Separate elements of episodic memory subserved by distinct hippocampal-prefrontal connections

Nature Neuroscience

Volumn 20, Issue 2, 2017, Pages 242-250

  Barker, Gareth R I ^a   Banks, Paul J ^a   Scott, Hannah ^a   Ralph, G Scott ^b   Mitrophanous, Kyriacos A ^b   Wong, Liang Fong ^a   Bashir, Zafar I ^a   Uney, James B ^a   Warburton, E Clea ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b OXFORD BIOMEDICA UK LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; EPISODIC MEMORY; FUNCTIONAL CONNECTIVITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; INTERMEDIATE HIPPOCAMPUS; MALE; MEDIAL PREFRONTAL CORTEX; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; PHARMACOGENETICS; PREFRONTAL CORTEX; PYRAMIDAL NERVE CELL; RAT; SPATIAL MEMORY; ANIMAL; NERVE CELL; NERVE CELL NETWORK; NERVE TRACT; PHYSIOLOGY;

ANIMALS; HIPPOCAMPUS; MALE; MEMORY, EPISODIC; NERVE NET; NEURAL PATHWAYS; NEURONS; PREFRONTAL CORTEX; RATS; SPATIAL MEMORY;

EID: 85008599044     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4472     Document Type: Article

References (55)

1. Tulving, E. Organisation of Memory (Academic, New York, 1972).
2. Diana, R.A., Yonelinas, A.P. & Ranganath, C. Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends Cogn. Sci. 11, 379-386 (2007).
3. Eichenbaum, H., Yonelinas, A.P. & Ranganath, C. The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123-152 (2007).
4. Eichenbaum, H.T. Memory Systems (MIT Press, Cambridge, Massachusetts, USA, 1994).
5. Dickerson, B.C. & Eichenbaum, H. The episodic memory system: neurocircuitry and disorders. Neuropsychopharmacology 35, 86-104 (2010).
6. King, D.R., de Chastelaine, M., Elward, R.L., Wang, T.H. & Rugg, M.D. Recollection-related increases in functional connectivity predict individual differences in memory accuracy. J. Neurosci. 35, 1763-1772 (2015).
7. Watrous, A.J., Tandon, N., Conner, C.R., Pieters, T. & Ekstrom, A.D. Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat. Neurosci. 16, 349-356 (2013).
8. Preston, A.R. & Eichenbaum, H. Interplay of hippocampus and prefrontal cortex in memory. Curr. Biol. 23, R764-R773 (2013).
9. Wheeler, M.A., Stuss, D.T. & Tulving, E. Frontal lobe damage produces episodic memory impairment. J. Int. Neuropsychol. Soc. 1, 525-536 (1995).
10. Duarte, A., Ranganath, C. & Knight, R.T. Effects of unilateral prefrontal lesions on familiarity, recollection, and source memory. J. Neurosci. 25, 8333-8337 (2005).
11. Nolde, S.F., Johnson, M.K. & Raye, C.L. The role of prefrontal cortex during tests of episodic memory. Trends Cogn. Sci. 2, 399-406 (1998).
12. Petrides, M. Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia 23, 601-614 (1985).
13. Ekstrom, A.D., Copara, M.S., Isham, E.A., Wang, W.C. & Yonelinas, A.P. Dissociable networks involved in spatial and temporal order source retrieval. Neuroimage 56, 1803-1813 (2011).
14. Buckner, R.L., Kelley, W.M. & Petersen, S.E. Frontal cortex contributes to human memory formation. Nat. Neurosci. 2, 311-314 (1999).
15. Barredo, J., Öztekin, I. & Badre, D. Ventral fronto-temporal pathway supporting cognitive control of episodic memory retrieval. Cereb. Cortex 25, 1004-1019 (2015).
16. Benchenane, K. et al. Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66, 921-936 (2010).
17. Dere, E., Huston, J.P. & De Souza Silva, M.A. Integrated memory for objects, places, and temporal order: evidence for episodic-like memory in mice. Neurobiol. Learn. Mem. 84, 214-221 (2005).
18. Good, M.A., Barnes, P., Staal, V., McGregor, A. & Honey, R.C. Context- but not familiarity-dependent forms of object recognition are impaired following excitotoxic hippocampal lesions in rats. Behav. Neurosci. 121, 218-223 (2007).
19. DeVito, L.M. & Eichenbaum, H. Distinct contributions of the hippocampus and medial prefrontal cortex to the "what-where-when" components of episodic-like memory in mice. Behav. Brain Res. 215, 318-325 (2010).
20. Condé, F., Maire-Lepoivre, E., Audinat, E. & Crépel, F. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. J. Comp. Neurol. 352, 567-593 (1995).
21. Hoover, W.B. & Vertes, R.P. Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct. Funct. 212, 149-179 (2007).
22. 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).
23. Ennaceur, A. One-trial object recognition in rats and mice: methodological and theoretical issues. Behav. Brain Res. 215, 244-254 (2010).
24. 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).
25. Koya, E. et al. Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization. Nat. Neurosci. 12, 1069-1073 (2009).
26. Cruz, F.C. et al. New technologies for examining the role of neuronal ensembles in drug addiction and fear. Nat. Rev. Neurosci. 14, 743-754 (2013).
27. Farquhar, D. et al. Suicide gene therapy using E. coli beta-galactosidase. Cancer Chemother. Pharmacol. 50, 65-70 (2002).
28. Dong, H.-W., Swanson, L.W., Chen, L., Fanselow, M.S. & Toga, A.W. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. USA 106, 11794-11799 (2009).
29. Barker, G.R.I. & Warburton, E.C. When is the hippocampus involved in recognition memory? J. Neurosci. 31, 10721-10731 (2011).
30. Navawongse, R. & Eichenbaum, H. Distinct pathways for rule-based retrieval and spatial mapping of memory representations in hippocampal neurons. J. Neurosci. 33, 1002-1013 (2013).
31. MacDonald, C.J., Carrow, S., Place, R. & Eichenbaum, H. Distinct hippocampal time cell sequences represent odor memories in immobilized rats. J. Neurosci. 33, 14607-14616 (2013).
32. Kraus, B.J., Robinson, R.J. II, White, J.A., Eichenbaum, H. & Hasselmo, M.E. Hippocampal "time cells": time versus path integration. Neuron 78, 1090-1101 (2013).
33. Eichenbaum, H. Time cells in the hippocampus: a new dimension for mapping memories. Nat. Rev. Neurosci. 15, 732-744 (2014).
34. Witter, M.P., Wouterlood, F.G., Naber, P.A. & Van Haeften, T. Anatomical organization of the parahippocampal-hippocampal network. Ann. NY Acad. Sci. 911, 1-24 (2000).
35. Naber, P.A., Lopes da Silva, F.H. & Witter, M.P. Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum. Hippocampus 11, 99-104 (2001).
36. Knierim, J.J., Neunuebel, J.P. & Deshmukh, S.S. Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local-global reference frames. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130369 (2013).
37. Ito, H.T. & Schuman, E.M. Functional division of hippocampal area CA1 via modulatory gating of entorhinal cortical inputs. Hippocampus 22, 372-387 (2012).
38. Kinnavane, L., Amin, E., Horne, M. & Aggleton, J.P. Mapping parahippocampal systems for recognition and recency memory in the absence of the rat hippocampus. Eur. J. Neurosci. 40, 3720-3734 (2014).
39. Henriksen, E.J. et al. Spatial representation along the proximodistal axis of CA1. Neuron 68, 127-137 (2010).
40. Bast, T., Wilson, I.A., Witter, M.P. & Morris, R.G.M. From rapid place learning to behavioral performance: a key role for the intermediate hippocampus. PLoS Biol. 7, 0730-0746 (2009).
41. Apergis-Schoute, J., Pinto, A. & Paré, D. Ultrastructural organization of medial prefrontal inputs to the rhinal cortices. Eur. J. Neurosci. 24, 135-144 (2006).
42. Xu, W. & Südhof, T.C. A neural circuit for memory specificity and generalization. Science 339, 1290-1295 (2013).
43. Lee, I., Yoganarasimha, D., Rao, G. & Knierim, J.J. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430, 456-459 (2004).
44. Neunuebel, J.P., Yoganarasimha, D., Rao, G. & Knierim, J.J. Conflicts between local and global spatial frameworks dissociate neural representations of the lateral and medial entorhinal cortex. J. Neurosci. 33, 9246-9258 (2013).
45. Knierim, J.J. & Neunuebel, J.P. Tracking the flow of hippocampal computation: Pattern separation, pattern completion, and attractor dynamics. Neurobiol. Learn. Mem. 129, 38-49 (2016).
46. Poppenk, J., Evensmoen, H.R., Moscovitch, M. & Nadel, L. Long-axis specialization of the human hippocampus. Trends Cogn. Sci. 17, 230-240 (2013).
47. Moser, M.-B. & Moser, E.I. Functional differentiation in the hippocampus. Hippocampus 8, 608-619 (1998).
48. Fanselow, M.S. & Dong, H.-W. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7-19 (2010).
49. 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).
50. Igarashi, K.M., Ito, H.T., Moser, E.I. & Moser, M.-B. Functional diversity along the transverse axis of hippocampal area CA1. FEBS Lett. 588, 2470-2476 (2014).
51. Swanson, L.W. Brain Maps: Structure of the Rat Brain (Elsevier, 1992).
52. Barker, G.R.I. et al. The different effects on recognition memory of perirhinal kainate and NMDA glutamate receptor antagonism: implications for underlying plasticity mechanisms. J. Neurosci. 26, 3561-3566 (2006).
53. Barker, G.R.I. & Warburton, E.C. NMDA receptor plasticity in the perirhinal and prefrontal cortices is crucial for the acquisition of long-term object-in-place associative memory. J. Neurosci. 28, 2837-2844 (2008).
54. Kerrigan, T.L., Brown, J.T. & Randall, A.D. Characterization of altered intrinsic excitability in hippocampal CA1 pyramidal cells of the Aβ-overproducing PDAPP mouse. Neuropharmacology 79, 515-524 (2014).
55. Booth, C.A., Brown, J.T. & Randall, A.D. Neurophysiological modification of CA1 pyramidal neurons in a transgenic mouse expressing a truncated form of disrupted-in-schizophrenia 1. Eur. J. Neurosci. 39, 1074-1090 (2014).