Perirhinal and Postrhinal Functional Inputs to the Hippocampus

Abstract

There is widespread agreement that perirhinal (PER) and postrhinal (POR) cortices are essential for episodic memory. The conventional view is that PER provides object information, and POR provides spatial and contextual information to the hippocampus through different information streams to support episodic memory. There is, however, considerable integration across these two information streams. Moreover, PER and POR also participate in non-mnemonic cognitive processes. PER is necessary for object recognition memory and is involved in high-level perceptual processing that conjoins elemental features to represent unique objects and items. POR represents the spatial layout of the current context, including objects and patterns located in that context, and then monitors the context for changes. Such object and pattern information in POR most likely arrives via a direct PER to POR pathway. Thus, the PER provides object information to both the POR and to the hippocampus, but for different purposes. Object information in POR would be used to represent and update the spatial layout of physical features of the local environment and for forming contextual associations. Such contextual information from the POR together with object and item information from the PER are made available to the hippocampus for associative learning and episodic memory.

References

  1. Aggleton JP, Kyd RJ, Bilkey DK (2004) When is the perirhinal cortex necessary for the performance of spatial memory tasks? Neurosci Biobehav Rev 28(6):611–624. doi:10.1016/j.neubiorev.2004.08.007 PubMedGoogle Scholar
  2. Aggleton JP, Albasser MM, Aggleton DJ, Poirier GL, Pearce JM (2010) Lesions of the rat perirhinal cortex spare the acquisition of a complex configural visual discrimination yet impair object recognition. Behav Neurosci 124(1):55–68PubMedCentralPubMedGoogle Scholar
  3. Albasser MM, Poirier GL, Aggleton JP (2010) Qualitatively different modes of perirhinal– hippocampal engagement when rats explore novel vs. familiar objects as revealed by c-Fos imaging. Eur J Neurosci 31(1):134–147. doi:10.1111/j.1460-9568.2009.07042.x PubMedGoogle Scholar
  4. Anagnostaras SG, Maren S, Fanselow MS (1999) Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J Neurosci 19(3):1106–1114PubMedGoogle Scholar
  5. Bang SJ, Brown TH (2009) Perirhinal cortex supports acquired fear of auditory objects. Neurobiol Learn Mem 92(1):53–62. doi:10.1016/j.nlm.2009.01.002 PubMedCentralPubMedGoogle Scholar
  6. Barker GRI, Warburton EC (2011) When is the hippocampus involved in recognition memory? J Neurosci 31(29):10721–10731. doi:10.1523/jneurosci.6413-10.2011 PubMedGoogle Scholar
  7. Barker GR, Warburton EC, Koder T, Dolman NP, More JC, Aggleton JP, Bashir ZI, Auberson YP, Jane DE, Brown MW (2006) The different effects on recognition memory of perirhinal kainate and NMDA glutamate receptor antagonism: implications for underlying plasticity mechanisms. J Neurosci 26(13):3561–3566. doi:10.1523/JNEUROSCI.3154-05.2006 PubMedGoogle Scholar
  8. Barker GRI, Bird F, Alexander V, Warburton EC (2007) Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J Neurosci 27(11):2948–2957. doi:10.1523/jneurosci.5289-06.2007 PubMedGoogle Scholar
  9. Bartko SJ, Winters BD, Cowell RA, Saksida LM, Bussey TJ (2007a) Perceptual functions of perirhinal cortex in rats: zero-delay object recognition and simultaneous oddity discriminations. J Neurosci 27(10):2548–2559. doi:10.1523/JNEUROSCI.5171-06.2007 PubMedGoogle Scholar
  10. Bartko SJ, Winters BD, Cowell RA, Saksida LM, Bussey TJ (2007b) Perirhinal cortex resolves feature ambiguity in configural object recognition and perceptual oddity tasks. Learn Mem 14(12):821–832. doi:10.1101/lm.749207 PubMedCentralPubMedGoogle Scholar
  11. Biedenkapp JC, Rudy JW (2009) Hippocampal and extrahippocampal systems compete for control of contextual fear: role of ventral subiculum and amygdala. Learn Mem 16(1):38–45. doi:10.1101/lm.1099109 PubMedCentralPubMedGoogle Scholar
  12. Bogacz R, Brown MW (2003) Comparison of computational models of familiarity discrimination in the perirhinal cortex. Hippocampus 13(4):494–524. doi:10.1002/hipo.10093 PubMedGoogle Scholar
  13. Broadbent NJ, Gaskin S, Squire LR, Clark RE (2010) Object recognition memory and the rodent hippocampus. Learn Mem 17(1):5–11. doi:10.1101/lm.1650110 PubMedCentralPubMedGoogle Scholar
  14. Brown MW, Wilson FAW, Riches IP (1987) Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory. Brain Res 409(1):158–162. doi:10.1016/0006-8993(87)90753-0 PubMedGoogle Scholar
  15. Brown MW, Barker GRI, Aggleton JP, Warburton EC (2012) What pharmacological interventions indicate concerning the role of the perirhinal cortex in recognition memory. Neuropsychologia 50(13):3122–3140. doi:10.1016/j.neuropsychologia.2012.07.034 PubMedCentralPubMedGoogle Scholar
  16. Bucci DJ, Burwell RD (2004) Deficits in attentional orienting following damage to the perirhinal or postrhinal cortices. Behav Neurosci 118(5):1117–1122. doi:10.1037/0735-7044.118.5.1117 PubMedGoogle Scholar
  17. Bucci DJ, Phillips RG, Burwell RD (2000) Contributions of postrhinal and perirhinal cortex to contextual information processing. Behav Neurosci 114(5):882–894PubMedGoogle Scholar
  18. Bucci DJ, Saddoris MP, Burwell RD (2002) Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. Behav Neurosci 116(3):479–488PubMedGoogle Scholar
  19. Buckley MJ, Gaffan D, Murray EA (1997) Functional double dissociation between two inferior temporal cortical areas: perirhinal cortex versus middle temporal gyrus. J Neurophysiol 77(2):587–598PubMedGoogle Scholar
  20. Burke SN, Maurer AP, Nematollahi S, Uprety AR, Wallace JL, Barnes CA (2011) The influence of objects on place field expression and size in distal hippocampal CA1. Hippocampus 21(7):783–801. doi:10.1002/hipo.20929 PubMedCentralPubMedGoogle Scholar
  21. 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(10):2032–2044. doi:10.1002/hipo.22060 PubMedCentralPubMedGoogle Scholar
  22. Burwell RD (2001) Borders and cytoarchitecture of the perirhinal and postrhinal cortices in the rat. J Comp Neurol 437(1):17–41PubMedGoogle Scholar
  23. Burwell RD, Agster KL (2008) Anatomy of the hippocampus and the declarative memory system. In: Eichenbaum H (ed) Memory systems, vol 3. Learning and memory: a comprehensive reference. Learning and memory: a comprehensive reference. Elsevier, Oxford, pp 47–66Google Scholar
  24. Burwell RD, Amaral DG (1998a) Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol 398(2):179–205PubMedGoogle Scholar
  25. Burwell RD, Amaral DG (1998b) Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J Comp Neurol 391(3):293–321. doi:10.1002/(SICI)1096-9861(19980216)391:3<293::AID-CNE2>3.0.CO;2-X PubMedGoogle Scholar
  26. Burwell RD, Hafeman DM (2003) Positional firing properties of postrhinal cortex neurons. Neuroscience 119(2):577–588PubMedGoogle Scholar
  27. Burwell RD, Witter MP, Amaral DG (1995) Perirhinal and postrhinal cortices of the rat: a review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5(5):390–408. doi:10.1002/hipo.450050503 PubMedGoogle Scholar
  28. Burwell RD, Shapiro ML, O’Malley MT, Eichenbaum H (1998) Positional firing properties of perirhinal cortex neurons. Neuroreport 9(13):3013–3018PubMedGoogle Scholar
  29. Burwell RD, Bucci DJ, Sanborn MR, Jutras MJ (2004a) Perirhinal and postrhinal contributions to remote memory for context. J Neurosci 24(49):11023–11028. doi:10.1523/JNEUROSCI.3781-04.2004 PubMedGoogle Scholar
  30. Burwell RD, Saddoris MP, Bucci DJ, Wiig KA (2004b) Corticohippocampal contributions to spatial and contextual learning. J Neurosci 24(15):3826–3836. doi:10.1523/JNEUROSCI.0410-04.2004 PubMedGoogle Scholar
  31. Bussey TJ, Saksida LM (2002) The organization of visual object representations: a connectionist model of effects of lesions in perirhinal cortex. Eur J Neurosci 15(2):355–364. doi:10.1046/j.0953-816x.2001.01850.x PubMedGoogle Scholar
  32. Bussey TJ, Saksida LM, Murray EA (2002) Perirhinal cortex resolves feature ambiguity in complex visual discriminations. Eur J Neurosci 15(2):365–374. doi:10.1046/j.0953-816x.2001.01851.x PubMedGoogle Scholar
  33. Campbell CBG, Hodos W (1970) The concept of homology and the evolution of the nervous system. Brain Behav Evol 3:353–367PubMedGoogle Scholar
  34. Campolattaro MM, Freeman JH (2006a) Perirhinal cortex lesions impair feature-negative discrimination. Neurobiol Learn Mem 86(2):205–213. doi:10.1016/j.nlm.2006.03.001 PubMedCentralPubMedGoogle Scholar
  35. Campolattaro MM, Freeman JH (2006b) Perirhinal cortex lesions impair simultaneous but not serial feature-positive discrimination learning. Behav Neurosci 120(4):970–975. doi:10.1037/0735-7044.120.4.970 PubMedCentralPubMedGoogle Scholar
  36. Chrobak JJ, Amaral DG (2007) Entorhinal cortex of the monkey: VII. Intrinsic connections. J Comp Neurol 500(4):612–633. doi:10.1002/cne.21200 PubMedGoogle Scholar
  37. Clark Robert E, Reinagel P, Broadbent Nicola J, Flister Erik D, Squire Larry R (2011) Intact performance on feature-ambiguous discriminations in rats with lesions of the perirhinal cortex. Neuron 70(1):132–140. doi:10.1016/j.neuron.2011.03.007 PubMedCentralPubMedGoogle Scholar
  38. Corodimas KP, LeDoux JE (1995) Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: contributions of contextual cues. Behav Neurosci 109(4):613–619PubMedGoogle Scholar
  39. Cowell RA, Bussey TJ, Saksida LM (2006) Why does brain damage impair memory? A connectionist model of object recognition memory in perirhinal cortex. J Neurosci 26(47):12186–12197. doi:10.1523/jneurosci.2818-06.2006 PubMedGoogle Scholar
  40. Cowell RA, Bussey TJ, Saksida LM (2010) Components of recognition memory: dissociable cognitive processes or just differences in representational complexity? Hippocampus 20(11):1245–1262. doi:10.1002/hipo.20865 PubMedGoogle Scholar
  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(10):2045–2058. doi:10.1002/hipo.22046 PubMedGoogle Scholar
  42. Deshmukh SS, Knierim JJ (2014) Spatial and nonspatial representations in the lateral entorhinal cortex. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  43. Dix SL, Aggleton JP (1999) Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res 99(2):191–200. doi:10.1016/S0166-4328(98)00079-5 PubMedGoogle Scholar
  44. Dolorfo CL, Amaral DG (1998a) Entorhinal cortex of the rat: organization of intrinsic connections. J Comp Neurol 398(1):49–82. doi:10.1002/(SICI)1096-9861(19980817)398:1<49::AID-CNE4>3.0.CO;2-9 PubMedGoogle Scholar
  45. Dolorfo CL, Amaral DG (1998b) Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J Comp Neurol 398(1):25–48PubMedGoogle Scholar
  46. Eacott MJ, Gaffan EA (2005) The roles of perirhinal cortex, postrhinal cortex, and the fornix in memory for objects, contexts, and events in the rat. Quart J Exp Psychol B 58(3–4):202–217. doi:10.1080/02724990444000203 Google Scholar
  47. Eacott MJ, Gaffan D, Murray EA (1994) Preserved recognition memory for small sets, and impaired stimulus identification for large sets, following rhinal cortex ablations in monkeys. Eur J Neurosci 6(9):1466–1478PubMedGoogle Scholar
  48. Eacott MJ, Machin PE, Gaffan EA (2001) Elemental and configural visual discrimination learning following lesions to perirhinal cortex in the rat. Behav Brain Res 124(1):55–70. doi:10.1016/S0166-4328(01)00234-0 PubMedGoogle Scholar
  49. Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30:123–152PubMedCentralPubMedGoogle Scholar
  50. Eichenbaum H, MacDonald CJ, Kraus BJ (2014) Time and the hippocampus. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  51. Ennaceur A, Aggleton JP (1997) The effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat. Behav Brain Res 88(2):181–193. doi:10.1016/S0166-4328(97)02297-3 PubMedGoogle Scholar
  52. Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31(1):47–59. doi:10.1016/0166-4328(88)90157-X PubMedGoogle Scholar
  53. Ennaceur A, Neave N, Aggleton JP (1996) Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80(1–2):9–25. doi:10.1016/0166-4328(96)00006-X PubMedGoogle Scholar
  54. Epstein R, Harris A, Stanley D, Kanwisher N (1999) The parahippocampal place area: recognition, navigation, or encoding? Neuron 23(1):115–125PubMedGoogle Scholar
  55. Fahy FL, Riches IP, Brown MW (1993) Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex. Exp Brain Res 96(3):457–472PubMedGoogle Scholar
  56. Feinberg LM, Allen TA, Ly D, Fortin NJ (2012) Recognition memory for social and non-social odors: differential effects of neurotoxic lesions to the hippocampus and perirhinal cortex. Neurobiol Learn Mem 97(1):7–16. doi:10.1016/j.nlm.2011.08.008 PubMedGoogle Scholar
  57. Forwood SE, Winters BD, Bussey TJ (2005) Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 15(3):347–355. doi:10.1002/hipo.20059 PubMedGoogle Scholar
  58. Forwood SE, Bartko SJ, Saksida LM, Bussey TJ (2007) Rats spontaneously discriminate purely visual, two-dimensional stimuli in tests of recognition memory and perceptual oddity. Behav Neurosci 121(5):1032–1042. doi:10.1037/0735-7044.121.5.1032 PubMedGoogle Scholar
  59. Frankland PW, Cestari V, Filipkowski RK, McDonald RJ, Silva AJ (1998) The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 112(4):863–874PubMedGoogle Scholar
  60. Furtak SC, Ahmed OJ, Burwell RD (2012) Single neuron activity and theta modulation in postrhinal cortex during visual object discrimination. Neuron 76(5):976–988. doi:10.1016/j.neuron.2012.10.039 PubMedCentralPubMedGoogle Scholar
  61. Futter JE, Davies M, Bilkey DK, Aggleton JP (2006) The effects of cytotoxic perirhinal cortex lesions on spatial learning by rats: a comparison of the dark agouti and Sprague–Dawley strains. Behav Neurosci 120(1):150–161. doi:10.1037/0735-7044.120.1.150 PubMedGoogle Scholar
  62. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305(5688):1258–1264. doi:10.1126/science.1099901 PubMedGoogle Scholar
  63. Griffiths S, Scott H, Glover C, Bienemann A, Ghorbel MT, Uney J, Brown MW, Warburton EC, Bashir ZI (2008) Expression of long-term depression underlies visual recognition memory. Neuron 58(2):186–194PubMedGoogle Scholar
  64. Hargreaves EL, Rao G, Lee I, Knierim JJ (2005) Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308(5729):1792–1794. doi:10.1126/science.1110449 PubMedGoogle Scholar
  65. Insausti R, Herrero MT, Witter MP (1997) Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7(2):146–183. doi:10.1002/(SICI)1098-1063(1997)7:2&amp;lt;146::AID-HIPO4&amp;gt;3.0.CO;2-L PubMedGoogle Scholar
  66. Kent BW, Burwell RD (2012) Single units in the postrhinal cortex signal changes in context. In: Society for Neuroscience, New Orleans, 13–17 October, 2012Google Scholar
  67. Kholodar-Smith DB, Allen TA, Brown TH (2008a) Fear conditioning to discontinuous auditory cues requires perirhinal cortical function. Behav Neurosci 122(5):1178–1185. doi:10.1037/a0012902 PubMedGoogle Scholar
  68. Kholodar-Smith DB, Boguszewski P, Brown TH (2008b) Auditory trace fear conditioning requires perirhinal cortex. Neurobiol Learn Mem 90(3):537–543. doi:10.1016/j.nlm.2008.06.006 PubMedCentralPubMedGoogle Scholar
  69. Knierim JJ, Lee I, Hargreaves EL (2006) Hippocampal place cells: parallel input streams, subregional processing, and implications for episodic memory. Hippocampus 16(9):755–764. doi:10.1002/hipo.20203 PubMedGoogle Scholar
  70. Knierim JJ, Neunuebel JP, Deshmukh SS (2014) Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local–global reference frames. Philos Trans R Soc B (in press)Google Scholar
  71. Komorowski RW, Manns JR, Eichenbaum H (2009) Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. J Neurosci 29(31):9918–9929. doi:10.1523/JNEUROSCI.1378-09.2009 PubMedCentralPubMedGoogle Scholar
  72. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445(7124):168–176. doi:10.1038/nature05453 PubMedGoogle Scholar
  73. Liu P, Bilkey DK (1998a) Excitotoxic lesions centered on perirhinal cortex produce delay-dependent deficits in a test of spatial memory. Behav Neurosci 112(3):512–524PubMedGoogle Scholar
  74. Liu P, Bilkey DK (1998b) Lesions of perirhinal cortex produce spatial memory deficits in the radial maze. Hippocampus 8(2):114–121. doi:10.1002/(SICI)1098-1063(1998)8:2&lt;114::AID-HIPO3&gt;3.0.CO;2-L PubMedGoogle Scholar
  75. Liu P, Bilkey DK (1998c) Perirhinal cortex contributions to performance in the Morris water maze. Behav Neurosci 112(2):304–315PubMedGoogle Scholar
  76. Liu P, Bilkey DK (1999) The effect of excitotoxic lesions centered on the perirhinal cortex in two versions of the radial arm maze task. Behav Neurosci 113(4):672–682PubMedGoogle Scholar
  77. Liu P, Bilkey DK (2001) The effect of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks. Behav Neurosci 115(1):94–111PubMedGoogle Scholar
  78. Liu Z, Richmond BJ (2000) Response differences in monkey TE and perirhinal cortex: stimulus association related to reward schedules. J Neurophysiol 83(3):1677–1692PubMedGoogle Scholar
  79. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84(1):87–136PubMedGoogle Scholar
  80. MacDonald Christopher J, Lepage Kyle Q, Eden Uri T, Eichenbaum H (2011) Hippocampal “Time Cells” bridge the gap in memory for discontiguous events. Neuron 71(4):737–749. doi:10.1016/j.neuron.2011.07.012 PubMedCentralPubMedGoogle Scholar
  81. Machin P, Vann SD, Muir JL, Aggleton JP (2002) Neurotoxic lesions of the rat perirhinal cortex fail to disrupt the acquisition or performance of tests of allocentric spatial memory. Behav Neurosci 116(2):232–240PubMedGoogle Scholar
  82. Mandler G (1980) Recognizing: the judgment of previous occurrence. Psychol Rev 87(3):252–271Google Scholar
  83. Maren S, Fanselow MS (1997) Electrolytic lesions of the fimbria/fornix, dorsal hippocampus, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats. Neurobiol Learn Mem 67(2):142–149. doi:10.1006/nlme.1996.3752 PubMedGoogle Scholar
  84. Maren S, Aharonov G, Fanselow MS (1997) Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 88(2):261–274PubMedGoogle Scholar
  85. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 2000(23):649–711Google Scholar
  86. McTighe SM, Cowell RA, Winters BD, Bussey TJ, Saksida LM (2010) Paradoxical false memory for objects after brain damage. Science 330(6009):1408–1410PubMedGoogle Scholar
  87. Meunier M, Bachevalier J, Mishkin M, Murray E (1993) Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci 13(12):5418–5432PubMedGoogle Scholar
  88. Milner B, Penfield W (1955) The effect of hippocampal lesions on recent memory. Trans Am Neurol Assoc (80th Meeting):42–48Google Scholar
  89. Mishkin M (1978) Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273(5660):297–298PubMedGoogle Scholar
  90. Muir GM, Bilkey DK (2001) Instability in the place field location of hippocampal place cells after lesions centered on the perirhinal cortex. J Neurosci 21(11):4016–4025PubMedGoogle Scholar
  91. Muller R (1996) A quarter of a century of place cells. Neuron 17(5):813–822. doi:10.1016/S0896-6273(00)80214-7 PubMedGoogle Scholar
  92. Mumby DG, Pinel JP (1994) Rhinal cortex lesions and object recognition in rats. Behav Neurosci 108(1):11–18PubMedGoogle Scholar
  93. Mumby DG, Glenn MJ, Nesbitt C, Kyriazis DA (2002) Dissociation in retrograde memory for object discriminations and object recognition in rats with perirhinal cortex damage. Behav Brain Res 132(2):215–226. doi:10.1016/S0166-4328(01)00444-2 PubMedGoogle Scholar
  94. Mumby DG, Piterkin P, Lecluse V, Lehmann H (2007) Perirhinal cortex damage and anterograde object-recognition in rats after long retention intervals. Behav Brain Res 185(2):82–87. doi:10.1016/j.bbr.2007.07.026 PubMedGoogle Scholar
  95. Murray EA, Mishkin M (1986) Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy. J Neurosci 6(7):1991–2003PubMedGoogle Scholar
  96. Murray EA, Wise SP (2012) Why is there a special issue on perirhinal cortex in a journal called hippocampus? The perirhinal cortex in historical perspective. Hippocampus 22(10):1941–1951. doi:10.1002/hipo.22055 PubMedGoogle Scholar
  97. Murray EA, Bussey TJ, Saksida LM (2007) Visual perception and memory: a new view of medial temporal lobe function in primates and rodents. Annu Rev Neurosci 30(1):99–122. doi:10.1146/annurev.neuro.29.051605.113046 PubMedGoogle Scholar
  98. Naber PA, Caballero-Bleda M, Jorritsma-Byham B, Witter MP (1997) Parallel input to the hippocampal memory system through peri- and postrhinal cortices. Neuroreport 8(11):2617–2621PubMedGoogle Scholar
  99. Naber PA, Witter MP, Lopes da Silva FH (2001) Evidence for a direct projection from the postrhinal cortex to the subiculum in the rat. Hippocampus 11(2):105–117. doi:10.1002/hipo.1029 PubMedGoogle Scholar
  100. Nadel L, Willner J (1980) Context and conditioning - a place for space. Physiol Psychol 8(2):218–228Google Scholar
  101. Nicholson DA, Freeman JH Jr (2000) Lesions of the perirhinal cortex impair sensory preconditioning in rats. Behav Brain Res 112(1–2):69–75PubMedGoogle Scholar
  102. Norman G, Eacott MJ (2004) Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions. Behav Brain Res 148(1–2):79–91. doi:10.1016/S0166-4328(03)00176-1 PubMedGoogle Scholar
  103. 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(2):557–566. doi:10.1037/0735-7044.119.2.557 PubMedGoogle Scholar
  104. Otto TE, Eichenbaum H (1992) Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. Behav Neurosci 106(5):762–775PubMedGoogle Scholar
  105. Paxinos G, Watson C (2006) The rat brain in stereotaxic coordinates: hard cover edition. Access Online via Elsevier,Google Scholar
  106. Richmond MA, Yee BK, Pouzet B, Veenman L, Rawlins JN, Feldon J, Bannerman DM (1999) Dissociating context and space within the hippocampus: effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behav Neurosci 113(6):1189–1203PubMedGoogle Scholar
  107. Rolls ET, Robertson RG, Georges-Francois P (1997) Spatial view cells in the primate hippocampus. Eur J Neurosci 9(8):1789–1794PubMedGoogle Scholar
  108. Rose M (1928) Die Inselrinde des Menschen und der Tiere. J Psychol Neurol 37:467–624Google Scholar
  109. Rothblat LA, Hayes LL (1987) Short-term object recognition memory in the rat: nonmatching with trial-unique junk stimuli. Behav Neurosci 101(4):587–590PubMedGoogle Scholar
  110. Rudy JW (2009) Context representations, context functions, and the parahippocampal-hippocampal system. Learn Mem 16(10):573–585. doi:10.1101/lm.1494409 PubMedCentralPubMedGoogle Scholar
  111. Sato N, Nakamura K (2003) Visual response properties of neurons in the parahippocampal cortex of monkeys. J Neurophysiol 90(2):876–886PubMedGoogle Scholar
  112. Scolville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20(1):11–21Google Scholar
  113. Seoane A, Tinsley CJ, Brown MW (2012) Interfering with Fos expression in rat perirhinal cortex impairs recognition memory. Hippocampus 22(11):2101–2113. doi:10.1002/hipo.22028 PubMedGoogle Scholar
  114. Shapiro ML, Tanila H, Eichenbaum H (1997) Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7(6):624–642. doi:10.1002/(SICI)1098-1063(1997)7:6&lt;624::AID-HIPO5&gt;3.0.CO;2-E PubMedGoogle Scholar
  115. Suzuki WA (2009) Perception and the medial temporal lobe: evaluating the current evidence. Neuron 61(5):657–666. doi:10.1016/j.neuron.2009.02.008 PubMedGoogle Scholar
  116. Suzuki WA (2010) Untangling memory from perception in the medial temporal lobe. Trends Cogn Sci 14(5):195–200. doi:10.1016/j.tics.2010.02.002 PubMedGoogle Scholar
  117. Suzuki WA, Amaral DG (1994) Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J Neurosci 14(3 Pt 2):1856–1877PubMedGoogle Scholar
  118. Swanson LW (2004) Brain maps III. Gulf Professional PublishingGoogle Scholar
  119. Tanila H, Shapiro ML, Eichenbaum H (1997) Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7(6):613–623. doi:10.1002/(SICI)1098-1063(1997)7:6&lt;613::AID-HIPO4&gt;3.0.CO;2-F PubMedGoogle Scholar
  120. Vidyasagar TR, Salzmann E, Creutzfeldt OD (1991) Unit activity in the hippocampus and the parahippocampal temporobasal association cortex related to memory and complex behaviour in the awake monkey. Brain Res 544(2):269–278PubMedGoogle Scholar
  121. Wan H, Aggleton JP, Brown MW (1999) Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19(3):1142–1148PubMedGoogle Scholar
  122. Warburton EC, Koder T, Cho K, Massey PV, Duguid G, Barker GR, Aggleton JP, Bashir ZI, Brown MW (2003) Cholinergic neurotransmission is essential for perirhinal cortical plasticity and recognition memory. Neuron 38(6):987–996PubMedGoogle Scholar
  123. Warburton EC, Glover CP, Massey PV, Wan H, Johnson B, Bienemann A, Deuschle U, Kew JN, Aggleton JP, Bashir ZI, Uney J, Brown MW (2005) cAMP responsive element-binding protein phosphorylation is necessary for perirhinal long-term potentiation and recognition memory. J Neurosci 25(27):6296–6303. doi:10.1523/JNEUROSCI.0506-05.2005 PubMedGoogle Scholar
  124. Wiig KA, Cooper LN, Bear MF (1996) Temporally graded retrograde amnesia following separate and combined lesions of the perirhinal cortex and fornix in the rat. Learn Mem 3(4):313–325PubMedGoogle Scholar
  125. Wiltgen BJ, Sanders MJ, Anagnostaras SG, Sage JR, Fanselow MS (2006) Context fear learning in the absence of the hippocampus. J Neurosci 26(20):5484–5491. doi:10.1523/JNEUROSCI.2685-05.2006 PubMedGoogle Scholar
  126. Winters BD, Bussey TJ (2005a) Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. J Neurosci 25(17):4243–4251. doi:10.1523/jneurosci.0480-05.2005 PubMedGoogle Scholar
  127. Winters BD, Bussey TJ (2005b) Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J Neurosci 25(1):52–61. doi:10.1523/JNEUROSCI.3827-04.2005 PubMedGoogle Scholar
  128. Winters BD, Reid JM (2010) A distributed cortical representation underlies crossmodal object recognition in rats. J Neurosci 30(18):6253–6261. doi:10.1523/jneurosci.6073-09.2010 PubMedGoogle Scholar
  129. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ (2004) Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 24(26):5901–5908. doi:10.1523/JNEUROSCI.1346-04.2004 PubMedGoogle Scholar
  130. Xiang JZ, Brown MW (1998) Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37(4–5):657–676PubMedGoogle Scholar
  131. Yi DJ, Chun MM (2005) Attentional modulation of learning-related repetition attenuation effects in human parahippocampal cortex. J Neurosci 25(14):3593–3600. doi:10.1523/JNEUROSCI.4677-04.2005 PubMedGoogle Scholar
  132. Young BJ, Otto T, Fox GD, Eichenbaum H (1997) Memory representation within the parahippocampal region. J Neurosci 17(13):5183–5195PubMedGoogle Scholar
  133. Zhu XO, Brown MW, Aggleton JP (1995a) Neuronal signalling of information important to visual recognition memory in rat rhinal and neighbouring cortices. Eur J Neurosci 7(4):753–765PubMedGoogle Scholar
  134. Zhu XO, Brown MW, McCabe BJ, Aggleton JP (1995b) Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain. Neuroscience 69(3):821–829PubMedGoogle Scholar
  135. Zola-Morgan S, Squire LR, Amaral DG, Suzuki WA (1989) Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J Neurosci 9(12):4355–4370PubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  1. 1.Department of Cognitive, Linguistic, and Psychological SciencesBrown UniversityProvidenceUSA

Personalised recommendations