Transfer of learning relates to intrinsic connectivity between hippocampus, ventromedial prefrontal cortex, and large-scale networks

Journal of Neuroscience

Volumn 34, Issue 34, 2014, Pages 11297-11303

  Gerraty, Raphael T ^a   Davidow, Juliet Y ^a   Wimmer, G Elliott ^b   Kahn, Itamar ^c   Shohamy, Daphna ^a  

^a Department of Psychology Kavli Institute for Brain Science Columbia University ^*  (United States)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Generalization; Intrinsic connectivity; Learning; Networks; Rest

Indexed keywords

ADULT; ARTICLE; ASSOCIATION; BEHAVIOR; CONNECTOME; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MEMORY; NERVE CELL NETWORK; NORMAL HUMAN; PRIORITY JOURNAL; TASK PERFORMANCE; VENTROMEDIAL PREFRONTAL CORTEX; VISUAL STIMULATION; YOUNG ADULT; ADOLESCENT; BLOOD; BRAIN MAPPING; DECISION MAKING; GAME; IMAGE PROCESSING; INDIVIDUALITY; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PREFRONTAL CORTEX; REWARD; VASCULARIZATION;

OXYGEN;

ADOLESCENT; ADULT; ASSOCIATION LEARNING; BRAIN MAPPING; DECISION MAKING; FEMALE; GAMES, EXPERIMENTAL; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDIVIDUALITY; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OXYGEN; PREFRONTAL CORTEX; REWARD; TRANSFER (PSYCHOLOGY); YOUNG ADULT;

EID: 84906262365     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0185-14.2014     Document Type: Article

References (45)

1. Andrews-Hanna J. R, Reidler JS, Sepulcre J, Poulin R, Buckner RL (2010) Functional-anatomic fractionation of the brain's default network. Neuron 65:550-562. CrossRef Medline
2. Beckmann C. F, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001-1013. CrossRef Medline
3. Bornstein A. M, Daw ND (2013) Cortical and hippocampal correlates of deliberation during model-based decisions for rewards in humans. PLoS Comput Biol 9:e1003387. CrossRef Medline
4. Brogden W. J (1939) Sensory pre-conditioning. J Experimental Psychology 25:9.
5. Buckner R. L, Andrews-Hanna JR, Schacter DL (2008) The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1-38. CrossRef Medline
6. Daw N. D, Niv Y, Dayan P (2005) Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat Neurosci 8:1704-1711. CrossRef Medline
7. Daw N. D, Gershman SJ, Seymour B, Dayan P, Dolan RJ (2011) Model-based influences on humans' choices and striatal prediction errors. Neuron 69:1204-1215. CrossRef Medline
8. Doll B. B, Simon DA, Daw ND (2012) The ubiquity of model-based reinforcement learning. Curr Opin Neurobiol 22:1075-1081. CrossRef Medline
9. Doll B. B, Shohamy D, DawN (2014) Multiple memory systems as substrates for multiple decision systems. Neurobiol Learn Mem. Advance online publication. Retrieved July 17, 2014. doi:10.1016/j.nlm.2014.04.014. CrossRef
10. Dosenbach N. U, Fair DA, Cohen AL, Schlaggar BL, Petersen SE (2008) A dual-networks architecture of top-down control. Trends in Cognitive Sciences 12:99-105. CrossRef Medline
11. DoyèreV, Burette F, Negro CR, Laroche S (1993) Long-term potentiation of hippocampal afferents and efferents to prefrontal cortex: implications for associative learning. Neuropsychologia 31:1031-1053. CrossRef Medline
12. Dusek J. A, Eichenbaum H (1997) The hippocampus and memory for orderly stimulus relations. Proc Natl Acad Sci U S A 94:7109-7114. CrossRef Medline
13. Fornito A., Harrison BJ, Zalesky A, Simons JS (2012) Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proc Natl Acad Sci U S A 109:12788-12793. CrossRef Medline
14. Greene A. J, Gross WL, Elsinger CL, Rao SM (2006) An FMRI analysis of the human hippocampus: inference, context, and task awareness. J Cogn Neurosci 18:1156-1173. CrossRef Medline
15. Hampton A. N, Bossaerts P, O'Doherty JP (2006) The role of the ventromedial prefrontal cortex in abstract state-based inference during decision making in humans. J Neurosci 26:8360-8367. CrossRef Medline
16. He B. J (2013) Spontaneous and task-evoked brain activity negatively interact. J Neurosci 33:4672-4682. CrossRef Medline
17. Ivleva E. I, Shohamy D, Mihalakos P, Morris DW, Carmody T, Tamminga CA (2012) Memory generalization is selectively altered in the psychosis dimension. Schizophr Res 138:74-80. CrossRef Medline
18. Jenkinson M., Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825-841. CrossRef Medline
19. Jones J. L, Esber GR, McDannald MA, Gruber AJ, Hernandez A, Mirenzi A, Schoenbaum G. (2012) Orbitofrontal cortex supports behavior and learning using inferred but not cached values. Science 338:953-956. CrossRef Medline
20. Kahn I., Shohamy D (2013) Intrinsic connectivity between the hippocampus, nucleus accumbens, and ventral tegmental area in humans. Hippocampus 23:187-192. CrossRef Medline
21. Kumaran D., McClelland JL (2012) Generalization through the recurrent interaction of episodic memories: a model of the hippocampal system. Psychol Rev 119:573-616. CrossRef Medline
22. Kumaran D., Summerfield JJ, Hassabis D, Maguire EA (2009) Tracking the emergence of conceptual knowledge during human decision making. Neuron 63:889-901. CrossRef Medline
23. McDannald M. A, Lucantonio F, Burke KA, Niv Y, Schoenbaum G (2011) Ventral striatum and orbitofrontal cortex are both required for modelbased, but not model-free, reinforcement learning. J Neurosci 31:2700-2705. CrossRef Medline
24. Meng X.-l., Rosenthal R, Rubin DB (1992) Comparing correlated correlation coefficients. Psychol Bull 111:172-175. CrossRef
25. Myers C. E, Shohamy D, Gluck MA, Grossman S, Kluger A, Ferris S, Golomb J, Schnirman G., Schwartz R (2003) Dissociating hippocampal versus basal ganglia contributions to learning and transfer. J Cogn Neurosci 15:185-193. CrossRef Medline
26. Port R. L, Beggs AL, PattersonMM (1987) Hippocampal substrate of sensory associations. Physiol Behav 39:643-647. CrossRef Medline
27. Power J. D, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, Vogel AC, Laumann T. O, Miezin FM, Schlaggar BL, Petersen SE (2011) Functional network organization of the human brain. Neuron 72:665-678. CrossRef Medline
28. Power J. D, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142-2154. CrossRef Medline
29. Roy M., Shohamy D, WagerTD (2012) Ventromedial prefrontal-subcortical systems and the generation of affective meaning. Trends Cogn Sci 16:147-156. CrossRef Medline
30. Satterthwaite T. D, Wolf DH, Loughead J, Ruparel K, Elliott MA, Hakonarson H, Gur RC, Gur RE (2012) Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 60:623-632. CrossRef Medline
31. Satterthwaite T. D, Elliott MA, Gerraty RT, Ruparel K, Loughead J, Calkins ME, Eickhoff SB, Hakonarson H, Gur RC, Gur RE, Wolf DH (2013) An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64:240-256. CrossRef Medline
32. Schoenbaum G., Takahashi Y, Liu TL, McDannald MA (2011) Does the orbitofrontal cortex signal value? Ann N Y Acad Sci 1239:87-99. CrossRef Medline
33. Shohamy D., Wagner AD (2008) Integrating memories in the human brain: hippocampal-midbrain encoding of overlapping events. Neuron 60:378-389. CrossRef Medline
34. SmithSM (2002) Fast robust automated brain extraction. HumBrain Mapp 17:143-155. CrossRef Medline
35. Sreenivas S., Boehm SG, Linden DE (2012) Emotional faces and the default mode network. Neurosci Lett 506:229-234. CrossRef Medline
36. Takita M., Izaki Y, Jay TM, Kaneko H, Suzuki SS (1999) Induction of stable long-term depression in vivo in the hippocampal-prefrontal cortex pathway. Eur J Neurosci 11:4145-4148. CrossRef Medline
37. van Kesteren M. T, Fernández G, Norris DG, Hermans EJ (2010) Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans. Proc Natl Acad Sci U S A 107:7550-7555. CrossRef Medline
38. van Kesteren M. T, Ruiter DJ, Fernández G, Henson RN (2012) How schema and novelty augment memory formation. Trends Neurosci 35:211-219. CrossRef Medline
39. Wimmer G. E, Shohamy D (2011) The striatum and beyond: contributions of the hippocampus to decision making. In: Decision making, affect, and learning: attention and performance XXIII (Delgado MR, Phelps EA, Robbins T. W, eds), pp 281-310. Oxford, New York: Oxford UP.
40. Wimmer G. E, Shohamy D (2012) Preference by association: how memory mechanisms in the hippocampus bias decisions. Science 338:270-273. CrossRef Medline
41. Wimmer G. E, Daw ND, Shohamy D (2012) Generalization of value in reinforcement learning by humans. Eur J Neurosci 35:1092-1104. CrossRef Medline
42. Woolrich M. W, Ripley BD, Brady M, Smith SM (2001) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14: 1370-1386. CrossRef Medline
43. Yeo B. T, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman J. L, Smoller JW, Zöllei L, Polimeni JR, Fischl B, Liu H, Buckner RL (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106:1125-1165. CrossRef Medline
44. Zeithamova D., Dominick AL, Preston AR (2012) Hippocampal and ventral medial prefrontal activation during retrieval-mediated learning supports novel inference. Neuron 75:168-179. CrossRef Medline
45. Zuo X. N, Kelly C, Adelstein JS, Klein DF, Castellanos FX, Milham MP (2010) Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. Neuroimage 49:2163-2177. CrossRef Medline