Reports

Uniform Inhibition of Dopamine Neurons in the Ventral Tegmental Area by Aversive Stimuli

Mark A. Ungless,^* Peter J. Magill, J. Paul Bolam

Dopamine neurons play a key role in reward-related behaviors. Reward coding theories predict that dopamine neurons will be inhibited by or will not respond to aversive stimuli. Paradoxically, between 3 and 49% of presumed dopamine neurons are excited by aversive stimuli. We found that, in the ventral tegmental area of anesthetized rats, the population of presumed dopamine neurons that are excited by aversive stimuli is actually not dopaminergic. The identified dopamine neurons were inhibited by the aversive stimulus. These findings suggest that dopamine neurons are specifically excited by reward and that a population of nondopamine neurons is excited by aversive stimuli.

Medical Research Council Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford OX1 3TH, UK.

^* Present address: Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.

To whom correspondence should be addressed. E-mail: mark.ungless{at}zoo.ox.ac.uk

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Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations.

J. Mena-Segovia, H. M. Sims, P. J. Magill, and J. P. Bolam (2008)
J. Physiol. 586, 2947-2960
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BOLD Responses Reflecting Dopaminergic Signals in the Human Ventral Tegmental Area.

K. D'Ardenne, S. M. McClure, L. E. Nystrom, and J. D. Cohen (2008)
Science 319, 1264-1267
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Performance Monitoring in the Anterior Cingulate is Not All Error Related: Expectancy Deviation and the Representation of Action-Outcome Associations..

F. T. P. Oliveira, J. J. McDonald, and D. Goodman (2007)
J. Cogn. Neurosci. 19, 1994-2004
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Functional Coupling between the Prefrontal Cortex and Dopamine Neurons in the Ventral Tegmental Area.

M. Gao, C.-L. Liu, S. Yang, G.-Z. Jin, B. S. Bunney, and W.-X. Shi (2007)
J. Neurosci. 27, 5414-5421
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A "Good Parent" Function of Dopamine: Transient Modulation of Learning and Performance during Early Stages of Training.

J. C. HORVITZ, W. Y. CHOI, C. MORVAN, Y. EYNY, and P. D. BALSAM (2007)
Ann. N.Y. Acad. Sci. 1104, 270-288
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The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons?.

E. B. Margolis, H. Lock, G. O. Hjelmstad, and H. L. Fields (2006)
J. Physiol. 577, 907-924
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Physiological Properties of Zebra Finch Ventral Tegmental Area and Substantia Nigra Pars Compacta Neurons.

S. D. Gale and D. J. Perkel (2006)
J Neurophysiol 96, 2295-2306
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Representation and Timing in Theories of the Dopamine System.

N. D. Daw, A. C. Courville, and D. S. Touretzky (2006)
Neural Comput. 18, 1637-1677
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No Effect of Morphine on Ventral Tegmental Dopamine Neurons during Withdrawal.

F. Georges, C. L. Moine, and G. Aston-Jones (2006)
J. Neurosci. 26, 5720-5726
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Differential Effects of Cocaine on Firing Rate and Pattern of Dopamine Neurons: Role of {alpha}1 Receptors and Comparison with L-Dopa and Apomorphine.

Y. Zhou, B. S. Bunney, and W.-X. Shi (2006)
J. Pharmacol. Exp. Ther. 317, 196-201
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Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location..

C. P. Ford, G. P. Mark, and J. T. Williams (2006)
J. Neurosci. 26, 2788-2797
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{kappa} opioids selectively control dopaminergic neurons projecting to the prefrontal cortex.

E. B. Margolis, H. Lock, V. I. Chefer, T. S. Shippenberg, G. O. Hjelmstad, and H. L. Fields (2006)
PNAS 103, 2938-2942
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Perturbation of the activity of a single identified neuron affects long-term memory formation in a molluscan semi-intact preparation.

M. R. Lowe and G. E. Spencer (2006)
J. Exp. Biol. 209, 711-721
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Slow Oscillatory Firing: A Major Firing Pattern of Dopamine Neurons in the Ventral Tegmental Area.

W.-X. Shi (2005)
J Neurophysiol 94, 3516-3522
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A Comparison of Visceral and Somatic Pain Processing in the Human Brainstem Using Functional Magnetic Resonance Imaging.

P. Dunckley, R. G. Wise, M. Fairhurst, P. Hobden, Q. Aziz, L. Chang, and I. Tracey (2005)
J. Neurosci. 25, 7333-7341
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How Visual Stimuli Activate Dopaminergic Neurons at Short Latency.

E. Dommett, V. Coizet, C. D. Blaha, J. Martindale, V. Lefebvre, N. Walton, J. E. W. Mayhew, P. G. Overton, and P. Redgrave (2005)
Science 307, 1476-1479
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By Carrot or by Stick: Cognitive Reinforcement Learning in Parkinsonism.

M. J. Frank, L. C. Seeberger, and R. C. O'Reilly (2004)
Science 306, 1940-1943
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Modulation of an Afterhyperpolarization by the Substantia Nigra Induces Pauses in the Tonic Firing of Striatal Cholinergic Interneurons.

J. N. J. Reynolds, B. I. Hyland, and J. R. Wickens (2004)
J. Neurosci. 24, 9870-9877
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