Cited by 335Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesMotor Control and Adaptation

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

Schultz, W., Romo, R.·1990·Journal of Neurophysiology

DOI 10.1152/jn.1990.63.3.607

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Abstract

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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“…in the ventral tegmental area and substantia nigra of awake monkeys while they repeatedly performed an instrumental or Pavlovian conditioning task4 (Ljungberg, Apicella, & Schultz, 1992; Romo & Schultz, 1990; Schultz, Apicella, & Ljungberg, 1993; Schultz & Romo, 1990; Mirenowicz & Schultz, 1994).”
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Background
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“After being repeatedly paired with unconditioned appetitive stimuli, the neutral stimuli become predictive of reward and are able to elicit DA burst activity (Ljungberg et al., 1991, Mirenowicz and Schultz, 1996, Schultz and Romo, 1990).”
Background
Dopamine in Schizophrenia Dysfunctional Information Processing in Basal Ganglia — Thalamocortical Split Circuits
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“Electrophysiological studies in behaving animals (Schultz 1986, 1998; Kiaytkin 1988; Schultz and Romo 1990; Miller et al. 1991; Schultz et al. 1992) have shown that DA cells switch to burst firing following the occurrence of salient, novel, or reinforcing (unconditioned and conditioned) stimuli.”
Background
Reinforcement learning links spontaneous cortical dopamine impulses to reward
Foo, C., Lozada, A. F., Aljadeff, J., Li, Y., Wang, J. W., Slesinger, P. A., & Kleinfeld, D. (2021) · Current Biology · doi:10.1016/j.cub.2021.06.069 · Cited by 36
“Early studies showed that a fraction of dopaminergic neurons in the midbrain produce impulses of spiking activity in response to a novel stimulus, even one that is not associated with a reward.(27) Further, such impulses may occur as a precursor to self-generated motion.”
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A mismatch between striatal cholinergic pauses and dopaminergic reward prediction errors
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“Many DA neurons also show fast responses to salient events ( 46 , 62 ).”
In vivo analysis of the role of dopamine in stimulant and opiate self-administration.
Gratton, A. P. (1996) · PubMed · Cited by 34
Fluctuations in neural activity during cocaine self-administration: clues provided by brain thermorecording
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The Basal Ganglia
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The Psychobiology of Attention-Deficit/Hyperactivity Disorder
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Risk-taking bias in human decision-making is encoded via a right–left brain push–pull system
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The deep mesencephalic nucleus as an output center of basal ganglia: Morphological and electrophysiological similarities with the substantia nigra
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Environmental and behavioral modulation of the number of substantia nigra dopamine neurons in adult mice
Aumann, T. D., Tomas, D., & Horne, M. K. (2013) · Brain and Behavior · doi:10.1002/brb3.163 · Cited by 30
“SNc DA neurons burst in response to presentation of rewards and this burst shifts back in time to any cue that is associated by the animal to forthcoming rewards (i.e., to just before movement to retrieve a reward) (Schultz and Romo 1990; Schultz et al. 1997).”
Background
Reward Processing in the Brain: A Prerequisite for Movement Preparation?
Keitz, M., Martin-Söelch, C., & Leenders, K. L. (2003) · Neural Plasticity · doi:10.1155/np.2003.121 · Cited by 30
“Primate studies In the search for the neuronal organization of reward processing, Schultz and coworkers (Romo & Schultz, 1990; Schultz & Romo, 1990) used single-cell recordings in macaque monkeys.”
Background
Hippocampus and Prefrontal Cortex Predict Distinct Timescales of Activation in the Human Ventral Tegmental Area
Murty, V. P., Ballard, I. C., & Adcock, R. A. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw005 · Cited by 29
“The physiologyof dopamine neurons in the VTA ismodulated by at least 2 mechanisms: Direct excitation, which has mainly been demonstrated to contribute to phasic burst firing (Schultz and Romo 1990; Karreman and Moghaddam 1996; Kulagina © The Author 2016.”
Dopamine and deep brain stimulation accelerate the neural dynamics of volitional action in Parkinson's disease
Köhler, R. M., Binns, T. S., Merk, T., Zhu, G., Yin, Z., Zhao, B., Chikermane, M., Vanhoecke, J., Busch, J. L., Habets, J., et al. (2024) · Brain · doi:10.1093/brain/awae219 · Cited by 28
“27,28 Since then, dopamine research has often been focused on reward processing.”
Background
Neuronal activity in the substantia nigra in the anaesthetized rat has fractal characteristics. Evidence for firing-code patterns in the basal ganglia
Rodr�guez, M., Pereda, E., Gonz�lez, J., Abdala, P., & Obeso, J. A. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1442-4 · Cited by 27
“Since fractal behaviour has been described in visual and auditory neurons (Lowen and Teich 1996), and these sensory systems may influence SN cells (Schultz and Romo 1990), the experimental set up was prepared so as to minimize the effect of the environment on brain activity.”
Background
Nitric oxide facilitates N-methyl-d-aspartate-induced burst firing in dopamine neurons from rat midbrain slices
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Distributional coding of associative learning in discrete populations of midbrain dopamine neurons
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A “Good Parent” Function of Dopamine: Transient Modulation of Learning and Performance during Early Stages of Training
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Cognitive factors in addiction and nucleus accumbens function: Some hints from rodent models
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Predictable and unpredictable rewards produce similar changes in dopamine tone.
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Dynamic Changes of Tyrosine Hydroxylase and Dopamine Concentrations in the Ventral Tegmental Area-Nucleus Accumbens Projection During the Expression of Morphine-Induced Conditioned Place Preference in Rats
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“When animals are reexposed to natural reward-related cues, DA neurons are excited in the VTA [11, 27, 28], subsequently leading to DA release in the NAc [12, 29] without the presence of the reward.”
Background
Striatal direct pathway modulates response time in execution of visual discrimination
Fukabori, R., Okada, K., Nishizawa, K., Kai, N., Kobayashi, K., Uchigashima, M., Watanabe, M., Tsutsui, Y., & Kobayashi, K. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08005.x · Cited by 24
“In addition, electrophysiological studies indicated that midbrain dopamine neurons are activated by a sensory stimulus that predicts reward (Schultz & Romo, 1990; Ljungberg et al., 1991, 1992; Kawagoe et al., 2004).”
Background
The agranular and granular insula differentially contribute to gambling-like behavior on a rat slot machine task: effects of inactivation and local infusion of a dopamine D4 agonist on reward expectancy
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The Hidden Life of the Basal Ganglia
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On the Origins of Signal Variance in FMRI of the Human Midbrain at High Field
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Rehabilitative approaches to Parkinson's disease
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“However, during behavior, dopamine neurons increase their neuronal activity, and thus release dopamine, over a very limited time, in the order of tenths of seconds [5].”
Background

Authors: Schultz, W., & Romo, R.
Affiliations: University of Fribourg (CH)
ORCID: Schultz, W.
Romo, R.
Venue: Journal of Neurophysiology
Publisher: American Physiological Society
Published: 1990-03-01
Volume: 63
Issue: 3
Pages: 607-624
ISSN: 0022-3077 (ISSN-L)
1522-1598
DOI: 10.1152/jn.1990.63.3.607
OpenAlex: W2402721223
Cited by: 334
References: 0
Citations by year: 2026: 5 · 2025: 6 · 2024: 7 · 2023: 9 · 2022: 5 · 2021: 5 · 2020: 10 · 2019: 9 · 2018: 4 · 2017: 6 · 2016: 12 · 2015: 12 · 2014: 7 · 2013: 11 · 2012: 12
FWCI: 3.21
Type: journal article
Language: en
Open access: closed
Locations: Journal of Neurophysiology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Keywords: dopaminergic neurons, substantia nigra, midbrain, go/no-go task, saccades, arm movement
MeSH terms: Acoustic Stimulation, Action Potentials, Animals, Arm, Dopamine, Eye Movements, Functional Laterality, Macaca, Macaca fascicularis, Psychomotor Performance, Reaction Time, Substantia Nigra, Visual Pathways

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

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