Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 26 March 2004:
Vol. 303. no. 5666, pp. 2040 - 2042
DOI: 10.1126/science.1093360
Prev | Table of Contents

Reports

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

Mark A. Ungless,*{dagger} 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.

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

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Phasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning.
H.-C. Tsai, F. Zhang, A. Adamantidis, G. D. Stuber, A. Bonci, L. de Lecea, and K. Deisseroth (2009)
Science 324, 1080-1084
   Abstract »    Full Text »    PDF »
From the Cover: Feature Article: Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior.
L. S. Zweifel, J. G. Parker, C. J. Lobb, A. Rainwater, V. Z. Wall, J. P. Fadok, M. Darvas, M. J. Kim, S. J. Y. Mizumori, C. A. Paladini, et al. (2009)
PNAS 106, 7281-7288
   Abstract »    Full Text »    PDF »
"To learn, you must pay attention." Molecular insights into teachers' wisdom.
M. G. Caron and R. M. Wightman (2009)
PNAS 106, 7267-7268
   Full Text »    PDF »
Dopamine Signaling Differences in the Nucleus Accumbens and Dorsal Striatum Exploited by Nicotine.
T. Zhang, L. Zhang, Y. Liang, A. G. Siapas, F.-M. Zhou, and J. A. Dani (2009)
J. Neurosci. 29, 4035-4043
   Abstract »    Full Text »    PDF »
Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli.
F. Brischoux, S. Chakraborty, D. I. Brierley, and M. A. Ungless (2009)
PNAS 106, 4894-4899
   Abstract »    Full Text »    PDF »
Human Substantia Nigra Neurons Encode Unexpected Financial Rewards.
K. A. Zaghloul, J. A. Blanco, C. T. Weidemann, K. McGill, J. L. Jaggi, G. H. Baltuch, and M. J. Kahana (2009)
Science 323, 1496-1499
   Abstract »    Full Text »    PDF »
Activity of Neurochemically Heterogeneous Dopaminergic Neurons in the Substantia Nigra during Spontaneous and Driven Changes in Brain State.
M. T. C. Brown, P. Henny, J. P. Bolam, and P. J. Magill (2009)
J. Neurosci. 29, 2915-2925
   Abstract »    Full Text »    PDF »
Effects of bifeprunox and aripiprazole on rat serotonin and dopamine neuronal activity and anxiolytic behaviour.
L Dahan, H Husum, O Mnie-Filali, J Arnt, P Hertel, and N Haddjeri (2009)
J Psychopharmacol 23, 177-189
   Abstract »    PDF »
Differential Effect of Reward and Punishment on Procedural Learning.
T. Wachter, O. V. Lungu, T. Liu, D. T. Willingham, and J. Ashe (2009)
J. Neurosci. 29, 436-443
   Abstract »    Full Text »    PDF »
Endogenous Fatty Acid Ethanolamides Suppress Nicotine-Induced Activation of Mesolimbic Dopamine Neurons through Nuclear Receptors.
M. Melis, G. Pillolla, A. Luchicchi, A. L. Muntoni, S. Yasar, S. R. Goldberg, and M. Pistis (2008)
J. Neurosci. 28, 13985-13994
   Abstract »    Full Text »    PDF »
The role of the striatum in aversive learning and aversive prediction errors.
M. R Delgado, J. Li, D. Schiller, and E. A Phelps (2008)
Phil Trans R Soc B 363, 3787-3800
   Abstract »    Full Text »    PDF »
Midbrain Dopaminergic Neurons and Striatal Cholinergic Interneurons Encode the Difference between Reward and Aversive Events at Different Epochs of Probabilistic Classical Conditioning Trials.
M. Joshua, A. Adler, R. Mitelman, E. Vaadia, and H. Bergman (2008)
J. Neurosci. 28, 11673-11684
   Abstract »    Full Text »    PDF »
A Dopamine-Acetylcholine Cascade: Simulating Learned and Lesion-Induced Behavior of Striatal Cholinergic Interneurons.
C. O. Tan and D. Bullock (2008)
J Neurophysiol 100, 2409-2421
   Abstract »    Full Text »    PDF »
Midbrain Dopamine Neurons: Projection Target Determines Action Potential Duration and Dopamine D2 Receptor Inhibition.
E. B. Margolis, J. M. Mitchell, J. Ishikawa, G. O. Hjelmstad, and H. L. Fields (2008)
J. Neurosci. 28, 8908-8913
   Abstract »    Full Text »    PDF »
Striatal outcome processing in healthy aging.
K. M. COX, H. J. AIZENSTEIN, and J. A. FIEZ (2008)
Cogn Affect Behav Neurosci 8, 304-317
   Abstract »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
{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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
Slow Oscillatory Firing: A Major Firing Pattern of Dopamine Neurons in the Ventral Tegmental Area.
W.-X. Shi (2005)
J Neurophysiol 94, 3516-3522
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »
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
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)