The perirhinal cortex

Annual Review of Neuroscience

Volumn 37, Issue , 2014, Pages 39-53

  Suzuki, Wendy A ^a   Naya, Yuji ^b  

^a NEW YORK UNIVERSITY   (United States)

^b PEKING UNIVERSITY   (China)

Author keywords

Association memory; Declarative memory; Medial temporal lobe

Indexed keywords

AMYGDALOID NUCLEUS; BRAIN FUNCTION; HIPPOCAMPUS; HUMAN; NERVE PROJECTION; NEUROANATOMY; NEUROPHYSIOLOGY; NONHUMAN; PERIRHINAL CORTEX; PRIORITY JOURNAL; RECALL; REVIEW; TEMPORAL LOBE; VISUAL SYSTEM; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN CORTEX; MEMORY; NERVE TRACT; PHYSIOLOGY;

AMYGDALA; ANIMALS; CEREBRAL CORTEX; HUMANS; MEMORY; NEURAL PATHWAYS; TEMPORAL LOBE;

EID: 84904615444     PISSN: 0147006X     EISSN: 15454126     Source Type: Book Series    
DOI: 10.1146/annurev-neuro-071013-014207     Document Type: Review

References (99)

1. Aggleton JP,BrownMW,AlbasserMM.2012. Contrasting brain activity patterns for item recognitionmemory and associative recognition memory: insights from immediate-early gene functional imaging. Neuropsychologia 50(13):3141-55
2. Aminoff E, Gronau N, BarM. 2007. The parahippocampal cortexmediates spatial and nonspatial associations. Cereb. Cortex 17(7):1493-503
3. BarM, Aminoff E, Ishai A. 2008. Famous faces activate contextual associations in the parahippocampal cortex. Cereb. Cortex 18(6):1233-38
4. Baxter MG. 2009. Involvement of medial temporal lobe structures in memory and perception. Neuron 61(5):667-77
5. Brodmann K. 1909. Vergleichende Lokalisationslehre der Grosshirnrinde. Leipzig: Johann Ambrosius Barth
6. Brown MW, Aggleton JP. 2001. Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat. Rev. Neurosci. 2(1):51-61
7. Brown MW, Warburton EC, Aggleton JP. 2010. Recognition memory: material, processes, and substrates. Hippocampus 20(11):1228-44
8. BuckleyMJ, BoothMCA, Rolls ET, Gaffan D. 2001. Selective perceptual impairments after perirhinal cortex ablation. J. Neurosci. 21(24):9824-36
9. Buckley MJ, Gaffan D. 1998. Perirhinal cortex ablation impairs visual object identification. J. Neurosci. 18(6):2268-75
10. Burwell RD, Amaral DG. 1998. Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J. Comp. Neurol. 391(3):293-321
11. Bussey TJ, Saksida LM. 2007. Memory, perception, and the ventral visual-perirhinal-hippocampal stream: thinking outside of the boxes. Hippocampus 17(9):898-908
12. BusseyTJ, Saksida LM, Murray EA. 2005. The perceptual-mnemonic/feature conjunction model of perirhinal cortex function. Q. J. Exp. Psychol. B 58(3-4):269-82
13. Chaudhry AM, Parkinson JA, Hinton EC, Owen AM, Roberts AC. 2009. Preference judgements involve a network of structures within frontal, cingulate and insula cortices. Eur. J. Neurosci. 29(5):1047-55
14. Clark AM, Bouret S, Young AM, Murray EA, Richmond BJ. 2013. Interaction between orbital prefrontal and rhinal cortex is required for normal estimates of expected value. J. Neurosci. 33(5):1833-45
15. Davachi L. 2006. Item, context and relational episodic encoding in humans. Curr. Opin. Neurobiol. 16(6):693-700
16. de Araujo IE, Rolls ET, Kringelbach ML, McGlone F, Phillips N. 2003. Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur. J. Neurosci. 18(7):2059-68
17. de CurtisM,PareD. 2004. The rhinal cortices: awall of inhibition between the neocortex and the hippocampus. Prog. Neurobiol. 74(2):101-10
18. Diana RA, Yonelinas AP, Ranganath C. 2007. Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends Cogn. Sci. 11(9):379-86
19. Egorov AV,Hamam BN, Fransen E, HasselmoME, Alonso AA. 2002. Graded persistent activity in entorhinal cortex neurons. Nature 420:173-78
20. Eichenbaum H, Cohen NJ. 2001. From Conditioning to Conscious Recollection. New York: Oxford Univ. Press
21. Eichenbaum H, Yonelinas AR, Ranganath C. 2007. Themedial temporal lobe and recognitionmemory. Annu. Rev. Neurosci. 30:123-52
22. Erickson CA, Desimone R. 1999. Responses of macaque perirhinal neurons during and after visual stimulus association learning. J. Neurosci. 19(23):10404-16
23. Fernandez G, Tendolkar I. 2006. The rhinal cortex: gatekeeper of the declarative memory system. Trends Cogn. Sci. 10(8):358-62
24. Foster DJ, Wilson MA. 2006. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440(7084):680-83
25. Fransen E, Tahvildari B, Egorov AV,HasselmoME, Alonso AA. 2006. Mechanism of graded persistent cellular activity of entorhinal cortex layer V neurons. Neuron 49(5):735-46
26. Fujimichi R, Naya Y, Koyano KW, Takeda M, Takeuchi D, Miyashita Y. 2010. Unitized representation of paired objects in area 35 of the macaque perirhinal cortex. Eur. J. Neurosci. 32(4):659-67
27. Gaffan D. 1992. Amnesia for complex naturalistic scenes and for objects following fornix transection in the rhesus monkey. Eur. J. Neurosci. 4:381-88
28. Graham KS, Barense MD, Lee AC. 2010. Going beyond LTM in the MTL: a synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception. Neuropsychologia 48(4):831-53
29. Hampton RR. 2005. Monkey perirhinal cortex is critical for visual memory, but not for visual perception: reexamination of the behavioural evidence from monkeys. Q. J. Exp. Psychol. B 58(3-4):283-99
30. Hargreaves EL, Rao G, Lee I, Knierim JJ. 2005. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308:1792-94
31. Higuchi S-I, Miyashita Y. 1996. Neural code of visual paired associate memory in primate inferotemporal cortex is impaired by perirhinal and entorhinal lesions. Proc. Natl. Acad. Sci. USA 93:739-43
32. HirabayashiT,TakeuchiD,TamuraK,Miyashita Y. 2013a. Functionalmicrocircuit recruited during retrieval of object association memory in monkey perirhinal cortex. Neuron 77(1):192-203
33. Hirabayashi T, Takeuchi D, Tamura K, Miyashita Y. 2013b. Microcircuits for hierarchical elaboration of object coding across primate temporal areas. Science 341:191-95
34. Insausti R, Amaral DG, Cowan WM. 1987. The entorhinal cortex of the monkey: II. Cortical afferents. J. Comp. Neurol. 264:356-95
35. Insausti R,MunozM. 2001. Cortical projections of the non-entorhinal hippocampal formation in the cynomolgus monkey (Macaca fascicularis). Eur. J. Neurosci. 14(3):435-51
36. Jones EG, Powell TPS. 1970. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93:793-820
37. Kent BA, Brown TH. 2012. Dual functions of perirhinal cortex in fear conditioning. Hippocampus 22(10):2068-79
38. Kuhl BA,Rissman J,ChunMM,Wagner AD. 2011. Fidelity of neural reactivation reveals competition between memories. Proc. Natl. Acad. Sci. USA 108(14):5903-8
39. Lavenex P, Suzuki WA, Amaral DG. 2002. Perirhinal and parahippocampal cortices of the macaque monkey: projections to the neocortex. J. Comp. Neurol. 447(4):394-420
40. Lavenex P, Suzuki WA, Amaral DG. 2004. Perirhinal and parahippocampal cortices of the macaque monkey: intrinsic projections and interconnections. J. Comp. Neurol. 472(3):371-94
41. Law JR, FlaneryMA, Wirth S, YanikeM, Smith AC, et al. 2005. Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory. J. Neurosci. 25(24):5720-29
42. Liu Z,Murray EA, Richmond BJ. 2000. Learning motivational significance of visual cues for reward schedules requires rhinal cortex. Nat. Neurosci. 3(12):1307-15
43. Liu Z, Richmond BJ. 2000. Response differences in monkey TE and perirhinal cortex: stimulus association related to reward schedules. J. Neurophysiol. 83(3):1677-92
44. MacDonald CJ, Legage KQ, Eden UT, Eichenbaum H. 2011. Hippocampal time cells bridge the gap in memory for discontiguous events. Neuron 71(4):737-49
45. Mayes A, Montaldi D, Migo E. 2007. Associative memory and the medial temporal lobes. Trends Cogn. Sci. 11(3):126-35
46. Messinger A, Squire LR, Zola SM, Albright TD. 2001. Neuronal representations of stimulus associations develop in the temporal lobe during learning. Proc. Natl. Acad. Sci. 98(21):12239-44
47. Miyashita Y. 1988. Neuronal correlate of visual associative long-term memory in the primate temporal cortex. Nature 335:817-20
48. Mogami T, Tanaka K. 2006. Reward association affects neuronal responses to visual stimuli in macaque TE and perirhinal cortices. J. Neurosci. 26(25):6761-70
49. Mohedano-Moriano A, Martinez-Marcos A, Pro-Sistiaga P, Blaizot X, Arroyo-Jimenez MM, et al. 2008. Convergence of unimodal and polymodal sensory input to the entorhinal cortex in the fascicularis monkey. Neuroscience 151(1):255-71
50. Munoz M, Insausti R. 2005. Cortical efferents of the entorhinal cortex and the adjacent parahippocampal region in the monkey (Macaca fascicularis). Eur. J. Neurosci. 22(6):1368-88
51. Murray EA, Bachevalier J, Mishkin M. 1989. Effects of rhinal cortical lesions on visual recognition memory in rhesus monkeys. Soc. Neurosci. Abstr. 15:342 (Abstr.)
52. Murray EA, Baxter MG, Gaffan D. 1998. Monkeys with rhinal cortex damage or neurotoxic hippocampal lesions are impaired on spatial scene learning and object reversals. Behav. Neurosci. 112:1291-303
53. Murray EA, Gaffan D, Mishkin M. 1993. Neural substrates of visual stimulus-stimulus association in rhesus monkeys. J. Neurosci. 13:4549-61
54. Murray EA, Richmond BJ. 2001. Role of perirhinal cortex in object perception, memory, and associations. Curr. Opin. Neurobiol. 11(2):188-93
55. Murray EA, Wise SP. 1996. Role of the hippocampus plus subjacent cortex but not amygdala in visuomotor conditional learning in rhesus monkeys. Behav. Neurosci. 110(6):1261-70
56. 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):1941-51
57. Navaroli VL, Zhao Y, Boguszewski P, Brown TH. 2012. Muscarinic receptor activation enables persistent firing in pyramidal neurons from superficial layers of dorsal perirhinal cortex. Hippocampus 22(6):1392-404
58. Naya Y, Sakai K, Miyashita Y. 1996. Activity of primate inferotemporal neurons related to a sought target in pair-association task. Proc. Natl. Acad. Sci. USA 93(7):2664-69
59. Naya Y, Suzuki WA. 2010. Associative memory in the medial temporal lobe. In Primate Neuroethology, ed.M Platt, A Ghazanfar, pp. 337-58. Oxford, UK: Oxford Univ. Press
60. Naya Y, Suzuki WA. 2011. Integrating what and when across the primate medial temporal lobe. Science 333:773-76
61. Naya Y, YoshidaM,Miyashita Y. 2001. Backward spreading ofmemory-retrieval signal in the primate temporal cortex. Science 291:661-64
62. Naya Y, Yoshida M, Miyashita Y. 2003a. Forward processing of long-term associative memory in monkey inferotemporal cortex. J. Neurosci. 23(7):2861-71
63. Naya Y, Yoshida M, Takeda M, Fujimichi R, Miyashita Y. 2003b. Delay-period activities in two subdivisions of monkey inferotemporal cortex during pair association memory task. Eur. J. Neurosci. 18(10):2915-18
64. Ohyama K, Sugase-Miyamoto Y, Matsumoto N, Shidara M, Sato C. 2012. Stimulus-related activity during conditional associations in monkey perirhinal cortex neurons depends on upcoming reward outcome. J. Neurosci. 32(48):17407-19
65. Padoa-Schioppa C, Assad JA. 2006. Neurons in the orbitofrontal cortex encode economic value. Nature 441:223-26
66. Pastalkova E, Itskov V, Amarasingham A, Buzsaki G. 2008. Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322-27
67. Paz R, Pare D. 2013. Physiological basis for emotional modulation of memory circuits by the amygdala. Curr. Opin. Neurobiol. 23(3):381-86
68. Paz R, Pelletier JG, Bauer EP, Pare D. 2006. Emotional enhancement of memory via amygdala-driven facilitation of rhinal interactions. Nat. Neurosci. 9(10):1321-29
69. Polyn SM, Natu VS, Cohen JD, Norman KA. 2005. Category-specific cortical activity precedes retrieval during memory search. Science 310:1963-66
70. Ranganath C, Ritchey M. 2012. Two cortical systems for memory-guided behaviour. Nat. Rev. Neurosci. 13(10):713-26
71. Sakai K, Miyashita Y. 1991. Neural organization for the long-term memory of paired associates. Nature 354:152-55
72. Schapiro AC, Kustner LV, Turk-Browne NB. 2012. Shaping of object representations in the human medial temporal lobe based on temporal regularities. Curr. Biol. 22(17):1622-27
73. SchonK, Atri A,HasselmoME, Tricarico MD, Lopresti ML, Stern CE. 2005. Scopolamine reduces persistent activity related to long-term encoding in the parahippocampal gyrus during delayed matching in humans. J. Neurosci. 25(40):9112-23
74. Schon K,HasselmoME, Lopresti ML,Tricarico MD, Stern CE. 2004. Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding: a functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task. J. Neurosci. 24(49):11088-97
75. Shrager Y, Gold JJ, Hopkins RO, Squire LR. 2006. Intact visual perception in memory-impaired patients with medial temporal lobe lesions. J. Neurosci. 26(8):2235-40
76. SmithELIII, HarwerthRS, LeviDM,Watson JT. 1981. Normal cortical responses in ocularly hypopigmented cats. Brain Res. 206:183-86
77. Squire LR,Wixted JT,Clark RE. 2007. Recognitionmemory and themedial temporal lobe: a new perspective. Nat. Rev. Neurosci. 8:872-83
78. Staresina BP, Davachi L. 2008. Selective and shared contributions of the hippocampus and perirhinal cortex to episodic item and associative encoding. J. Cogn. Neurosci. 20(8):1478-89
79. Staresina BP, Davachi L. 2009. Mind the gap: binding experiences across space and time in the human hippocampus. Neuron 63(2):267-76
80. Staresina BP, Duncan KD,Davachi L. 2011. Perirhinal and parahippocampal cortices differentially contribute to later recollection of object- and scene-related event details. J. Neurosci. 31(24):8739-47
81. Stefanacci L, Suzuki WA, Amaral DG. 1996. Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 375:552-82
82. Suzuki WA. 2009a. Comparative analysis of the cortical afferents, intrinsic projections and interconnections of the parahippocampal regions in monkeys and rats. In The Cognitive Neurosciences, ed. M Gazzaniga, pp. 659-74. Boston, MA: MIT Press
83. Suzuki WA. 2009b. Perception and the medial temporal lobe: evaluating the current evidence. Neuron 61(5):657-66
84. Suzuki WA, Amaral DG. 1990. Cortical inputs to the CA1 field of the monkey hippocampus originate from the perirhinal and parahippocampal cortex but not from area TE. Neurosci. Lett. 115:43-48
85. Suzuki WA, Amaral DG. 1994a. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J. Comp. Neurol. 350:497-533
86. Suzuki WA, Amaral DG. 1994b. Topographic organization of the reciprocal connections between monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J. Neurosci. 14:1856-77
87. Suzuki WA, Amaral DG. 2003. The perirhinal and parahippocampal cortices of the macaque monkey: cytoarchitectonic and chemoarchitectonic organization. J. Comp. Neurol. 463:67-91
88. Suzuki WA, Baxter MG. 2009. Memory, perception, and the medial temporal lobe: a synthesis of opinions. Neuron 61(5):678-79
89. Suzuki WA, Zola-Morgan S, Squire LR, Amaral DG. 1993. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J. Neurosci. 13:2430-51
90. Van Hoesen GW, Pandya DN. 1975. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Res. 95:1-24
91. Watson HC,Wilding EL, Graham KS. 2012. A role for perirhinal cortex in memory for novel object-context associations. J. Neurosci. 32(13):4473-81
92. Wirth S, Yanike M, Frank LM, Smith AC, Brown EN, Suzuki WA. 2003. Single neurons in the monkey hippocampus and learning of new associations. Science 300:1578-81
93. Wixted JT, Squire LR. 2010. The role of the human hippocampus in familiarity-based and recollection-based recognition memory. Behav. Brain Res. 215(2):197-208
94. Xiang JZ, Brown MW. 1998. Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37:657-76
95. Yakovlev V, Fusi S, Berman E, Zohary E. 1998. Inter-trial neuronal activity in inferior temporal cortex: a putative vehicle to generate long-term visual associations. Nat. Neurosci. 1(4):310-17
96. Yanike M, Wirth S, Smith AC, Brown EN, Suzuki WA. 2009. Comparison of associative learning-related signals in the macaque perirhinal cortex and hippocampus. Cereb. Cortex 19(5):1064-78
97. Yoshida M, Naya Y, Miyashita Y. 2003. Anatomical organization of forward fiber projections from area TE to perirhinal neurons representing visual long-term memory in monkeys. Proc. Natl. Acad. Sci. USA 100(7):4257-62
98. Yukie M. 2000. Connections between the medial temporal cortex and the CA1 subfield of the hippocampal formation in the Japanese monkey (Macaca fuscata). J. Comp. Neurol. 423:282-98
99. 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. 9:4355-70