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Hippocampal brain-network coordination during volitional exploratory behavior enhances learning

Nature Neuroscience volume 14, pages 115–120 (2011)Cite this article

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Abstract

Exploratory behaviors during learning determine what is studied and when, helping to optimize subsequent memory performance. To elucidate the cognitive and neural determinants of exploratory behaviors, we manipulated the control that human subjects had over the position of a moving window through which they studied objects and their locations. Our behavioral, neuropsychological and neuroimaging data indicate that volitional control benefits memory performance and is linked to a brain network that is centered on the hippocampus. Increases in correlated activity between the hippocampus and other areas were associated with specific aspects of memory, which suggests that volitional control optimizes interactions among specialized neural systems through the hippocampus. Memory is therefore an active process that is intrinsically linked to behavior. Furthermore, brain structures that are typically seen as passive participants in memory encoding (for example, the hippocampus) are actually part of an active network that controls behavior dynamically as it unfolds.

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Figure 1: Volitional control enhances spatial and object-specific memory.
Figure 2: Volitional control confers no perceptual benefit.
Figure 3: Volitional control caused disproportionate memory enhancement with increasing study durations.
Figure 4: Volitional control does not benefit memory performance in amnesia subjects with hippocampal amnesia.
Figure 5: A coordinated brain network for volitional control.

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References

  1. Gibson, J.J. The Ecological Approach to Visual Perception (Houghton Mifflin, Boston, 1979).

  2. Held, R. Plasticity in sensory-motor systems. Sci. Am. 213, 84–94 (1965).

    Article  CAS  PubMed  Google Scholar 

  3. Neisser, U. Cognition and Reality: Principles and Implications of Cognitive Psychology (W.H. Freeman & Company, San Francisco, 1976).

  4. Piaget, J. The Origins of Intelligence in Children (Routledge and Kegan Paul, London, 1953).

  5. National Research Council. How People Learn (National Academies Press, Washington, DC, 1999).

  6. Metcalfe, J. Metacognitive judgments and control of study. Curr. Dir. Psychol. Sci. 18, 159–163 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Mackworth, N.H. & Morandi, A.J. The gaze selects informative details within pictures. Percept. Psychophys. 2, 547–552 (1967).

    Article  Google Scholar 

  8. Jonides, J. et al. The mind and brain of short-term memory. Annu. Rev. Psychol. 59, 193–224 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Chun, M.M. & Turk-Browne, N.B. Interactions between attention and memory. Curr. Opin. Neurobiol. 17, 177–184 (2007).

    Article  CAS  PubMed  Google Scholar 

  10. Cohen, N.J. & Squire, L.R. Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. Science 210, 207–210 (1980).

    Article  CAS  PubMed  Google Scholar 

  11. Squire, L.R. & Zola-Morgan, S. The medial temporal lobe memory system. Science 253, 1380–1386 (1991).

    Article  CAS  PubMed  Google Scholar 

  12. Koechlin, E. & Hyafil, A. Anterior prefrontal function and the limits of human decision-making. Science 318, 594–598 (2007).

    Article  CAS  PubMed  Google Scholar 

  13. Sakagami, M. & Watanabe, M. Integration of cognitive and motivational information in the primate lateral prefrontal cortex. Ann. NY Acad. Sci. 1104, 89–107 (2007).

    Article  PubMed  Google Scholar 

  14. Smith, E.E. & Jonides, J. Storage and executive processes in the frontal lobes. Science 283, 1657–1661 (1999).

    Article  CAS  PubMed  Google Scholar 

  15. Tanji, J. & Hoshi, E. Role of the lateral prefrontal cortex in executive behavioral control. Physiol. Rev. 88, 37–57 (2008).

    Article  PubMed  Google Scholar 

  16. Cabeza, R., Ciaramelli, E., Olson, I.R. & Moscovitch, M. The parietal cortex and episodic memory: an attentional account. Nat. Rev. Neurosci. 9, 613–625 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Uncapher, M.R. & Wagner, A.D. Posterior parietal cortex and episodic encoding: insights from fMRI subsequent memory effects and dual-attention theory. Neurobiol. Learn. Mem. 91, 139–154 (2009).

    Article  PubMed  Google Scholar 

  18. Held, R. & Hein, A. Movement-produced stimulation in the development of visually guided behavior. J. Comp. Physiol. Psychol. 56, 872–876 (1963).

    Article  CAS  PubMed  Google Scholar 

  19. Harman, K.L., Humphrey, G.K. & Goodale, M.A. Active manual control of object views facilitates visual recognition. Curr. Biol. 9, 1315–1318 (1999).

    Article  CAS  PubMed  Google Scholar 

  20. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, UK, 1978).

  21. Foster, T.C., Castro, C.A. & McNaughton, B.L. Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement. Science 244, 1580–1582 (1989).

    Article  CAS  PubMed  Google Scholar 

  22. Song, E.Y., Kim, Y.B., Kim, Y.H. & Jung, M.W. Role of active movement in place-specific firing of hippocampal neurons. Hippocampus 15, 8–17 (2005).

    Article  PubMed  Google Scholar 

  23. Eichenbaum, H. & Cohen, N.J. From Conditioning to Conscious Recollection: Memory Systems of the Brain (Oxford University Press, Oxford, UK, 2004).

  24. Allen, J.S., Tranel, D., Bruss, J. & Damasio, H. Correlations between regional brain volumes and memory performance in anoxia. J. Clin. Exp. Neuropsychol. 28, 457–476 (2006).

    Article  PubMed  Google Scholar 

  25. Konkel, A., Warren, D.E., Duff, M.C., Tranel, D.N. & Cohen, N.J. Hippocampal amnesia impairs all manner of relational memory. Front. Hum. Neurosci. 2, 15 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Friston, K.J. Functional and effective connectivity in neuroimaging: a synthesis. Hum. Brain Mapp. 2, 56–78 (1994).

    Article  Google Scholar 

  27. Kesner, R.P. The posterior parietal cortex and long-term memory representation of spatial information. Neurobiol. Learn. Mem. 91, 197–206 (2009).

    Article  PubMed  Google Scholar 

  28. Bellebaum, C. & Daum, I. Cerebellar involvement in executive control. Cerebellum 6, 184–192 (2007).

    Article  PubMed  Google Scholar 

  29. Chua, E.F., Schacter, D.L. & Sperling, R.A. Neural correlates of metamemory: a comparison of feeling-of-knowing and retrospective confidence judgments. J. Cogn. Neurosci. 21, 1751–1765 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Habas, C. et al. Distinct cerebellar contributions to intrinsic connectivity networks. J. Neurosci. 29, 8586–8594 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Krienen, F.M. & Buckner, R.L. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb. Cortex 19, 2485–2497 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kesner, R.P. & Rogers, J. An analysis of independence and interactions of brain substrates that subserve multiple attributes, memory systems, and underlying processes. Neurobiol. Learn. Mem. 82, 199–215 (2004).

    Article  PubMed  Google Scholar 

  33. Simons, J.S. & Spiers, H.J. Prefrontal and medial temporal lobe interactions in long-term memory. Nat. Rev. Neurosci. 4, 637–648 (2003).

    Article  CAS  PubMed  Google Scholar 

  34. Epstein, R.A. Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn. Sci. 12, 388–396 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Martin, A. The representation of object concepts in the brain. Annu. Rev. Psychol. 58, 25–45 (2007).

    Article  PubMed  Google Scholar 

  36. Tolman, E.C. Purposive Behavior in Animals and Men (Century, New York, 1932).

  37. Metcalfe, J. & Jacobs, W.J. People's study time allocation and its relation to animal foraging. Behav. Processes 83, 213–221 (2010).

    Article  PubMed  Google Scholar 

  38. Custers, R. & Aarts, H. The unconscious will: How the pursuit of goals operates outside of conscious awareness. Science 329, 47–50 (2010).

    Article  CAS  PubMed  Google Scholar 

  39. Shimamura, A.P. & Wickens, T.D. Superadditive memory strength for item and source recognition: the role of hierarchical relational binding in the medial temporal lobe. Psychol. Rev. 116, 1–19 (2009).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  41. Gupta, R. et al. Declarative memory is critical for sustained advantageous complex decision-making. Neuropsychologia 47, 1686–1693 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Bird, C.M. & Burgess, N. The hippocampus and memory: insights from spatial processing. Nat. Rev. Neurosci. 9, 182–194 (2008).

    Article  CAS  PubMed  Google Scholar 

  43. Van Hoesen, G.W., Rosene, D.L. & Mesulam, M.M. Subicular input from temporal cortex in the rhesus monkey. Science 205, 608–610 (1979).

    Article  CAS  PubMed  Google Scholar 

  44. 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 

  45. Roission, B. & Pourtois, G. Revisiting Snodgrass and Vanderwart's object set: the role of surface detail in basic-level object recognition. Perception 3, 217–236 (2004).

    Article  Google Scholar 

  46. Cox, R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162–173 (1996).

    Article  CAS  PubMed  Google Scholar 

  47. Insausti, R. et al. MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. AJNR Am. J. Neuroradiol. 19, 659–671 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Reber, P.J., Wong, E.C. & Buxton, R.B. Encoding activity in the medial temporal lobe examined with anatomically constrained fMRI analysis. Hippocampus 12, 363–376 (2002).

    Article  PubMed  Google Scholar 

  49. Voss, J.L., Hauner, K.K. & Paller, K.A. Establishing a relationship between activity reduction in human perirhinal cortex and priming. Hippocampus 19, 773–778 (2009).

    Article  PubMed  Google Scholar 

  50. Forman, S.D. et al. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33, 636–647 (1995).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Research was supported by a US National Institutes of Health (NIH) Pathway to Independence award (K99-NS069788) and a Beckman Institute Postdoctoral Fellowship Award to J.L.V., by funds from the Kiwanis Foundation to D.T.T., and by NIH grants MH062500 to N.J.C. and NS19632 to D.T.T.

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Authors and Affiliations

  1. Beckman Institute for Advanced Science and Technology, University of Illinois Urbana-Champaign, Urbana, Illinois, USA

    Joel L Voss, Brian D Gonsalves, Kara D Federmeier & Neal J Cohen

  2. Department of Neurology, Division of Cognitive Neuroscience, University of Iowa Carver College of Medicine, Iowa City, Iowa, USA

    Daniel Tranel

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  1. Joel L Voss
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Contributions

J.L.V., N.J.C., B.D.G. and K.D.F. conceived the experiments. J.L.V. designed and performed the experiments and analyzed data. D.T. provided access and support for testing subjects with amnesia. All authors co-wrote the paper, discussed results and commented on the manuscript.

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Correspondence to Joel L Voss.

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Voss, J., Gonsalves, B., Federmeier, K. et al. Hippocampal brain-network coordination during volitional exploratory behavior enhances learning. Nat Neurosci 14, 115–120 (2011). https://doi.org/10.1038/nn.2693

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