Functional correlates of the lateral and medial entorhinal cortex: Objects, path integration and local - Global reference frames

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1635, 2014, Pages

  Knierim, James J ^a   Neunuebel, Joshua P ^a   Deshmukh, Sachin S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Episodic memory; Lateral entorhinal cortex; Medial entorhinal cortex; Memory; Path integration

Indexed keywords

BRAIN; DATA ACQUISITION; NEUROLOGY; NUMERICAL MODEL; SENSORY SYSTEM;

ANIMAL; CYTOLOGY; ENTORHINAL CORTEX; EPISODIC MEMORY; HIPPOCAMPUS; HISTOLOGY; LATERAL ENTORHINAL CORTEX; MEDIAL ENTORHINAL CORTEX; MEMORY; NERVE CELL; NERVE TRACT; PATH INTEGRATION; PHYSIOLOGY; RAT; REVIEW; SPATIAL BEHAVIOR;

EPISODIC MEMORY; LATERAL ENTORHINAL CORTEX; MEDIAL ENTORHINAL CORTEX; MEMORY; PATH INTEGRATION;

ANIMALS; ENTORHINAL CORTEX; HIPPOCAMPUS; NEURAL PATHWAYS; NEURONS; RATS; SPATIAL BEHAVIOR;

EID: 84906921314     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0369     Document Type: Review

References (83)

1. O'Keefe J, Nadel L. 1978 The hippocampus as a cognitive map. Oxford, UK: Clarendon Press.
2. O'Keefe J. 1976 Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78-109. (doi:10.1016/0014-4886(76)90055-8)
3. O'Keefe J. 1999 Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus 9, 352-364. (doi:10.1002/(SICI)1098-1063(1999)9:4,352::AID-HIPO3.3.0.CO;2-1)
4. Shapiro ML, Eichenbaum H. 1999 Hippocampus as a memory map: synaptic plasticity and memory encoding by hippocampal neurons. Hippocampus 9, 365-384. (doi:10.1002/(SICI)1098-1063 (1999)9:4,365::AID-HIPO4.3.0.CO;2-T)
5. Burwell RD. 2000 The parahippocampal region: corticocortical connectivity. Ann. NY Acad. Sci. 911, 25-42. (doi:10.1111/j.1749-6632.2000.tb06717.x)
6. Manns JR, Eichenbaum H. 2006 Evolution of declarative memory. Hippocampus 16, 795-808. (doi:10.1002/hipo.20205)
7. Knierim JJ, Lee I, Hargreaves EL. 2006 Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus 16, 755-764. (doi:10.1002/hipo.20203)
8. Eichenbaum H, Yonelinas AP, Ranganath C. 2007 The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123-152. (doi:10.1146/ annurev.neuro.30.051606.094328)
9. Caballero-Bleda M, Witter MP. 1993 Regional and laminar organization of projections from the presubiculum and parasubiculum to the entorhinal cortex: an anterograde tracing study in the rat. J. Comp. Neurol. 328, 115-129. (doi:10.1002/cne.903280109)
10. Ishizuka N, Weber J, Amaral DG. 1990 Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J. Comp Neurol. 295, 580-623. (doi:10.1002/cne.902950407)
11. Scharfman HE. 2007 The CA3 'backprojection' to the dentate gyrus. Prog. Brain Res. 163, 627-637. (doi:10.1016/S0079-6123(07)63034-9)
12. Buckmaster PS, Wenzel HJ, Kunkel DD, Schwartzkroin PA. 1996 Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J. Comp. Neurol. 366, 271-292. (doi:10.1002/(SICI)1096-9861(19960304)366:2,270::AID-CNE7.3.0.CO;2-2)
13. Witter MP, Amaral DG. 2004 Hippocampal formation. In The rat nervous system, vol. 3, 3rd edn (ed. G Paxinos), pp. 635-704. Amsterdam, The Netherlands: Elsevier.
14. Amaral DG, Witter MP. 1989 The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571-591. (doi:10.1016/0306-4522(89)90424-7)
15. Witter MP, Wouterlood FG, Naber PA, Van Haeften T. 2000 Anatomical organization of the parahippocampal-hippocampal network. Ann. NY Acad. Sci. 911, 1-24. (doi:10.1111/j.1749-6632. 2000.tb06716.x)
16. Burwell RD. 2001 Borders and cytoarchitecture of the perirhinal and postrhinal cortices in the rat. J. Comp. Neurol. 437, 17-41. (doi:10.1002/cne.1267)
17. Deshmukh SS, Knierim JJ. 2012 Hippocampus. WIREs Cogn. Sci. 3, 231-251. (doi:10.1002/ wcs.1164)
18. Henriksen EJ, Colgin LL, Barnes CA, Witter MP, Moser MB, Moser EI. 2010 Spatial representation along the proximodistal axis of CA1. Neuron 68, 127-137. (doi:10.1016/j.neuron.2010.08.042)
19. Hargreaves EL, Rao G, Lee I, Knierim JJ. 2005 Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308, 1792-1794. (doi:10.1126/science.1110449)
20. Yoganarasimha D, Rao G, Knierim JJ. 2011 Lateral entorhinal neurons are not spatially selective in cuerich environments. Hippocampus 21, 1363-1374. (doi:10.1002/hipo.20839)
21. Deshmukh SS, Yoganarasimha D, Voicu H, Knierim JJ. 2010 Theta modulation in the medial and the lateral entorhinal cortex. J. Neurophysiol. 104, 994-1006. (doi:10.1152/jn.01141.2009)
22. Suzuki WA, Miller EK, Desimone R. 1997 Object and place memory in the macaque entorhinal cortex. J. Neurophysiol. 78, 1062-1081.
23. Gaffan D. 1998 Idiothetic input into object-place configuration as the contribution to memory of the monkey and human hippocampus: a review. Exp. Brain Res. 123, 201-209. (doi:10.1007/ s002210050562)
24. Redish AD, Touretzky DS. 1997 Cognitive maps beyond the hippocampus. Hippocampus 7, 15-35. (doi:10.1002/(SICI)1098-1063(1997)7:1,15::AIDHIPO3.3.0. CO;2-6)
25. Redish AD. 1999 Beyond the cognitive map: from place cells to episodic memory. Cambridge, MA: MIT Press.
26. Ungerleider LG, Mishkin M. 1982 Two cortical visual systems. In Analysis of visual behavior (eds DJ Ingle, MA Goodale, RJW Mansfield), pp. 549-586. Cambridge, MA: MIT Press.
27. Ungerleider LG, Haxby JV. 1994 'What' and 'where' in the human brain. Curr. Opin. Neurobiol. 4, 157-165. (doi:10.1016/0959-4388(94)90066-3)
28. Kravitz DJ, Saleem KS, Baker CI, Mishkin M. 2011 A new neural framework for visuospatial processing. Nat. Rev. Neurosci. 12, 217-230. (doi:10.1038/ nrn3008)
29. Kravitz DJ, Saleem KS, Baker CI, Ungerleider LG, Mishkin M. 2013 The ventral visual pathway: an expanded neural framework for the processing of object quality. Trends Cogn. Sci. 17, 26-49. (doi:10.1016/j.tics.2012.10.011)
30. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. 2004 Spatial representation in the entorhinal cortex. Science 305, 1258-1264. (doi:10.1126/science. 1099901)
31. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005 Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806. (doi:10. 1038/nature03721)
32. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI. 2006 Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758-762. (doi:10.1126/science.1125572)
33. Savelli F, Yoganarasimha D, Knierim JJ. 2008 Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18, 1270-1282. (doi:10.1002/ hipo.20511)
34. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008 Representation of geometric borders in the entorhinal cortex. Science 322, 1865-1868. (doi:10.1126/science.1166466)
35. Deshmukh SS, Knierim JJ. 2011 Representation of non-spatial and spatial information in the lateral entorhinal cortex. Front. Behav. Neurosci. 5, 69. (doi:10.3389/fnbeh.2011.00069)
36. Ferbinteanu J, Holsinger RM, McDonald RJ. 1999 Lesions of the medial or lateral perforant path have different effects on hippocampal contributions to place learning and on fear conditioning to context. Behav. Brain Res. 101, 65-84. (doi:10.1016/S0166-4328(98)00144-2)
37. Van Cauter T, Camon J, Alvernhe A, Elduayen C, Sargolini F, Save E. 2013 Distinct roles of medial and lateral entorhinal cortex in spatial cognition. Cereb. Cortex 23, 451-459. (doi:10.1093/cercor/ bhs033)
38. Wilson DI, Langston RF, Schlesiger MI, Wagner M, Watanabe S, Ainge JA. 2013 Lateral entorhinal cortex is critical for novel object-context recognition. Hippocampus 23, 352-366. (doi:10.1002/hipo. 22095)
39. Hunsaker MR, Chen V, Tran GT, Kesner RP. 2013 The medial and lateral entorhinal cortex both contribute to contextual and item recognition memory: a test of the binding of items and context model. Hippocampus 23, 380-391. (doi:10.1002/ hipo.22097)
40. Furtak SC, Ahmed OJ, Burwell RD. 2012 Single neuron activity and theta modulation in postrhinal cortex during visual object discrimination. Neuron 76, 976-988. (doi:10.1016/j.neuron.2012.10.039)
41. Deshmukh SS, Johnson JL, Knierim JJ. 2012 Perirhinal cortex represents nonspatial, but not spatial, information in rats foraging in the presence of objects: comparison with lateral entorhinal cortex. Hippocampus 22, 2045-2058. (doi:10.1002/ hipo.22046)
42. Deshmukh SS, Knierim JJ. 2013 Influence of local objects on hippocampal representations: landmark vectors and memory. Hippocampus 23, 253-267. (doi:10.1002/hipo.22101)
43. Weible AP, Rowland DC, Pang R, Kentros C. 2009 Neural correlates of novel object and novel location recognition behavior in the mouse anterior cingulate cortex. J. Neurophysiol. 102, 2055-2068. (doi:10.1152/jn.00214.2009)
44. Tsao A, Moser MB, Moser EI. 2013 Traces of experience in the lateral entorhinal cortex. Curr. Biol. 23, 399-405. (doi:10.1016/j.cub.2013.01.036)
45. Weible AP, Rowland DC, Monaghan CK, Wolfgang NT, Kentros CG. 2012 Neural correlates of long-term object memory in the mouse anterior cingulate cortex. J. Neurosci. 32, 5598-5608. (doi:10.1523/ JNEUROSCI.5265-11.2012)
46. Dolorfo CL, Amaral DG. 1998 Entorhinal cortex of the rat: organization of intrinsic connections. J. Comp. Neurol. 398, 49-82. (doi:10.1002/ (SICI)1096-9861(19980817)398:1,49::AIDCNE4.3.0. CO;2-9)
47. Witter MP, Canto CB, Couey JJ, Koganezawa N, O'Reilly KC. 2014 Architecture of spatial circuits in the hippocampal region. Phil. Trans. R. Soc. B 369, 20120515. (doi:10.1098/rstb.2012.0515)
48. Kloosterman F, Van Haeften T, Witter MP, Lopes DSF. 2003 Electrophysiological characterization of interlaminar entorhinal connections: an essential link for re-entrance in the hippocampal-entorhinal system. Eur. J. Neurosci. 18, 3037-3052. (doi:10. 1111/j.1460-9568.2003.03046.x)
49. Lisman JE. 2007 Role of the dual entorhinal inputs to hippocampus: a hypothesis based on cue/action (non-self/self) couplets. Prog. Brain Res. 163, 615-625. (doi:10.1016/S0079-6123(07)63033-7)
50. Neunuebel JP, Yoganarasimha D, Rao G, Knierim JJ. 2013 Conflicts between local and global spatial frameworks dissociate neural representations of the lateral and medial entorhinal cortex. J. Neurosci. 33, 9246-9258. (doi:10.1523/JNEUROSCI.0946-13.2013)
51. Witter MP, Moser EI. 2006 Spatial representation and the architecture of the entorhinal cortex. Trends Neurosci. 29, 671-678. (doi:10.1016/j.tins.2006.10. 003)
52. Hargreaves EL, Yoganarasimha D, Knierim JJ. 2007 Cohesiveness of spatial and directional representations recorded from neural ensembles in the anterior thalamus, parasubiculum, medial entorhinal cortex, and hippocampus. Hippocampus 17, 826-841. (doi:10.1002/hipo.20316)
53. Taube JS, Muller RU, Ranck Jr JB. 1990 Headdirection cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10, 436-447.
54. Zugaro MB, Berthoz A, Wiener SI. 2001 Background, but not foreground, spatial cues are taken as references for head direction responses by rat anterodorsal thalamus neurons. J. Neurosci. 21, RC154.
55. Yoganarasimha D, Yu X, Knierim JJ. 2006 Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J. Neurosci. 26, 622-631. (doi:10.1523/JNEUROSCI. 3885-05.2006)
56. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser MB. 2010 Grid cells in pre-and parasubiculum. Nat. Neurosci. 13, 987-994. (doi:10.1038/nn.2602)
57. Taube JS. 1995 Place cells recorded in the parasubiculum of freely moving rats. Hippocampus 5, 569-583. (doi:10.1002/hipo.450050608)
58. Cho J, Sharp PE. 2001 Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav. Neurosci. 115, 3-25. (doi:10.1037/ 0735-7044.115.1.3)
59. Cacucci F, Lever C, Wills TJ, Burgess N, O'Keefe J. 2004 Theta-modulated place-by-direction cells in the hippocampal formation in the rat. J. Neurosci. 24, 8265-8277. (doi:10.1523/JNEUROSCI.2635-04.2004)
60. Vanderwolf CH. 1969 Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407-418. (doi:10.1016/0013-4694(69)90092-3)
61. McNaughton BL, Barnes CA, O'Keefe J. 1983 The contributions of position, direction, and velocity to single unit activity in the hippocampus of freelymoving rats. Exp. Brain Res. 52, 41-49. (doi:10. 1007/BF00237147)
62. Wiener SI, Paul CA, Eichenbaum H. 1989 Spatial and behavioral correlates of hippocampal neuronal activity. J. Neurosci. 9, 2737-2763.
63. Hasselmo ME, Giocomo LM, Zilli EA. 2007 Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17, 1252-1271. (doi:10.1002/hipo. 20374)
64. Fuhs MC, Touretzky DS. 2006 A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 4266-4276. (doi:10.1523/ JNEUROSCI.4353-05.2006)
65. Burgess N, Barry C, O'Keefe J. 2007 An oscillatory interference model of grid cell firing. Hippocampus 17, 801-812. (doi:10.1002/hipo.20327)
66. Blair HT, Gupta K, Zhang K. 2008 Conversion of a phase-to a rate-coded position signal by a threestage model of theta cells, grid cells, and place cells. Hippocampus 18, 1239-1255. (doi:10. 1002/hipo.20509)
67. Samsonovich A, McNaughton BL. 1997 Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900-5920.
68. Whishaw IQ. 1998 Place learning in hippocampal rats and the path integration hypothesis. Neurosci. Biobehav. Rev. 22, 209-220. (doi:10.1016/S0149-7634(97)00002-X)
69. McNaughton BL, Chen LL, Markus EJ. 1991 'Dead reckoning', landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J. Cogn. Neurosci. 3, 190-202. (doi:10.1162/jocn.1991.3.2.190)
70. Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL. 1995 A model of the neural basis of the rat's sense of direction. Adv. Neural Inf. Process Syst. 7, 173-180.
71. Zhang K. 1996 Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 16, 2112-2126.
72. Knierim JJ, Hamilton DA. 2011 Framing spatial cognition: neural representations of proximal and distal frames of reference and their roles in navigation. Physiol. Rev. 91, 1245-1279. (doi:10.1152/physrev.00021.2010)
73. Taube JS. 2007 The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181-207. (doi:10.1146/annurev.neuro.29. 051605.112854)
74. Epstein R, Kanwisher N. 1998 A cortical representation of the local visual environment. Nature 392, 598-601. (doi:10.1038/33402)
75. Epstein RA, Parker WE, Feiler AM. 2007 Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J. Neurosci. 27, 6141-6149. (doi:10.1523/ JNEUROSCI.0799-07.2007)
76. Zhu XO, Brown MW, Aggleton JP. 1995 Neuronal signalling of information important to visual recognition memory in rat rhinal and neighbouring cortices. Eur. J. Neurosci. 7, 753-765. (doi:10.1111/ j.1460-9568.1995.tb00679.x)
77. Norman G, Eacott MJ. 2005 Dissociable effects of lesions to the perirhinal cortex and the postrhinal cortex on memory for context and objects in rats. Behav. Neurosci. 119, 557-566. (doi:10.1037/0735-7044.119.2.557)
78. Bussey TJ, Saksida LM, Murray EA. 2005 The perceptual-mnemonic/feature conjunction model of perirhinal cortex function. Q. J. Exp. Psychol. B. 58, 269-282. (doi:10.1080/02724990544000004)
79. Burke SN, Maurer AP, Hartzell AL, Nematollahi S, Uprety A, Wallace JL, Barnes CA. 2012 Representation of three-dimensional objects by the rat perirhinal cortex. Hippocampus 22, 2032-2044. (doi:10.1002/hipo.22060)
80. Konkle T, Oliva A. 2012 A real-world size organization of object responses in occipitotemporal cortex. Neuron 74, 1114-1124. (doi:10.1016/j. neuron.2012.04.036)
81. Kajiwara R, Takashima I, Mimura Y, Witter MP, Iijima T. 2003 Amygdala input promotes spread of excitatory neural activity from perirhinal cortex to the entorhinal-hippocampal circuit. J. Neurophysiol. 89, 2176-2184. (doi:10.1152/jn.01033.2002)
82. de Curtis M, Pare D. 2004 The rhinal cortices: a wall of inhibition between the neocortex and the hippocampus. Prog. Neurobiol. 74, 101-110. (doi:10.1016/j.pneurobio.2004.08.005)
83. Morris RG, Frey U. 1997 Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Phil. Trans. R. Soc. Lond. B 352, 1489-1503. (doi:10.1098/rstb.1997.0136)