Hippocampal networks habituate as novelty accumulates

Learning and Memory

Volumn 20, Issue 4, 2013, Pages 229-235

  Murty, Vishnu P ^a,b,c   Ballard, Ian C ^a   MacDuffie, Katherine E ^a   Krebs, Ruth M ^d   Adcock, R Alison ^a,b  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY   (United States)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BRAIN CORTEX; BRAIN SIZE; CAUDATE NUCLEUS; CEREBELLUM; CLINICAL ARTICLE; CORPUS CALLOSUM; CORPUS STRIATUM; DECLARATIVE MEMORY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HABITUATION; HIPPOCAMPUS; HUMAN; MALE; MEDIAL TEMPORAL LOBE; MENTAL TASK; MIDDLE TEMPORAL GYRUS; NORMAL HUMAN; PARAHIPPOCAMPAL CORTEX; PERIRHINAL CORTEX; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; SUPERIOR TEMPORAL GYRUS; TASK PERFORMANCE; TEMPORAL LOBE; VENTROMEDIAL PREFRONTAL CORTEX; VISION;

ADULT; ANALYSIS OF VARIANCE; BRAIN MAPPING; EXPLORATORY BEHAVIOR; FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MODELS, STATISTICAL; NERVE NET; OXYGEN; REACTION TIME; RECOGNITION (PSYCHOLOGY); TEMPORAL LOBE; YOUNG ADULT;

EID: 84876568784     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.029728.112     Document Type: Article

References (57)

1. Acquas E, Wilson C, Fibiger HC. 1996. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: Effects of novelty, habituation, and fear. J Neurosci 16: 3089-3096. (Pubitemid 26121851)
2. Adcock RA, Thangavel A, Whitfield-Gabrieli S, Knutson B, Gabrieli JD. 2006. Reward-motivated learning: Mesolimbic activation precedes memory formation. Neuron 50: 507-517.
3. Amso D, Davidson MC, Johnson SP, Glover G, Casey BJ. 2005. Contributions of the hippocampus and the striatum to simple association and frequency-based learning. Neuroimage 27: 291-298. (Pubitemid 41074832)
4. Ballard IC, Murty VP, Carter RM, MacInnes JJ, Huettel SA, Adcock RA. 2011. Dorsolateral prefrontal cortex drives mesolimbic dopaminergic regions to initiate motivated behavior. J Neurosci 31: 10340-10346.
5. Blackford JU, Buckholtz JW, Avery SN, Zald DH. 2010. A unique role for the human amygdala in novelty detection. Neuroimage 50: 1188-1193.
6. Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, Strauss MM, Hyman SE, Rosen BR. 1996. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17: 875-887. (Pubitemid 26424015)
7. Brozinsky CJ, Yonelinas AP, Kroll NE, Ranganath C. 2005. Lag-sensitive repetition suppression effects in the anterior parahippocampal gyrus. Hippocampus 15: 557-561. (Pubitemid 41149578)
8. Buchel C, Morris J, Dolan RJ, Friston KJ. 1998. Brain systems mediating aversive conditioning: An event-related fMRI study. Neuron 20: 947-957. (Pubitemid 28247400)
9. Buchel C, Dolan RJ, Armony JL, Friston KJ. 1999. Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imaging. J Neurosci 19: 10869-10876. (Pubitemid 30235731)
10. Bunzeck N, Duzel E. 2006. Absolute coding of stimulus novelty in the human substantia nigra/VTA. Neuron 51: 369-379. (Pubitemid 44118710)
11. Bunzeck N, Dayan P, Dolan RJ, Duzel E. 2010. A common mechanism for adaptive scalingofrewardandnovelty. Hum Brain Mapp31:1380-1394.
12. Dale AM. 1999. Optimal experimental design for event-related fMRI. Hum Brain Mapp 8: 109-114. (Pubitemid 29480297)
13. Fischer H, Wright CI, Whalen PJ, McInerney SC, Shin LM, Rauch SL. 2003. Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study. Brain Res Bull 59: 387-392. (Pubitemid 36042833)
14. Foerde K, Shohamy D. 2011. The role of the basal ganglia in learning and memory: Insight from Parkinson's disease. Neurobiol Learn Mem 96: 624-636.
15. Gabrieli JD, Brewer JB, Desmond JE, Glover GH. 1997. Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276: 264-266. (Pubitemid 27172686)
16. Giovannini MG, Rakovska A, Benton RS, Pazzagli M, Bianchi L, Pepeu G. 2001. Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106: 43-53. (Pubitemid 32831072)
17. Grabenhorst F, Rolls ET. 2011. Value, pleasure and choice in the ventral prefrontal cortex. Trends Cogn Sci 15: 56-67.
18. Hasselmo ME, Stern CE. 2006. Mechanisms underlying working memory for novel information. Trends Cogn Sci 10: 487-493. (Pubitemid 44602572)
19. Henson RN, Cansino S, Herron JE, Robb WG, Rugg MD. 2003. A familiarity signal in human anterior medial temporal cortex? Hippocampus 13: 301-304. (Pubitemid 36503542)
20. Howard LR, Kumaran D, Olafsdottir HF, Spiers HJ.2011. Double dissociation between hippocampal and parahippocampal responses to object-background context and scene novelty. J Neurosci 31: 5253-5261.
21. Jessen F, Manka C, Scheef L, Granath DO, Schild HH, Heun R. 2002. Novelty detection and repetition suppression in a passive picture viewing task: A possible approach for the evaluation of neuropsychiatric disorders. Hum Brain Mapp 17: 230-236. (Pubitemid 35375535)
22. Kim H. 2011. Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies. Neuroimage 54: 2446-2461.
23. Kirchhoff BA, Wagner AD, Maril A, Stern CE. 2000. Prefrontal-temporal circuitry for episodic encoding and subsequent memory. J Neurosci 20: 6173-6180. (Pubitemid 30658411)
24. Kohler S, Danckert S, Gati JS, Menon RS. 2005. Novelty responses to relational and non-relational information in the hippocampus and the parahippocampal region: A comparison based on event-related fMRI. Hippocampus 15: 763-774. (Pubitemid 41300826)
25. Kumaran D, Maguire EA. 2006. An unexpected sequence of events: Mismatch detection in the human hippocampus. PLoS Biol 4: e424.
26. LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA. 1998. Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study. Neuron 20: 937-945. (Pubitemid 28247399)
27. Leussis MP, Bolivar VJ. 2006. Habituation in rodents: A review of behavior, neurobiology, and genetics. Neurosci Biobehav Rev 30: 1045-1064. (Pubitemid 44308646)
28. Levy R, Goldman-Rakic PS. 2000. Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133: 23-32. (Pubitemid 30411654)
29. Mumford JA, Turner BO, Ashby FG, Poldrack RA. 2012. Deconvolving BOLD activation in event-related designs for multivoxel pattern classification analyses. Neuroimage 59: 2636-2643.
30. Murty VP, Labar KS, Adcock RA. 2012. Threat of punishment motivates memory encoding via amygdala, not midbrain, interactions with the medial temporal lobe. J Neurosci 32: 8969-8976.
31. Owen AM, McMillan KM, Laird AR, Bullmore E. 2005. N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25: 46-59. (Pubitemid 40656192)
32. Poldrack RA, Clark J, Pare-Blagoev EJ, Shohamy D, Creso Moyano J, Myers C, Gluck MA. 2001. Interactive memory systems in the human brain. Nature 414: 546-550. (Pubitemid 33131537)
33. Ranganath C, Rainer G. 2003. Neural mechanisms for detecting and remembering novel events. Nat Rev Neurosci 4: 193-202. (Pubitemid 37280184)
34. Rangel A, Hare T. 2010. Neural computations associated with goal-directed choice. Curr Opin Neurobiol 20: 262-270.
35. Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, et al. 2009. Habituation revisited: An updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 92: 135-138.
36. Roy M, Shohamy D, Wager TD. 2012. Ventromedial prefrontal-subcortical systems and the generation of affective meaning. Trends Cogn Sci 16: 147-156.
37. Savine AC, Braver TS. 2010. Motivated cognitive control: Reward incentives modulate preparatory neural activity during task-switching. J Neurosci 30: 10294-10305.
38. Schiller D, Delgado MR. 2010. Overlapping neural systems mediating extinction, reversal and regulation of fear. Trends Cogn Sci 14: 268-276.
39. Schoenbaum G, Takahashi Y, Liu TL, McDannald MA. 2011. Does the orbitofrontal cortex signal value? Ann N Y Acad Sci 1239: 87-99.
40. Shohamy D. 2011. Learning and motivation in the human striatum. Curr Opin Neurobiol 21: 408-414.
41. Silvetti M, Seurinck R, Verguts T. 2011. Value and prediction errorinmedial frontal cortex: Integrating the single-unit and systems levelsofanalysis. Front Hum Neurosci 5: 75.
42. Sokolov EN. 1963. Perception and the conditioned reflex. Pergamon Press, Oxford, UK.
43. Spaniol J, Davidson PS, Kim AS, Han H, Moscovitch M, Grady CL. 2009. Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation. Neuropsychologia 47: 1765-1779.
44. Stern CE, Corkin S, Gonzalez RG, Guimaraes AR, Baker JR, Jennings PJ, Carr CA, Sugiura RM, Vedantham V, Rosen BR. 1996. The hippocampal formation participates in novel picture encoding: Evidence from functional magnetic resonance imaging. Proc Natl Acad Sci 93: 8660-8665. (Pubitemid 26269616)
45. Stern CE, Sherman SJ, Kirchhoff BA, Hasselmo ME. 2001. Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli. Hippocampus 11: 337-346. (Pubitemid 32799001)
46. Strange BA, Dolan RJ. 2001. Adaptive anterior hippocampal responses to oddball stimuli. Hippocampus 11: 690-698. (Pubitemid 34065498)
47. Vertes RP. 2006. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142: 1-20. (Pubitemid 44353937)
48. White NM, McDonald RJ. 2002. Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77: 125-184. (Pubitemid 34971650)
49. Wilson FA, Rolls ET. 1990a. Learning and memory is reflected in the responses of reinforcement-related neurons in the primate basal forebrain. J Neurosci 10: 1254-1267.
50. Wilson FA, Rolls ET. 1990b. Neuronal responses related to the novelty and familiarity of visual stimuli in the substantia innominata, diagonal band of Broca and periventricular region of the primate basal forebrain. Exp Brain Res 80: 104-120. (Pubitemid 20144429)
51. Wittmann BC, Bunzeck N, Dolan RJ, Duzel E. 2007. Anticipationof novelty recruits reward system and hippocampus while promoting recollection. Neuroimage 38: 194-202. (Pubitemid 47429984)
52. Woolrich MW, Ripley BD, Brady M, Smith SM. 2001. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14: 1370-1386. (Pubitemid 33124185)
53. Worsley KJ. 2001. Statistical analysis of activation images. In Functional MRI: An introduction to methods (ed. Jezzard P, et al.), Vol 1, pp. 251-270. Oxford University Press, Oxford, UK.
54. Wright CI, Fischer H, Whalen PJ, McInerney SC, Shin LM, Rauch SL. 2001. Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli. Neuroreport 12: 379-383. (Pubitemid 32114384)
55. Yamaguchi S, Hale LA, D'Esposito M, Knight RT. 2004. Rapid prefrontal-hippocampal habituation to novel events. J Neurosci 24: 5356-5363. (Pubitemid 38747677)
56. Yantis S. 2000. Attentional capture in vision. In Control of cognitive processes: Attention and performance XVIII (ed. Monsell S, Driver J), pp. 71-208. MIT Press, Cambridge, MA.
57. Yassa MA, Stark CE. 2008. Multiple signals of recognition memory in the medial temporal lobe. Hippocampus 18: 945-954.