Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions

1. This study investigates the behavioral conditions in which dopamine (DA) neurons of substantia nigra and adjoining areas A8 and A10 respond with impulses to visual and auditory trigger stimuli eliciting immediate arm- and eye-movement reactions. 2. In a formal task, the rapid opening of the door of a small, food-containing box located at eye level ahead of the animal served as visible and audible trigger stimulus. Most DA neurons on the contralateral side responded to this stimulus with a short burst of impulses with median onset latency of 50 ms and duration of 90 ms (75% of 164 neurons). Similar responses were seen in a comparable fraction of DA neurons during ipsilateral task performance, suggesting that responses were not specific for the limb being used. 3. When the sensory components of the door opening stimulus were separated, DA neurons typically responded in a similar manner to the moving visual stimulus of the opening door, the low-intensity sliding noise of the opening door, and the 1-kHz sound of 90-92 dB intensity emitted from a distant source at the onset of door opening. Responses to each component alone were lower in magnitude than to all three together. 4. In a variation of the task, a neighboring, identical food box opened in random alternation with the other box but without permitting animals to reach out (asymmetric, direct-reaction go/no-go task). With each sensory component, DA neurons typically responded both to opening of go and no-go boxes. Responses were enhanced when stimuli elicited limb movements in go trials. 5. Monkeys reacted to door opening with target-directed saccadic eye movements in the majority of both go and no-go trials. Neuronal responses were equally present during the occasional absence of eye movements. Thus responses were not specific for the initiation of individual arm or eye movements. 6. Neuronal responses were absent when the same stimuli occurred outside of the behavioral task with target-direct arm and eye movements lacking. This shows that responses were not of purely sensory nature but were related to the capacity of the stimulus for eliciting behavioral reactions. 7. In a variation of the go/no-go task, an instruction light illuminated 2-3 s before door opening prepared the animal to perform the reaching movement on door opening or to refrain from moving (asymmetric, instruction-dependent go/no-go task).(ABSTRACT TRUNCATED AT 400 WORDS)

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Responses of monkey dopamine neurons during learning of behavioral reactions

Journal of Neurophysiology ◽

10.1152/jn.1992.67.1.145 ◽

1992 ◽

Vol 67 (1) ◽

pp. 145-163 ◽

Cited By ~ 563

Author(s):

T. Ljungberg ◽

P. Apicella ◽

W. Schultz

Keyword(s):

Saccadic Eye Movements ◽

Stimulus Presentation ◽

Dopamine Neurons ◽

Neuronal Responses ◽

Behavioral Reactions ◽

Reaching Movement ◽

Door Opening ◽

Long Duration ◽

Spontaneous Frequency ◽

Unexpected Stimulus

1. Previous studies have shown that dopamine (DA) neurons respond to stimuli of behavioral significance, such as primary reward and conditioned stimuli predicting reward and eliciting behavioral reactions. The present study investigated how these responses develop and vary when the behavioral significance of stimuli changes during different stages of learning. Impulses from DA neurons were recorded with movable microelectrodes from areas A8, A9, and A10 in two awake monkeys during the successive acquisition of two behavioral tasks. Impulses of DA neurons were distinguished from other neurons by their long duration (1.8-5.0 ms) and low spontaneous frequency (0.5-7.0 imp/s). 2. In the first task, animals learned to reach in a small box in front of them when it opened visibly and audibly. Before conditioning, DA neurons were activated the first few times that the empty box opened and animals reacted with saccadic eye movements. Neuronal and behavioral responses disappeared on repeated stimulus presentation. Thus neuronal responses were related to the novelty of an unexpected stimulus eliciting orienting behavior. 3. Subsequently, the box contained a small morsel of apple in one out of six trials. Animals reacted with ocular saccades to nearly every box opening and reached out when the morsel was present. One-third of 49 neurons were phasically activated by every door opening. The response was stronger when food was present. Thus DA neurons responded simultaneously to the sight of primary food reward and to the conditioned stimulus associated with reward. 4. When the box contained a morsel of apple on every trial, animals regularly reacted with target-directed eye and arm movements, and the majority of 76 DA neurons responded to door opening. The same neurons lacked responses to a light not associated with task performance that was illuminated at the position of the food box in alternate sessions, thus demonstrating specificity for the behavioral significance of stimuli. 5. The second task employed the operant conditioning of a reaction time situation in which animals reached from a resting key toward a lever when a small light was illuminated. DA neurons lacked responses to the unconditioned light. During task acquisition lasting 2-3 days, one-half of 25 DA neurons were phasically activated when a drop of liquid reward was delivered for reinforcing the reaching movement. In contrast, neurons were not activated when reward was delivered at regular intervals (2.5-3.5 s) but a task was not performed.(ABSTRACT TRUNCATED AT 400 WORDS)

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Amplitude and Direction of Saccadic Eye Movements Depend on the Synchronicity of Collicular Population Activity

Journal of Neurophysiology ◽

10.1152/jn.00639.2003 ◽

2004 ◽

Vol 92 (1) ◽

pp. 424-432 ◽

Cited By ~ 20

Author(s):

Michael Brecht ◽

Wolf Singer ◽

Andreas K. Engel

Keyword(s):

Eye Movements ◽

Saccadic Eye Movements ◽

Brain Structures ◽

High Temporal Resolution ◽

Temporal Relations ◽

Neuronal Responses ◽

Population Activity ◽

Neuronal Processing ◽

The Individual ◽

Cat Superior Colliculus

Synchronization of neuronal discharges has been observed in numerous brain structures, but opinions diverge regarding its significance in neuronal processing. Here we investigate whether the motion vectors of saccadic eye movements evoked by electrical multisite stimulation of the cat superior colliculus (SC) are influenced by varying the degree of synchrony between the stimulus trains. With synchronous activation of SC sites, the vectors of the resulting saccades correspond approximately to the averages of the vectors of saccades evoked from each site alone. In contrast, when the pulses of trains applied to the different sites are temporally offset by as little as 5–10 ms, the vectors of the resulting saccades come close to the sum of the individual vectors. Thus saccade vectors depend not only on the site and amplitude of collicular activation but also on the precise temporal relations among the respective spike trains. These data indicate that networks within or downstream from the SC discriminate with high temporal resolution between synchronous and asynchronous population responses. This supports the hypothesis that information is encoded not only in the rate of neuronal responses but also in the precise temporal relations between discharges.

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Effects of eye position on saccadic eye movements and on the neuronal responses to auditory and visual stimuli in cat superior colliculus

Experimental Brain Research ◽

10.1007/bf00231709 ◽

1995 ◽

Vol 103 (2) ◽

Cited By ~ 37

Author(s):

CarolK. Peck ◽

JohnA. Baro ◽

StephanieM. Warder

Keyword(s):

Eye Movements ◽

Superior Colliculus ◽

Visual Stimuli ◽

Saccadic Eye Movements ◽

Eye Position ◽

Neuronal Responses ◽

Cat Superior Colliculus

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

Journal of Neurophysiology ◽

10.1152/jn.1990.63.3.592 ◽

1990 ◽

Vol 63 (3) ◽

pp. 592-606 ◽

Cited By ~ 207

Author(s):

R. Romo ◽

W. Schultz

Keyword(s):

Discharge Rate ◽

Arm Movements ◽

Arm Movement ◽

Contralateral Side ◽

Dopamine Neurons ◽

Door Opening ◽

Touch Response ◽

Midbrain Dopamine ◽

Spontaneous Frequency ◽

External Stimuli

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)

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Modification of saccadic eye movements by GABA-related substances. I. Effect of muscimol and bicuculline in monkey superior colliculus

Journal of Neurophysiology ◽

10.1152/jn.1985.53.1.266 ◽

1985 ◽

Vol 53 (1) ◽

pp. 266-291 ◽

Cited By ~ 381

Author(s):

O. Hikosaka ◽

R. H. Wurtz

Keyword(s):

Eye Movements ◽

Superior Colliculus ◽

Injection Site ◽

Saccadic Eye Movements ◽

Contralateral Side ◽

Slow Phase ◽

Gamma Aminobutyric Acid ◽

Affected Area ◽

Related Substances ◽

Movement Field

Our previous observations led to the hypothesis that cells in the substantia nigra pars reticulata (SNr) tonically inhibit saccade-related cells in the intermediate layers of the superior colliculus (SC). Before saccades to visual or remembered targets, cells in SNr briefly reduce that inhibition, allowing a burst of spikes of SC cells that, in turn, leads to the initiation of a saccadic eye movement. Since this inhibition is likely to be mediated by gamma-aminobutyric acid (GABA), we tested this hypothesis by injecting a GABA agonist (muscimol) or a GABA antagonist (bicuculline) into the superior colliculus and measured the effects on saccadic eye movements made to visual or remembered targets. An injection of muscimol selectively suppressed saccades to the movement field of the cells near the injection site. The affected area expanded over time, thus suggesting the diffusion of muscimol in the SC; the area never included the other hemifield, suggesting that the diffusion was limited to one SC. One of the monkeys became unable to make any saccades to the affected area. Saccades to visual targets following injection of muscimol had longer latency and slightly shorter amplitudes that were corrected by subsequent saccades. The most striking change was a decrease in the peak velocity of the saccade, frequently to less than half the preinjection value. Saccades to remembered targets following injection of muscimol also showed an increase in latency and decrease in velocity, but in addition, showed a striking decrease in the accuracy of the saccades. The trajectories of saccades became distorted as if they were deflected away from the affected area. After muscimol injection, the area over which spontaneous eye movements were made shifted toward the side ipsilateral to the injection. Saccades toward the contralateral side were less frequent and slower. In nystagmus, which developed later, the slow phase was toward the contralateral side. In contrast to muscimol, injection of bicuculline facilitated the initiation of saccades. Injection was followed almost immediately by stereotyped and apparently irrepressible saccades made toward the center of the movement field of the SC cells at the injection site. The monkeys became unable to fixate during the tasks; the fixation was interrupted by saccadic jerks made to the affected area of the visual field and then back to the fixation point.(ABSTRACT TRUNCATED AT 400 WORDS)

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