Rapid signalling in distinct dopaminergic axons during locomotion and reward

Nature

Volumn 535, Issue 7613, 2016, Pages 505-510

  Howe, M W ^a   Dombeck, D A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE;

CHEMICAL COMPOUND; LOCOMOTION; MOVEMENT; NERVOUS SYSTEM DISORDER; NEUROLOGY; OPTICAL METHOD; RODENT;

ACCELERATION; ARTICLE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; DORSAL STRIATUM; LOCOMOTION; MOUSE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REWARD; SPIKE; TOPOGRAPHY; ANIMAL; AXON; CYTOLOGY; FEMALE; LEARNING; MALE; METABOLISM; NEOSTRIATUM; OPTOGENETICS; PHYSIOLOGY; SIGNAL TRANSDUCTION; TIME FACTOR;

ANIMALIA; MUS;

ACCELERATION; ANIMALS; AXONS; DOPAMINE; DOPAMINERGIC NEURONS; FEMALE; LEARNING; LOCOMOTION; MALE; MICE; NEOSTRIATUM; OPTOGENETICS; REWARD; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84978134216     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature18942     Document Type: Article

References (57)

1. Dauer, W., Przedborski, S. Parkinson's disease: mechanisms and models. Neuron 39, 889-909 (2003).
2. Hornykiewicz, O. [Dopamine (3-hydroxytyramine) in the central nervous system and its relation to the Parkinson syndrome in man]. Dtsch. Med. Wochenschr. 87, 1807-1810 (1962).
3. Carlsson, A. Evidence for a role of dopamine in extrapyramidal functions. Acta Neuroveg. (Wien) 26, 484-493 (1964).
4. Day, J. J., Roitman, M. F., Wightman, R. M., Carelli, R. M. Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat. Neurosci. 10, 1020-1028 (2007).
5. Howe, M. W., Tierney, P. L., Sandberg, S. G., Phillips, P. E., Graybiel, A. M. Prolonged dopamine signalling in striatum signals proximity and value of distant rewards. Nature 500, 575-579 (2013).
6. Romo, R., Schultz, W. Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements. J. Neurophysiol. 63, 592-606 (1990).
7. Pan, W. X., Schmidt, R., Wickens, J. R., Hyland, B. I. Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J. Neurosci. 25, 6235-6242 (2005).
8. Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B., Uchida, N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482, 85-88 (2012).
9. Mirenowicz, J., Schultz, W. Importance of unpredictability for reward responses in primate dopamine neurons. J. Neurophysiol. 72, 1024-1027 (1994).
10. Hamid, A. A. et al. Mesolimbic dopamine signals the value of work. Nat. Neurosci. 19, 117-126 (2016).
11. Berridge, K. C. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl.) 191, 391-431 (2007).
12. Schultz, W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259-288 (2007).
13. Schultz, W., Dayan, P., Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593-1599 (1997).
14. Mazzoni, P., Hristova, A., Krakauer, J. W. Why don't we move faster? Parkinson's disease, movement vigor, and implicit motivation. J. Neurosci. 27, 7105-7116 (2007).
15. Niv, Y., Daw, N. D., Joel, D., Dayan, P. Tonic dopamine: opportunity costs and the control of response vigor. Psychopharmacology (Berl.) 191, 507-520 (2007).
16. Jin, X., Costa, R. M. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466, 457-462 (2010).
17. Puryear, C. B., Kim, M. J., Mizumori, S. J. Conjunctive encoding of movement and reward by ventral tegmental area neurons in the freely navigating rodent. Behav. Neurosci. 124, 234-247 (2010).
18. Tobler, P. N., Fiorillo, C. D., Schultz, W. Adaptive coding of reward value by dopamine neurons. Science 307, 1642-1645 (2005).
19. Roesch, M. R., Calu, D. J., Schoenbaum, G. Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards. Nat. Neurosci. 10, 1615-1624 (2007).
20. Barter, J. W. et al. Beyond reward prediction errors: the role of dopamine in movement kinematics. Front. Integr. Neurosci. 9, 39 (2015).
21. Dodson, P. D. et al. Representation of spontaneous movement by dopaminergic neurons is cell-type selective and disrupted in parkinsonism. Proc. Natl Acad. Sci. USA, 113, E2180-E2188 (2016).
22. Margolis, E. B., Lock, H., Hjelmstad, G. O., Fields, H. L. The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J. Physiol. (Lond.) 577, 907-924 (2006).
23. Wang, L. et al. Modulation of dopamine release in the striatum by physiologically relevant levels of nicotine. Nat. Commun. 5, 3925 (2014).
24. Threlfell, S. et al. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75, 58-64 (2012).
25. Robinson, D. L., Venton, B. J., Heien, M. L., Wightman, R. M. Detecting subsecond dopamine release with fast-scan cyclic voltammetry in vivo. Clin. Chem. 49, 1763-1773 (2003).
26. Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L., Tank, D. W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 13, 1433-1440 (2010).
27. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
28. Matsuda, W. et al. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J. Neurosci. 29, 444-453 (2009).
29. Petreanu, L. et al. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489, 299-303 (2012).
30. Cox, C. L., Denk, W., Tank, D. W., Svoboda, K. Action potentials reliably invade axonal arbors of rat neocortical neurons. Proc. Natl Acad. Sci. USA 97, 9724-9728 (2000).
31. Turner, T. J. Nicotine enhancement of dopamine release by a calciumdependent increase in the size of the readily releasable pool of synaptic vesicles. J. Neurosci. 24, 11328-11336 (2004).
32. Woodward, J. J., Chandler, L. J., Leslie, S. W. Calcium-dependent and-independent release of endogenous dopamine from rat striatal synaptosomes. Brain Res. 473, 91-98 (1988).
33. Tritsch, N. X., Ding, J. B., Sabatini, B. L. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490, 262-266 (2012).
34. Parker, N. F. et al. Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target. Nat. Neurosci. 19, 845-854 (2016).
35. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., Deisseroth, K. Millisecondtimescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268 (2005).
36. Ikemoto, S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 56, 27-78 (2007).
37. Hollerman, J. R., Schultz, W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat. Neurosci. 1, 304-309 (1998).
38. Schultz, W., Romo, R. Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. J. Neurophysiol. 63, 607-624 (1990).
39. Lerner, T. N. et al. Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits. Cell 162, 635-647 (2015).
40. Salamone, J. D., Correa, M. The mysterious motivational functions of mesolimbic dopamine. Neuron 76, 470-485 (2012).
41. Dombeck, D. A., Khabbaz, A. N., Collman, F., Adelman, T. L., Tank, D. W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56, 43-57 (2007).
42. Steinberg, E. E., Janak, P. H. Establishing causality for dopamine in neural function and behavior with optogenetics. Brain Res. 1511, 46-64 (2013).
43. Steinbeck, J. A. et al. Optogenetics enables functional analysis of human embryonic stem cell-derived grafts in a Parkinson's disease model. Nat. Biotechnol. 33, 204-209 (2015).
44. Lammel, S. et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature 491, 212-217 (2012).
45. Beier, K. T. et al. Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping. Cell 162, 622-634 (2015).
46. Poulin, J. F. et al. Defining midbrain dopaminergic neuron diversity by single-cell gene expression profiling. Cell Rep. 9, 930-943 (2014).
47. Roeper, J. Dissecting the diversity of midbrain dopamine neurons. Trends Neurosci. 36, 336-342 (2013).
48. Lammel, S. et al. Diversity of transgenic mouse models for selective targeting of midbrain dopamine neurons. Neuron 85, 429-438 (2015).
49. Matsumoto, M., Hikosaka, O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459, 837-841 (2009).
50. Gunaydin, L. A. et al. Natural neural projection dynamics underlying social behavior. Cell 157, 1535-1551 (2014).
51. Harvey, C. D., Collman, F., Dombeck, D. A., Tank, D. W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941-946 (2009).
52. Heys, J. G., Rangarajan, K. V., Dombeck, D. A. The functional microorganization of grid cells revealed by cellular-resolution imaging. Neuron 84, 1079-1090 (2014).
53. Sheffield, M. E., Dombeck, D. A. Calcium transient prevalence across the dendritic arbour predicts place field properties. Nature 517, 200-204 (2015).
54. Hofer, S. B. et al. Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat. Neurosci. 14, 1045-1052 (2011).
55. Miyashita, T., Shao, Y. R., Chung, J., Pourzia, O., Feldman, D. E. Long-term channelrhodopsin-2 (ChR2) expression can induce abnormal axonal morphology and targeting in cerebral cortex. Front. Neural Circuits 7, 8 (2013).
56. Miri, A. et al. Spatial gradients and multidimensional dynamics in a neural integrator circuit. Nat. Neurosci. 14, 1150-1159 (2011).
57. Mukamel, E. A., Nimmerjahn, A., Schnitzer, M. J. Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 63, 747-760 (2009).