Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli

Journal of Neuroscience

Volumn 33, Issue 11, 2013, Pages 4710-4725

  Fiorillo, Christopher D ^a,b   Song, Minryung R ^a   Yun, Sora R ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHLORIDE;

ANIMAL EXPERIMENT; APPETITE; ARTICLE; AVERSIVE BEHAVIOR; AVOIDANCE BEHAVIOR; BITTER TASTE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EYE TRACKING; FEMALE; FRUIT JUICE; GAZE; LATENT PERIOD; MALE; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; REWARD; RHESUS MONKEY; SPIKE; TASK PERFORMANCE; VISUAL STIMULATION;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; APPETITIVE BEHAVIOR; AVOIDANCE LEARNING; CHOICE BEHAVIOR; CONDITIONING, CLASSICAL; DOPAMINERGIC NEURONS; FEMALE; JUDGMENT; MACACA MULATTA; MALE; MESENCEPHALON; MOTIVATION; NEURAL INHIBITION; NONLINEAR DYNAMICS; REACTION TIME; REGRESSION ANALYSIS; REINFORCEMENT (PSYCHOLOGY); TIME FACTORS;

EID: 84874900519     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3883-12.2013     Document Type: Article

References (44)

1. Arbuthnott GW, Wickens J (2007) Space, time and dopamine. Trends Neurosci 30:62-69. CrossRef Medline
2. Barlow HB (1961) Possible principles underlying the transformation of sensory messages. In: Sensory communication (Rosenblith WA, ed), pp 217-234. Cambridge, MA: MIT.
3. Berg RW, Alaburda A, Hounsgaard J (2007) Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315:390-393. CrossRef Medline
4. Brischoux F, Chakraborty S, Brierley DI, Ungless MA (2009) Phasic excitation of dopamine neurons in the ventral VTA by noxious stimuli. Proc Natl Acad Sci U S A 106:4894-4899. CrossRef Medline
5. Bromberg-Martin ES, Matsumoto M, Hikosaka O (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815-834. CrossRef Medline
6. Brown J, Bullock D, Grossberg S (1999) How the basal ganglia use parallel excitatory and inhibitory learning pathways to selectively respond to unexpected rewarding cues. J Neurosci 19:10502-10511. Medline
7. Budygin EA, Park J, Bass CE, Grinevich VP, Bonin KD, Wightman RM (2012) Aversive stimulus differentially triggers subsecond dopamine release in reward regions. Neuroscience 201:331-337. CrossRef Medline
8. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N (2012) Neuron-typespecific signals for reward and punishment in the ventral tegmental area. Nature 482:85-88. CrossRef Medline
9. Coizet V, Dommett EJ, Redgrave P, Overton PG (2006) Nociceptive responses of midbrain dopaminergic neurones are modulated by the superior colliculus in the rat. Neuroscience 139:1479-1493. CrossRef Medline
10. Dommett E, Coizet V, Blaha CD, Martindale J, Lefebvre V, Walton N, Mayhew JE, Overton PG, Redgrave P (2005) How visual stimuli activate dopaminergic neurons at short latency. Science 307:1476-1479. CrossRef Medline
11. Fiorillo CD (2008) Towards a general theory of neural computation based on prediction by single neurons. PLo S ONE 3:e3298. CrossRef Medline
12. Fiorillo CD (2011) Transient activation of midbrain dopamine neurons by reward risk. Neuroscience 197:162-171. CrossRef Medline
13. Fiorillo CD, Williams JT (1998) Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394:78-82. CrossRef Medline
14. Fiorillo CD, Tobler PN, Schultz W (2003) Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299:1898-1902. CrossRef Medline
15. Fiorillo CD, Newsome WT, Schultz W (2008) The temporal precision of reward prediction in dopamine neurons. Nat Neurosci 11:966-973. CrossRef Medline
16. Fiorillo CD, Yun SR, Song MR (2013) Diversity and homogeneity in responses of midbrain dopamine neurons. J Neurosci 33:4693-4709. CrossRef
17. Guarraci FA, Kapp BS (1999) An electrophysiological characterization of ventral tegmental area dopaminegic neurons during differential pavalovian fear conditioning in the awake rabbit. Behav Brain Res 99:169-179. CrossRef Medline
18. Hong S, Jhou TC, Smith M, Saleem KS, Hikosaka O (2011) Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates. J Neurosci 31:11457-11471. CrossRef Medline
19. Horvitz JC (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96:651-656. CrossRef Medline
20. Horvitz JC, Stewart T, Jacobs BL (1997) Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat. Brain Res 759:251-258. CrossRef Medline
21. Hosoya T, Baccus SA, Meister M (2005) Dynamic predictive coding by the retina. Nature 436:71-77. CrossRef Medline
22. Jhou TC, Fields HL, Baxter MG, Saper CB, Holland PC (2009) The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61:786-800. CrossRef Medline
23. Joshua M, Adler A, Mitelman R, Vaadia E, Bergman H (2008) Midbrain dopaminergic neurons and striatal cholinergic interneurons encode the difference between reward and aversive events at different epochs of probabilistic classical conditioning trials. J Neurosci 28:11673-11684. CrossRef Medline
24. Kakade S, Dayan P (2002) Dopamine: generalization and bonuses. Neural Netw 15:549-559. CrossRef Medline
25. Matsumoto M, Hikosaka O (2007) Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447:1111-1115. CrossRef Medline
26. Matsumoto M, Hikosaka O (2009) Representation of negative motivational value in lateral habenula. Nat Neurosci 12:77-84. CrossRef Medline
27. Matsumoto M, Hikosaka O (2009) Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459: 837-841. CrossRef Medline
28. Mileykovskiy B, Morales M (2011) Duration of suppression of ventral tegmental area dopamine neurons encodes a level of conditioned fear. J Neurosci 31:7471-7476. CrossRef Medline
29. Mirenowicz J, Schultz W (1996) Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379:449-451. CrossRef Medline
30. Mogami T, Tanaka K (2006) Reward association affects neuronal responses to visual stimuli in macaque TE and perirhinal cortices. J Neurosci 26: 6761-6770. CrossRef Medline
31. Montague PR, Dayan P, Sejnowski TJ (1996) A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J Neurosci 16:1936-1947. Medline
32. Nomoto K, Schultz W, Watanabe T, Sakagami M (2010) Temporally extended dopamine responses to perceptually demanding rewardpredictive stimuli. J Neurosci 30:10692-10702. CrossRef Medline
33. Redgrave P, Prescott TJ, Gurney K (1999) Is the short-latency dopamine response too short to signal reward error? Trends Neurosci 22:146-151. CrossRef Medline
34. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27. Medline
35. Schultz W (2007) Multiple dopamine functions at different time courses. Annu Rev Neurosci 30:259-288. CrossRef Medline
36. Schultz W, Romo R (1987) Responses of nigrostriatal dopamine neurons to high-intensity somatosensory stimulation in the anesthetized monkey. J Neurophysiol 57:201-217. Medline
37. Schultz W, Apicella P, Ljungberg T (1993) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13:900-913. Medline
38. Strecker RE, Jacobs BL (1985) Substantia nigra dopaminergic unit activity in behaving cats: effect of arousal on spontaneous discharge and sensory evoked activity. Brain Res 361:339-350. CrossRef Medline
39. Tobler PN, Dickinson A, Schultz W (2003) Coding of predicted reward omission by dopamine neurons in a conditioned inhibition paradigm. J Neurosci 23:10402-10410. Medline
40. Tobler PN, Fiorillo CD, Schultz W (2005) Adaptive coding of reward value by dopamine neurons. Science 307:1642-1645. CrossRef Medline
41. Wang DV, Tsien JZ (2011) Convergent processing of both positive and negative motivational signals by the VTA dopamine neuronal populations. PLo S ONE 6:e17047. CrossRef Medline
42. Wang X, Sommer FT, Hirsch JA (2011) Inhibitory circuits for visual processing in thalamus. Curr Opin Neurobiol 21:726-733. CrossRef Medline
43. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 476:442-446. CrossRef Medline
44. Wise RA (2002) Brain reward circuitry: insights from unsensed incentives. Neuron 36:229-240. CrossRef Medline