Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex

Abstract

The hippocampus and the orbitofrontal cortex (OFC) both have important roles in cognitive processes such as learning, memory and decision making. Nevertheless, research on the OFC and hippocampus has proceeded largely independently, and little consideration has been given to the importance of interactions between these structures. Here, evidence is reviewed that the hippocampus and OFC encode parallel, but interactive, cognitive 'maps' that capture complex relationships between cues, actions, outcomes and other features of the environment. A better understanding of the interactions between the OFC and hippocampus is important for understanding the neural bases of flexible, goal-directed decision making.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Hippocampal and orbitofrontal cognitive mapping.
Figure 2: Cognitive maps in action.

Similar content being viewed by others

References

  1. Rudebeck, P. H. & Murray, E. A. The orbitofrontal oracle: cortical mechanisms for the prediction and evaluation of specific behavioral outcomes. Neuron 84, 1143–1156 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Buckner, R. L. The role of the hippocampus in prediction and imagination. Annu. Rev. Psychol. 61, 27–48 (2010).

    Article  PubMed  Google Scholar 

  3. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon Press, 1978).

    Google Scholar 

  4. Tolman, E. C. Cognitive maps in rats and men. Psychol. Rev. 55, 189–208 (1948).

    Article  CAS  PubMed  Google Scholar 

  5. Tolman, E. C. Purposive Behavior in Animals and Men (Appleton-Century-Crofts, 1932).

    Google Scholar 

  6. Tolman, E. C. & Brunswik, E. The organism and the causal texture of the environment. Psychol. Rev. 42, 43 (1935).

    Article  Google Scholar 

  7. Buzsáki, G. & Moser, E. I. Memory, navigation and theta rhythm in the hippocampal–entorhinal system. Nat. Neurosci. 16, 130–138 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Eichenbaum, H. & Cohen Neal, J. Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83, 764–770 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M. & Tanila, H. The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23, 209–226 (1999).

    Article  CAS  PubMed  Google Scholar 

  10. Wikenheiser, A. M. & Redish, A. D. Decoding the cognitive map: ensemble hippocampal sequences and decision making. Curr. Opin. Neurobiol. 32, 8–15 (2015).

    Article  CAS  PubMed  Google Scholar 

  11. Dudchenko, P. A. & Wood, E. R. Place fields and the cognitive map. Hippocampus 25, 709–712 (2015).

    Article  PubMed  Google Scholar 

  12. Redish, A. D. Beyond the Cognitive Map: From Place Cells to Episodic Memory (MIT Press, 1999).

    Book  Google Scholar 

  13. Gallagher, M., McMahan, R. & Schoenbaum, G. Orbitofrontal cortex and representation of incentive value in associative learning. J. Neurosci. 19, 6610–6614 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tremblay, L. & Schultz, W. Relative reward preference in primate orbitofrontal cortex. Nature 398, 704–708 (1999).

    Article  CAS  PubMed  Google Scholar 

  15. O'Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J. & Andrews, C. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat. Neurosci. 4, 95–102 (2001).

    Article  CAS  PubMed  Google Scholar 

  16. Gottfried, J. A., O'Doherty, J. & Dolan, R. J. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301, 1104–1107 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. Padoa-Schioppa, C. & Assad, J. A. Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223–226 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Wallis, J. D. Orbitofrontal cortex and its contribution to decision-making. Annu. Rev. Neurosci. 30, 31–56 (2007).

    Article  CAS  PubMed  Google Scholar 

  19. McDannald, M. A., Jones, J. L., Takahashi, Y. K. & Schoenbaum, G. Learning theory: a driving force in understanding orbitofrontal function. Neurobiol. Learn. Mem. 108, 22–27 (2014).

    Article  PubMed  Google Scholar 

  20. Thorpe, S., Rolls, E. & Maddison, S. The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp. Brain Res. 49, 93–115 (1983).

    Article  CAS  PubMed  Google Scholar 

  21. Takahashi, Y. K. et al. Expectancy-related changes in firing of dopamine neurons depend on orbitofrontal cortex. Nat. Neurosci. 14, 1590–1597 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Wilson, R. C., Takahashi, Y. K., Schoenbaum, G. & Niv, Y. Orbitofrontal cortex as a cognitive map of task space. Neuron 81, 267–279 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Fanselow, M. S. & Dong, H. W. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7–19 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Wallis, J. D. Cross-species studies of orbitofrontal cortex and value-based decision-making. Nat. Neurosci. 15, 13–19 (2012).

    Article  CAS  Google Scholar 

  25. Strange, B. A., Witter, M. P., Lein, E. S. & Moser, E. I. Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. 15, 655–669 (2014).

    Article  CAS  PubMed  Google Scholar 

  26. Andersen, P., Morris, R., Amaral, D., Bliss, T. & O'Keefe, J. The Hippocampus Book (Oxford Univ. Press, 2006).

    Book  Google Scholar 

  27. Komorowski, R. W., Manns, J. R. & Eichenbaum, H. Robust conjunctive item–place coding by hippocampal neurons parallels learning what happens where. J. Neurosci. 29, 9918–9929 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Manns, J. R. & Eichenbaum, H. A cognitive map for object memory in the hippocampus. Learn. Mem. 16, 616–624 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Fenton, A. A. et al. Attention-like modulation of hippocampus place cell discharge. J. Neurosci. 30, 4613–4625 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Moita, M. A., Rosis, S., Zhou, Y., LeDoux, J. E. & Blair, H. T. Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37, 485–497 (2003).

    Article  CAS  PubMed  Google Scholar 

  31. Larkin, M. C., Lykken, C., Tye, L. D., Wickelgren, J. G. & Frank, L. M. Hippocampal output area CA1 broadcasts a generalized novelty signal during an object–place recognition task. Hippocampus 24, 773–783 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Lever, C. et al. Environmental novelty elicits a later theta phase of firing in CA1 but not subiculum. Hippocampus 20, 229–234 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Quirk, G. J., Muller, R. U. & Kubie, J. L. The firing of hippocampal place cells in the dark depends on the rat's recent experience. J. Neurosci. 10, 2008–2017 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kennedy, P. J. & Shapiro, M. L. Motivational states activate distinct hippocampal representations to guide goal-directed behaviors. Proc. Natl Acad. Sci. USA 106, 10805–10810 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hollup, S. A., Molden, S., Donnett, J. G., Moser, M.-B. & Moser, E. I. Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J. Neurosci. 21, 1635–1644 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Hok, V. et al. Goal-related activity in hippocampal place cells. J. Neurosci. 27, 472–482 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Pfeiffer, B. E. & Foster, D. J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74–79 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Singer, A. C., Carr, M. F., Karlsson, M. P. & Frank, L. M. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron 77, 1163–1173 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Dragoi, G. & Tonegawa, S. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469, 397–401 (2011).

    Article  CAS  PubMed  Google Scholar 

  40. Ólafsdóttir, H. F., Barry, C., Saleem, A. B., Hassabis, D. & Spiers, H. J. Hippocampal place cells construct reward related sequences through unexplored space. eLife 4, e06063 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Barron, H. C., Dolan, R. J. & Behrens, T. E. J. Online evaluation of novel choices by simultaneous representation of multiple memories. Nat. Neurosci. 16, 1492–1498 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Tavares, R. M. et al. A map for social navigation in the human brain. Neuron 87, 231–243 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Bornstein, A. M. & Daw, N. D. Cortical and hippocampal correlates of deliberation during model-based decisions for rewards in humans. PLoS Comput. Biol. 9, e1003387 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Bornstein, A. M. & Daw, N. D. Dissociating hippocampal and striatal contributions to sequential prediction learning. Eur. J. Neurosci. 35, 1011–1023 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Schapiro, A. C., Turk-Browne, N. B., Norman, K. A. & Botvinick, M. M. Statistical learning of temporal community structure in the hippocampus. Hippocampus 26, 3–8 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Shohamy, D. & Turk-Browne, N. B. Mechanisms for widespread hippocampal involvement in cognition. J. Exp. Psychol. Gen. 142, 1159 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Ginther, M. R., Walsh, D. F. & Ramus, S. J. Hippocampal neurons encode different episodes in an overlapping sequence of odors task. J. Neurosci. 31, 2706–2711 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Allen, T. A., Salz, D. M., McKenzie, S. & Fortin, N. J. Nonspatial sequence coding in CA1 neurons. J. Neurosci. 36, 1547–1563 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. McNaughton, B. L., Barnes, C. A. & O'Keefe, J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 52, 41–49 (1983).

    Article  CAS  PubMed  Google Scholar 

  50. Stalnaker, T. A., Cooch, N. K. & Schoenbaum, G. What the orbitofrontal cortex does not do. Nat. Neurosci. 18, 620–627 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Padoa-Schioppa, C. Neurobiology of economic choice: a good-based model. Annu. Rev. Neurosci. 34, 333 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Schoenbaum, G., Roesch, M. R., Stalnaker, T. A. & Takahashi, Y. K. A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat. Rev. Neurosci. 10, 885–892 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. West, E. A., Forcelli, P. A., McCue, D. L. & Malkova, L. Differential effects of serotonin-specific and excitotoxic lesions of OFC on conditioned reinforcer devaluation and extinction in rats. Behav. Brain Res. 246, 10–14 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Rhodes, S. E. & Murray, E. A. Differential effects of amygdala, orbital prefrontal cortex, and prelimbic lesions on goal-directed behavior in rhesus macaques. J. Neurosci. 33, 3380–3389 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Izquierdo, A. D., Suda, R. K. & Murray, E. A. Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J. Neurosci. 24, 7540–7548 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Gremel, C. M. & Costa, R. M. Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat. Commun. 4, 2264 (2013).

    Article  PubMed  CAS  Google Scholar 

  57. Ostlund, S. B. & Balleine, B. W. Orbitofrontal cortex mediates outcome encoding in Pavlovian but not instrumental learning. J. Neurosci. 27, 4819–4825 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. McDannald, M. A., Saddoris, M. P., Gallagher, M. & Holland, P. C. Lesions of orbitofrontal cortex impair rats' differential outcome expectancy learning but not conditioned stimulus-potentiated feeding. J. Neurosci. 25, 4626–4632 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. McDannald, M. A., Lucantonio, F., Burke, K. A., Niv, Y. & Schoenbaum, G. Ventral striatum and orbitofrontal cortex are both required for model-based, but not model-free, reinforcement learning. J. Neurosci. 31, 2700–2705 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Redish, A. D., Jensen, S., Johnson, A. & Kurth-Nelson, Z. Reconciling reinforcement learning models with behavioral extinction and renewal: Implications for addiction, relapse, and problem gambling. Psychol. Rev. 114, 784–805 (2007).

    Article  PubMed  Google Scholar 

  61. Sutton, R. S. & Barto, A. G. Reinforcement Learning: An Introduction (MIT Press, 1998).

    Google Scholar 

  62. Gershman, S. J. & Niv, Y. Learning latent structure: carving nature at its joints. Curr. Opin. Neurobiol. 20, 251–256 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. O'Doherty, J. P., Lee, S. W. & McNamee, D. The structure of reinforcement-learning mechanisms in the human brain. Curr. Opin. Behav. Sci. 1, 94–100 (2015).

    Article  Google Scholar 

  64. Gershman, S. J., Blei, D. & Niv, Y. Context, learning and extinction. Psychol. Rev. 117, 197–209 (2010).

    Article  PubMed  Google Scholar 

  65. Courville, A. C., Daw, N. D. & Touretzky, D. S. Similarity and discrimination in classical conditioning: a latent variable account. Adv. Neural Inform. Process. Syst. 17, 313–320 (2005).

    Google Scholar 

  66. Ramus, S. J. & Eichenbaum, H. Neural correlates of olfactory recognition memory in the rat orbitofrontal cortex. J. Neurosci. 20, 8199–8208 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Schoenbaum, G. & Eichenbaum, H. Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in piriform cortex. J. Neurophysiol. 74, 733–750 (1995).

    Article  CAS  PubMed  Google Scholar 

  68. Steiner, A. P. & Redish, A. D. Behavioral and neurophysiological correlates of regret in rat decision-making on a neuroeconomic task. Nat. Neurosci. 17, 995–1002 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Steiner, A. P. & Redish, A. D. The road not taken: neural correlates of decision making in orbitofrontal cortex. Front. Neurosci. 6, 131 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Abe, H. & Lee, D. Distributed coding of actual and hypothetical outcomes in the orbital and dorsolateral prefrontal cortex. Neuron 70, 731–741 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Stalnaker, T. A. et al. Orbitofrontal neurons infer the value and identity of predicted outcomes. Nat. Commun. 5, 3926 (2014).

    Article  PubMed  CAS  Google Scholar 

  72. Tsujimoto, S., Genovesio, A. & Wise, S. P. Monkey orbitofrontal cortex encodes response choices near feedback time. J. Neurosci. 29, 2569–2574 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Tsujimoto, S. & Sawaguchi, T. Neuronal activity representing temporal prediction of reward in the primate prefrontal cortex. J. Neurophysiol. 93, 3687–3692 (2005).

    Article  PubMed  Google Scholar 

  74. Bradfield, L. A., Dezfouli, A., van Holstein, M., Chieng, B. & Balleine, B. W. Medial orbitofrontal cortex mediates outcome retrieval in partially observable task situations. Neuron 88, 1268–1280 (2015).

    Article  CAS  PubMed  Google Scholar 

  75. Gläscher, J., Daw, N., Dayan, P. & O'Doherty, J. P. States versus rewards: dissociable neural prediction error signals underlying model-based and model-free reinforcement learning. Neuron 66, 585–595 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Riceberg, J. S. & Shapiro, M. L. Reward stability determines the contribution of orbitofrontal cortex to adaptive behavior. J. Neurosci. 32, 16402–16409 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Doll, B. B., Duncan, K. D., Simon, D. A., Shohamy, D. & Daw, N. D. Model-based choices involve prospective neural activity. Nat. Neurosci. 18, 767–772 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Feierstein, C. E., Quirk, M. C., Uchida, N., Sosulski, D. L. & Mainen, Z. F. Representation of spatial goals in rat orbitofrontal cortex. Neuron 60, 495–507 (2006).

    Article  CAS  Google Scholar 

  79. Roesch, M. R., Taylor, A. R. & Schoenbaum, G. Encoding of time-discounted rewards in orbitofrontal cortex is independent of value representation. Neuron 51, 509–520 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Gupta, A. S., van der Meer, M. A., Touretzky, D. S. & Redish, A. D. Segmentation of spatial experience by hippocampal theta sequences. Nat. Neurosci. 15, 1032–1039 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Blumenthal, A., Steiner, A., Seeland, K. D. & Redish, A. D. Effects of pharmacological manipulations of NMDA-receptors on deliberation in the multiple-T task. Neurobiol. Learn. Mem. 95, 376–384 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Gupta, A. S., van der Meer, M. A., Touretzky, D. S. & Redish, A. D. Hippocampal replay is not a simple function of experience. Neuron 65, 695–705 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Johnson, A. & Redish, A. D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176–12189 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Tolman, E. C. Prediction of vicarious trial and error by means of the schematic sowbug. Psychol. Rev. 46, 318–336 (1939).

    Article  Google Scholar 

  85. Muenzinger, K. F. Vicarious trial and error at a point of choice: I. A general survey of its relation to learning efficiency. Pedagog. Semin. J. Genet. Psychol. 53, 75–86 (1938).

    Article  Google Scholar 

  86. Redish, A. D. Vicarious trial and error. Nat. Rev. Neurosci. 17, 147–159 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Wikenheiser, A. M. & Redish, A. D. Hippocampal theta sequences reflect current goals. Nat. Neurosci. 18, 289–294 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Bieri, K. W., Bobbitt, K. N. & Colgin, L. L. Slow and fast gamma rhythms coordinate different spatial coding modes in hippocampal place cells. Neuron 82, 670–681 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Simon, D. A. & Daw, N. D. Neural correlates of forward planning in a spatial decision task in humans. J. Neurosci. 31, 5526–5539 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Chadwick, M. J., Jolly, A. E., Amos, D. P., Hassabis, D. & Spiers, H. J. A goal direction signal in the human entorhinal/subicular region. Curr. Biol. 25, 87–92 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. Ferbinteanu, J., Shirvalkar, P. & Shapiro, M. L. Memory modulates journey-dependent coding in the rat hippocampus. J. Neurosci. 31, 9135–9146 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Young, J. J. & Shapiro, M. L. Dynamic coding of goal-directed paths by orbital prefrontal cortex. J. Neurosci. 31, 5989–6000 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Rich, E. L. & Shapiro, M. Rat prefrontal cortical neurons selectively code strategy switches. J. Neurosci. 29, 7208–7219 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Ferbinteanu, J. & Shapiro, M. L. Prospective and retrospective memory coding in the hippocampus. Neuron 40, 1227–1239 (2003).

    Article  CAS  PubMed  Google Scholar 

  95. Bahar, A. S. & Shapiro, M. L. Remembering to learn: independent place and journey coding mechanisms contribute to memory transfer. J. Neurosci. 32, 2191–2203 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Shapiro, M. L. & Ferbinteanu, J. Relative spike timing in pairs of hippocampal neurons distinguishes the beginning and end of journeys. Proc. Natl Acad. Sci. USA 103, 4287–4292 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Young, J. J. & Shapiro, M. L. The orbitofrontal cortex and response selection. Ann. NY Acad. Sci. 1239, 25–32 (2011).

    Article  PubMed  Google Scholar 

  98. Shapiro, M. L., Riceberg, J. S., Seip-Cammack, K. & Guise, K. G. in Space, Time and Memory in the Hippocampal Formation (eds Derdikman, D. & Knierim, J. J.) 517–560 (Springer, 2014).

    Book  Google Scholar 

  99. Farovik, A. et al. Orbitofrontal cortex encodes memories within value-based schemas and represents contexts that guide memory retrieval. J. Neurosci. 35, 8333–8344 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. McKenzie, S. et al. Hippocampal representation of related and opposing memories develop within distinct, hierarchically organized neural schemas. Neuron 83, 202–215 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Brogden, W. J. Sensory pre-conditioning. J. Exp. Psychol. 25, 323–332 (1939).

    Article  Google Scholar 

  102. Matsumoto, Y., Hirashima, D. & Mizunami, M. Analysis and modeling of neural processes underlying sensory preconditioning. Neurobiol. Learn. Mem. 101, 103–113 (2013).

    Article  PubMed  Google Scholar 

  103. Muller, D., Gerber, B., Hellstern, F., Hammer, M. & Menzel, R. Sensory preconditioning in honeybees. J. Exp. Biol. 203, 1351–1364 (2000).

    CAS  PubMed  Google Scholar 

  104. Port, R. L., Beggs, A. L. & Patterson, M. M. Hippocampal substrate of sensory associations. Physiol. Behav. 39, 643–647 (1987).

    Article  CAS  PubMed  Google Scholar 

  105. Hall, D. & Suboski, M. D. Sensory preconditioning and secord-order conditioning of alarm reactions in zebra danio fish (Brachydanio rerio). J. Comp. Psychol. 109, 76 (1995).

    Article  Google Scholar 

  106. Ward-Robinson, J. et al. Excitotoxic lesions of the hippocampus leave sensory preconditioning intact: implications for models of hippocampal functioning. Behav. Neurosci. 115, 1357–1362 (2001).

    Article  CAS  PubMed  Google Scholar 

  107. Yu, T., Lang, S., Birbaumer, N. & Kotchoubey, B. Neural correlates of sensory preconditioning: a preliminary fMRI investigation. Hum. Brain Mapp. 35, 1297–1304 (2014).

    Article  PubMed  Google Scholar 

  108. Wimmer, G. E. & Shohamy, D. Preference by association: how memory mechanisms in the hippocampus bias decisions. Science 338, 270–273 (2012).

    Article  CAS  PubMed  Google Scholar 

  109. Karn, H. W. Sensory pre-conditioning and incidental learning in human subjects. J. Exp. Psychol. 37, 540 (1947).

    Article  CAS  PubMed  Google Scholar 

  110. Kojima, S. et al. Sensory preconditioning for feeding response in the pond snail, Lymnaea stagnalis. Brain Res. 808, 113–115 (1998).

    Article  CAS  PubMed  Google Scholar 

  111. Port, R. L. & Patterson, M. M. Fimbrial lesions and sensory preconditioning. Behav. Neurosci. 98, 584 (1984).

    Article  CAS  PubMed  Google Scholar 

  112. Rescorla, R. A. & Cunningham, C. L. Within-compound flavor associations. J. Exp. Psychol. Anim. Behav. Process 4, 267–275 (1978).

    Article  CAS  PubMed  Google Scholar 

  113. Nicholson, D. A. & Freeman Jr, J. H. Lesions of the perirhinal cortex impair sensory preconditioning in rats. Behav. Brain Res. 112, 69–75 (2000).

    Article  CAS  PubMed  Google Scholar 

  114. Robinson, S., Keene, C. S., Iaccarino, H. F., Duan, D. & Bucci, D. J. Involvement of retrosplenial cortex in forming associations between multiple sensory stimuli. Behav. Neurosci. 125, 578 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Robinson, S. et al. Chemogenetic silencing of neurons in retrosplenial cortex disrupts sensory preconditioning. J. Neurosci. 34, 10982–10988 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Jones, J. L. et al. Orbitofrontal cortex supports behavior and learning using inferred but not cached values. Science 338, 953–956 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Abela, A. R. & Chudasama, Y. Dissociable contributions of the ventral hippocampus and orbitofrontal cortex to decision-making with a delayed or uncertain outcome. Eur. J. Neurosci. 37, 640–647 (2013).

    Article  PubMed  Google Scholar 

  118. Mariano, T. Y. et al. Impulsive choice in hippocampal but not orbitofrontal cortex-lesioned rats on a nonspatial decision-making maze task. Eur. J. Neurosci. 30, 472–484 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  119. Cheung, T. H. C. & Cardinal, R. N. Hippocampal lesions facilitate instrumental learning with delayed reinforcement but induce impulsive choice in rats. BMC Neurosci. 6, 36 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  120. Bett, D., Murdoch, L. H., Wood, E. R. & Dudchenko, P. A. Hippocampus, delay discounting, and vicarious trial-and-error. Hippocampus 25, 643–654 (2015).

    Article  PubMed  Google Scholar 

  121. O'Doherty, J. et al. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 11, 399–403 (2000).

    Article  CAS  PubMed  Google Scholar 

  122. West, E. A., DesJardin, J. T., Gale, K. & Malkova, L. Transient inactivation of orbitofrontal cortex blocks reinforcer devaluation in macaques. J. Neurosci. 31, 15128–15135 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. Schoenbaum, G. & Roesch, M. Orbitofrontal cortex, associative learning, and expectancies. Neuron 47, 633–636 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Higgs, S., Williamson, A. C., Rotshtein, P. & Humphreys, G. W. Sensory-specific satiety is intact in amnesics who eat multiple meals. Psychol. Sci. 19, 623–628 (2008).

    Article  PubMed  Google Scholar 

  125. Corbit, L. H., Ostlund, S. B. & Balleine, B. W. Sensitivity to instrumental contingency degradation is mediated by the entorhinal cortex and its efferents via the dorsal hippocampus. J. Neurosci. 22, 10976–10984 (2002).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Corbit, L. H. & Balleine, B. W. The role of the hippocampus in instrumental conditioning. J. Neurosci. 20, 4233–4239 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Chudasama, Y., Wright, K. S. & Murray, E. A. Hippocampal lesions in rhesus monkeys disrupt emotional responses but not reinforcer devaluation effects. Biol. Psychiatry 63, 1084–1091 (2008).

    Article  PubMed  Google Scholar 

  128. Machado, C. J. & Bachevalier, J. The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). Behav. Neurosci. 120, 761 (2006).

    Article  PubMed  Google Scholar 

  129. Reichelt, A. C., Lin, T. E., Harrison, J. J., Honey, R. C. & Good, M. A. Differential role of the hippocampus in response-outcome and context-outcome learning: evidence from selective satiation procedures. Neurobiol. Learn. Mem. 96, 248–253 (2011).

    Article  PubMed  Google Scholar 

  130. Carr, M. F., Jadhav, S. P. & Frank, L. M. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14, 147–153 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  131. Malhotra, S., Cross, R. W. & van der Meer, M. A. Theta phase precession beyond the hippocampus. Rev. Neurosci. 23, 39–65 (2012).

    Article  PubMed  Google Scholar 

  132. van der Meer, M., Kurth-Nelson, Z. & Redish, A. D. Information processing in decision-making systems. Neuroscientist 18, 342–359 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  133. Johnson, A., van der Meer, M. A. & Redish, A. D. Integrating hippocampus and striatum in decision-making. Curr. Opin. Neurobiol. 17, 692–697 (2007).

    Article  CAS  PubMed  Google Scholar 

  134. Kurth-Nelson, Z., Bickel, W. & Redish, A. D. A theoretical account of cognitive effects in delay discounting. Eur. J. Neurosci. 35, 1052–1064 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  135. Rolls, E., Sienkiewicz, Z. & Yaxley, S. Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur. J. Neurosci. 1, 53–60 (1989).

    Article  PubMed  Google Scholar 

  136. Rolls, E. T. The functions of the orbitofrontal cortex. Brain Cogn. 55, 11–29 (2004).

    Article  PubMed  Google Scholar 

  137. Pearson, J. M., Watson, K. K. & Platt, M. L. Decision making: the neuroethological turn. Neuron 82, 950–965 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  138. Watson, K. K. & Platt, M. L. Social signals in primate orbitofrontal cortex. Curr. Biol. 22, 2268–2273 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  139. Ross, R., LoPresti, M., Schon, K. & Stern, C. Role of the hippocampus and orbitofrontal cortex during the disambiguation of social cues in working memory. Cogn. Affect. Behav. Neurosci. 13, 900–915 (2013).

    Article  PubMed  Google Scholar 

  140. Eichenbaum, H. Memory on time. Trends Cogn. Sci. 17, 81–88 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  141. Eichenbaum, H. Time cells in the hippocampus: a new dimension for mapping memories. Nat. Rev. Neurosci. 15, 732–744 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. MacDonald, C. J., Lepage, K. Q., Eden, U. T. & Eichenbaum, H. Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron 71, 737–749 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  143. Johnson, A. & Crowe, D. Revisiting Tolman: theories and cognitive maps. Cognitive Critique 1, 43–72 (2009).

    Google Scholar 

  144. Tolman, E. C. There is more than one kind of learning. Psychol. Rev. 56, 144 (1949).

    Article  CAS  PubMed  Google Scholar 

  145. Tolman, E. C. The determiners of behavior at a choice point. Psychol. Rev. 45, 1–41 (1938).

    Article  Google Scholar 

  146. Tolman, E. C., Ritchie, B. F. & Kalish, D. Studies in spatial learning. I. Orientation and the short-cut. J. Exp. Psychol. 36, 13–24 (1946).

    Article  CAS  PubMed  Google Scholar 

  147. Tolman, E. C., Ritchie, B. F. & Kalish, D. Studies in spatial learning. II. Place learning versus response learning. J. Exp. Psychol. 36, 221–229 (1946).

    Article  CAS  PubMed  Google Scholar 

  148. Schiller, D. et al. Memory and space: towards an understanding of the cognitive map. J. Neurosci. 35, 13904–13911 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Rescorla, R. A. & Wagner, A. R. in Classical Conditioning II: Current Research and Theory (eds Black, A. H. & Prokasy, W. F.) 64–99 (Appleton-Century-Crofts, 1972).

    Google Scholar 

  150. Pearce, J. M. & Hall, G. A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol. Rev. 87, 532–552 (1980).

    Article  CAS  PubMed  Google Scholar 

  151. Mackintosh, N. J. A theory of attention: variations in the associability of stimuli with reinforcement. Psychol. Rev. 82, 276–298 (1975).

    Article  Google Scholar 

  152. Doll, B. B., Shohamy, D. & Daw, N. D. Multiple memory systems as substrates for multiple decision systems. Neurobiol. Learn. Mem. 117, 4–13 (2015).

    Article  PubMed  Google Scholar 

  153. Dayan, P. & Daw, N. D. Decision theory, reinforcement learning, and the brain. Cogn. Affect. Behav. Neurosci. 8, 429–453 (2008).

    Article  PubMed  Google Scholar 

  154. Balleine, B. W., Daw, N. D. & O'Doherty, J. P. in Neuroeconomics: Decision Making and the Brain (eds Glimcher, P. W. & Fehr, E.) 367–385 (Academic Press, 2008).

    Google Scholar 

  155. Daw, N. D., Niv, Y. & Dayan, P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat. Neurosci. 8, 1704–1711 (2005).

    Article  CAS  PubMed  Google Scholar 

  156. Jay, T. M. & Witter, M. P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 313, 574–586 (1991).

    Article  CAS  PubMed  Google Scholar 

  157. Barbas, H. & Blatt, G. J. Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus 5, 511–533 (1995).

    Article  CAS  PubMed  Google Scholar 

  158. Insausti, R. & Munoz, M. Cortical projections of the non-entorhinal hippocampal formation in the cynomolgus monkey (Macaca fascicularis). Eur. J. Neurosci. 14, 435–451 (2001).

    Article  CAS  PubMed  Google Scholar 

  159. Aggleton, J. P. & Christiansen, K. The subiculum: the heart of the extended hippocampal system. Prog. Brain Res. 219, 65–82 (2015).

    Article  PubMed  Google Scholar 

  160. Prasad, J. A. & Chudasama, Y. Viral tracing identifies parallel disynaptic pathways to the hippocampus. J. Neurosci. 33, 8494–8503 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  161. McKenna, J. T. & Vertes, R. P. Afferent projections to nucleus reuniens of the thalamus. J. Comp. Neurol. 480, 115–142 (2004).

    Article  PubMed  Google Scholar 

  162. Vertes, R. P., Hoover, W. B., Szigeti-Buck, K. & Leranth, C. Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res. Bull. 71, 601–609 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  163. Griffin, A. L. Role of the thalamic nucleus reuniens in mediating interactions between the hippocampus and medial prefrontal cortex during spatial working memory. Front. Syst. Neurosci. 9, 29 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  164. Varela, C., Kumar, S., Yang, J. Y. & Wilson, M. A. Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens. Brain Struct. Funct. 219, 911–929 (2014).

    Article  CAS  PubMed  Google Scholar 

  165. Mitchell, A. S. et al. Advances in understanding mechanisms of thalamic relays in cognition and behavior. J. Neurosci. 34, 15340–15346 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  166. Witter, M. P. et al. Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10, 398–410 (2000).

    Article  CAS  PubMed  Google Scholar 

  167. Schultz, W., Dayan, P. & Montague, R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).

    Article  CAS  PubMed  Google Scholar 

  168. Jo, Y. S. & Mizumori, S. J. Y. Prefrontal regulation of neuronal activity in the ventral tegmental area. Cereb. Cortex http://dx.doi.org/10.1093/cercor/bhv215 (2015).

  169. Luo, A. H., Tahsili-Fahadan, P., Wise, R. A., Lupica, C. R. & Aston-Jones, G. Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 333, 353–357 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  170. Fujisawa, S. & Buzsáki, G. A. 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72, 153–165 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  171. Groenewegen, H. J., Wright, C. I. & Beijer, A. V. J. in The Emotional Motor System (eds Holstege, G., Bandler, R. & Saper, C. B.) 485–512 (Elsevier, 1996).

    Book  Google Scholar 

  172. Mogenson, G. J., Jones, D. L. & Yim, C. Y. From motivation to action: Functional interface between the limbic system and the motor system. Prog. Neurobiol. 14, 69–97 (1980).

    Article  CAS  PubMed  Google Scholar 

  173. van der Meer, M. A. & Redish, A. D. Expectancies in decision making, reinforcement learning, and ventral striatum. Front. Neurosci. 4, 6 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  174. Lavoie, A. M. & Mizumori, S. J. Y. Spatial-, movement- and reward-sensitive discharge by medial ventral striatum neurons in rats. Brain Res. 638, 157–168 (1994).

    Article  CAS  PubMed  Google Scholar 

  175. van der Meer, M. A & Redish, A. D. Covert expectation-of-reward in rat ventral striatum at decision points. Front. Integr. Neurosci. 3, 1–15 (2009).

    PubMed  PubMed Central  Google Scholar 

  176. Miyazaki, K., Miwazaki, K. W. & Matsumoto, G. Different representation of forthcoming reward in nucleus accumbens and medial prefrontal cortex. Neuroreport 15, 721–726 (2003).

    Article  Google Scholar 

  177. van der Meer, M. A. A. & Redish, A. D. Theta phase precession in rat ventral striatum links place and reward information. J. Neurosci. 31, 2843–2854 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  178. Cooch, N. K. et al. Orbitofrontal lesions eliminate signalling of biological significance in cue-responsive ventral striatal neurons. Nat. Commun. 6, 7195 (2015).

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank members of the Schoenbaum laboratory for helpful discussions on the topics addressed here and for feedback on earlier versions of this manuscript. This work was supported by funding from the US National Institute on Drug Abuse at the Intramural Research Program. The opinions expressed in this article are the authors' own and do not reflect the view of the US National Institutes of Health, the US Department of Health and Human Services or the US government.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Andrew M. Wikenheiser or Geoffrey Schoenbaum.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Glossary

Economic value

An integrative measure of how good an outcome is to a decision maker that distils the many multidimensional features of that outcome into a unidimensional measure of worth.

Outcome devaluation

The process of rendering a normally appetitive outcome aversive, typically by pairing it with illness.

Place cells

Pyramidal neurons in the hippocampus that fire action potentials when an animal occupies or passes through particular portions of the environment.

Reinforcement-learning models

A collection of machine-learning models that are inspired by psychological learning theory and that are aimed at solving the problem of using experience of the world to guide future behaviour.

Representational similarity analysis

An analysis approach that quantifies the similarity (or dissimilarity) of neural ensemble representations evoked by different conditions.

Response inhibition

The active suppression of actions that are not adaptive in the current setting.

Specific satiety

A means of devaluing a particular outcome by allowing an animal unrestricted access to it before a test session.

Stimulus–stimulus associations

Associations that are formed between neutral stimuli in the environment in the absence of explicit reinforcement.

Vicarious trial and error

(VTE). A pause and orient pattern of behaviour that decision makers often show when deliberating over potential choices. This is thought to be an overt marker of covert, mental processes that simulate potential outcomes of each course of action.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wikenheiser, A., Schoenbaum, G. Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex. Nat Rev Neurosci 17, 513–523 (2016). https://doi.org/10.1038/nrn.2016.56

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn.2016.56

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing