in terms of latency, duration, and magnitude.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  D. Bindra Neuropsychological interpretation of the effects of drive and incentive-motivation on general activity and instrumental behavior. , 1968 .

[2]  D. Bindra A motivational view of learning, performance, and behavior modification. , 1974, Psychological review.

[3]  O. Creutzfeldt,et al.  Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation. , 1977, Journal of neurophysiology.

[4]  G. Aghajanian,et al.  Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra , 1978, Brain Research.

[5]  N. A. Buchwald,et al.  Preparation for movement in the cat. II. Unit activity in the basal ganglia and thalamus. , 1978, Electroencephalography and clinical neurophysiology.

[6]  G. Arbuthnott,et al.  Electrophysiological evidence for an input from the anterior olfactory nucleus to substantia nigra , 1979, Experimental Neurology.

[7]  Shoji Nakamura,et al.  Inhibition of neuronal activity of the substantia nigra by noxious stimuli and its modification by the caudate nucleus , 1980, Brain Research.

[8]  W. Schultz,et al.  Dopaminergic activation of reticulata neurones in the substantia nigra , 1980, Nature.

[9]  J. Rehfeld,et al.  Peptide-monoamine coexistence: Studies of the actions of cholecystokinin-like peptide on the electrical activity of midbrain dopamine neurons , 1981, Neuroscience.

[10]  R. Wise Neuroleptics and operant behavior: The anhedonia hypothesis , 1982, Behavioral and Brain Sciences.

[11]  B. Jacobs,et al.  Behavioral correlates of dopaminergic unit activity in freely moving cats , 1983, Brain Research.

[12]  W. Schultz Neuronal processes involved in initiating a behavioral act , 1985, Behavioral and Brain Sciences.

[13]  B. Jacobs,et al.  Substantia nigra dopaminergic unit activity in behaving cats: Effect of arousal on spontaneous discharge and sensory evoked activity , 1985, Brain Research.

[14]  R. Romo,et al.  In vivo presynaptic control of dopamine release in the cat caudate nucleus—III. Further evidence for the implication of corticostriatal glutamatergic neurons , 1986, Neuroscience.

[15]  W. Schultz Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey. , 1986, Journal of neurophysiology.

[16]  W. Schultz,et al.  The catecholamine uptake inhibitor nomifensine depresses impulse activity of dopamine neurons in mouse substantia nigra , 1987, Neuroscience Letters.

[17]  W. Schultz,et al.  Responses of nigrostriatal dopamine neurons to high-intensity somatosensory stimulation in the anesthetized monkey. , 1987, Journal of neurophysiology.

[18]  W Schultz,et al.  Deficits in reaction times and movement times as correlates of hypokinesia in monkeys with MPTP-induced striatal dopamine depletion. , 1989, Journal of neurophysiology.

[19]  W. Schultz,et al.  Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. , 1990, Journal of neurophysiology.