VTA neurons coordinate with the hippocampal reactivation of spatial experience

eLife

Volumn 4, Issue OCTOBER2015, 2015, Pages

  Gomperts, Stephen N ^a,b   Kloosterman, Fabian ^c,d,e   Wilson, Matthew A ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c Belgium   (Belgium)

^d IMEC   (Belgium)

^e Lab of Experimental Radiotherapy   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

COORDINATION; HIPPOCAMPUS; NERVE CELL; PREDICTION; REINFORCEMENT; REWARD; SLOW WAVE SLEEP; SPATIAL MEMORY; ANIMAL; FEEDING BEHAVIOR; PHYSIOLOGY; RAT; SLEEP; SPATIAL LEARNING; VENTRAL TEGMENTUM;

ANIMALS; FEEDING BEHAVIOR; HIPPOCAMPUS; NEURONS; RATS; SLEEP; SPATIAL LEARNING; VENTRAL TEGMENTAL AREA;

EID: 84955252478     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/elife.05360     Document Type: Article

References (42)

1. Cardinal RN, Parkinson JA, Hall J, Everitt BJ. 2002. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience and Biobehavioral Reviews 26:321-352. doi: 10.1016/S0149-7634 (02)00007-6
2. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. 2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482:85-88. doi: 10.1038/nature10754
3. Davidson TJ, Kloosterman F, Wilson MA. 2009. Hippocampal replay of extended experience. Neuron 63:497- 507. doi: 10.1016/j.neuron.2009.07.027
4. de Lavilléon G, Lacroix MM, Rondi-Reig L, Benchenane K. 2015. Explicit memory creation during sleep demonstrates a causal role of place cells in navigation. Nature Neuroscience 18:493-495. doi: 10.1038/nn.3970
5. Diba K, Buzsáki György. 2007. Forward and reverse hippocampal place-cell sequences during ripples. Nature Neuroscience 10:1241-1242. doi: 10.1038/nn1961
6. Doll BB, Simon DA, Daw ND. 2012. The ubiquity of model-based reinforcement learning. Current Opinion in Neurobiology 22:1075-1081. doi: 10.1016/j.conb.2012.08.003
7. Ego-Stengel Valérie, Wilson MA. 2010. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1-10. doi: 10.1002/hipo.20707
8. Foster DJ, Wilson MA. 2006. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680-683. doi: 10.1038/nature04587
9. Fujisawa S, Buzsáki György. 2011. A 4 hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72:153-165. doi: 10.1016/j.neuron.2011.08.018
10. Girardeau G, Benchenane K, Wiener SI, Buzsáki György, Zugaro Michaël B. 2009. Selective suppression of hippocampal ripples impairs spatial memory. Nature Neuroscience 12:1222-1223. doi: 10.1038/nn.2384
11. Hnasko TS, Hjelmstad GO, Fields HL, Edwards RH. 2012. Ventral tegmental area glutamate neurons: electrophysiological properties and projections. The Journal of Neuroscience 32:15076-15085. doi: 10.1523/ JNEUROSCI.3128-12.2012
12. Jadhav SP, Kemere C, German PW, Frank LM. 2012. Awake hippocampal sharp-wave ripples support spatial memory. Science 336:1454-1458. doi: 10.1126/science.1217230
13. Ji D, Wilson MA. 2007. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nature Neuroscience 10:100-107. doi: 10.1038/nn1825
14. Jones MW, Wilson MA. 2005. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biology 3:e402 http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.0030402 doi: 10.1371/journal.pbio.0030402
15. Karlsson MP, Frank LM. 2009. Awake replay of remote experiences in the hippocampus. Nature Neuroscience 12:913-918. doi: 10.1038/nn.2344
16. Kloosterman F, Layton SP, Chen Z, Wilson MA. 2014. Bayesian decoding using unsorted spikes in the rat hippocampus. Journal of Neurophysiology 111:217-227. doi: 10.1152/jn.01046.2012
17. Kloosterman F. 2012. Analysis of Hippocampal Memory Replay Using Neural Population Decoding. Neuronal network analysis. New York: Springer; 259-282.
18. Lammel S, Hetzel A, Häckel O, Jones I, Liss B, Roeper J. 2008. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773. doi: 10.1016/j.neuron.2008.01.022
19. Lansink CS, Goltstein PM, Lankelma JV, Mcnaughton BL, Pennartz CMA. 2009. Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biology 7:e1000173. Epub 2009 Aug 18 doi: 10.1371/ journal.pbio.1000173
20. Lee AK, Wilson MA. 2002. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183-1194. doi: 10.1016/S0896-6273(02)01096-6
21. Margolis EB, Lock H, Hjelmstad GO, Fields HL. 2006. The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? The Journal of Physiology 577:907-924. doi: 10.1113/ jphysiol.2006.117069
22. Margolis EB, Toy B, Himmels P, Morales M, Fields HL. 2012. Identification of rat ventral tegmental area GABAergic neurons. PloS One 7:e42365. Epub 2012 Jul 31 doi: 10.1371/journal.pone.0042365
23. Mcnamara CG, Tejero-Cantero Á lvaro, Trouche Stéphanie, Campo-Urriza N, Dupret D. 2014. Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nature Neuroscience 17:1658-1660. doi: 10.1038/nn.3843
24. Montague PR, Dayan P, Sejnowski TJ. 1996. A framework for mesencephalic dopamine systems based on predictive hebbian learning. The Journal of Neuroscience 16:1936-1947.
25. Morris G, Nevet A, Arkadir D, Vaadia E, Bergman H. 2006. Midbrain dopamine neurons encode decisions for future action. Nature Neuroscience 9:1057-1063. doi: 10.1038/nn1743
26. Nádasdy Z, Hirase H, CzurkóA, Csicsvari J, Buzsáki G. 1999. Replay and time compression of recurring spike sequences in the hippocampus. The Journal of Neuroscience 19:9497-9507.
27. O'Keefe J, Dostrovsky J. 1971. The hippocampus as a spatial map. preliminary evidence from unit activity in the freely-moving rat. Brain Research 34:171-175. doi: 10.1016/0006-8993(71)90358-1
28. Pavlides C, Winson J. 1989. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. The Journal of Neuroscience 9:2907-2918.
29. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. London:Academic Press.
30. Pennartz CMA, Lee E, Verheul J, Lipa P, Barnes CA, Mcnaughton BL. 2004. The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. The Journal of Neuroscience 24:6446-6456. doi: 10.1523/JNEUROSCI.0575-04.2004
31. Pfeiffer BE, Foster DJ. 2013. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497:74-79. doi: 10.1038/nature12112
32. Roesch MR, Calu DJ, Schoenbaum G. 2007. Dopamine neurons encode the better option in rats deciding between differently delayed or sized rewards. Nature Neuroscience 10:1615-1624. doi: 10.1038/nn2013
33. Schultz W, Apicella P, Scarnati E, Ljungberg T. 1992. Neuronal activity in monkey ventral striatum related to the expectation of reward. The Journal of Neuroscience 12:4595-4610.
34. Schultz W. 1998. Predictive reward signal of dopamine neurons. Journal of Neurophysiology 80:1-27.
35. Siapas AG, Lubenov EV, Wilson MA. 2005. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141-151. doi: 10.1016/j.neuron.2005.02.028
36. Singer AC, Carr MF, Karlsson MP, Frank LM. 2013. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron 77:1163-1173. doi: 10.1016/j.neuron.2013.01.027
37. Singer AC, Frank LM. 2009. Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron 64:910-921. doi: 10.1016/j.neuron.2009.11.016
38. Totah NKB, Kim Y, Moghaddam B. 2013. Distinct prestimulus and poststimulus activation of VTA neurons correlates with stimulus detection. Journal of Neurophysiology 110:75-85. doi: 10.1152/jn.00784.2012
39. Ungless MA, Grace AA. 2012. Are you or aren't you? challenges associated with physiologically identifying dopamine neurons. Trends in Neurosciences 35:422-430. doi: 10.1016/j.tins.2012.02.003
40. Walsh MM, Anderson JR. 2014. Navigating complex decision spaces: problems and paradigms in sequential choice. Psychological Bulletin 140:466-486. doi: 10.1037/a0033455
41. Wilson MA, Mcnaughton BL. 1994. Reactivation of hippocampal ensemble memories during sleep. Science 265: 676-679. doi: 10.1126/science.8036517
42. Zhang K, Ginzburg I, McNaughton BL, Sejnowski TJ. 1998. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. Journal of Neurophysiology 79: 1017-1044.