Subcortical connections of the perirhinal, postrhinal, and entorhinal cortices of the rat. I. afferents

Hippocampus

Volumn 26, Issue 9, 2016, Pages 1189-1212

  Tomás Pereira, Inês ^a   Agster, Kara L ^b,c   Burwell, Rebecca D ^a,b  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

anatomy; connectivity; memory; parahippocampal; retrograde

Indexed keywords

AMYGDALA; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN FUNCTION; CELL DENSITY; CELL NUCLEUS; CELL STRUCTURE; CLAUSTRUM; CONNECTOME; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; HYPOTHALAMUS; INFORMATION PROCESSING; MEDIAL GENICULATE THALAMIC NUCLEUS; MEDIAL TEMPORAL LOBE; MOTIVATION; NONHUMAN; OLFACTORY SYSTEM; PARAHIPPOCAMPAL GYRUS; PERCEPTION; PERIRHINAL CORTEX; PRIORITY JOURNAL; RAT; REUNIENS NUCLEUS; SENSORY NERVE; SENSORY STIMULATION; SEPTUM PELLUCIDUM; SUBCORTICAL AFFERENT; SUPRAGENICULATE NUCLEUS; THALAMUS; THALAMUS VENTRAL NUCLEUS; VISUOSPATIAL ATTENTION; ANIMAL; CYTOLOGY; MALE; NEUROANATOMICAL TRACT TRACING; SENSORY NERVE CELL; SPRAGUE DAWLEY RAT;

AFFERENT PATHWAYS; ANIMALS; ENTORHINAL CORTEX; MALE; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONS, AFFERENT; PERIRHINAL CORTEX; RATS, SPRAGUE-DAWLEY;

EID: 84971350747     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22603     Document Type: Article

References (93)

1. Agster KL, Burwell RD. 2009. Cortical efferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. Hippocampus 19:1159–1186.
2. Agster KL, Burwell RD. 2013. Hippocampal and subicular efferents and afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. Behav Brain Res 254:50–64.
3. Agster KL, Tomás Pereira I, Saddoris MP, Burwell RD. 2016. Subcortical connections of the perirhinal, postrhinal, and entorhinal cortices of the rat. II. efferents. Hippocampus, xx:yy-yy.
4. Alonso A, Kohler C. 1984. A study of the reciprocal connections between the septum and the entorhinal area using anterograde and labeled cells axonal transport methods in the rat brain. J Comp Neurol 225:327–343.
5. Amaral DG, Price JL. 1984. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J Comp Neurol 230:465–496.
6. Amaral DG, Insausti R, Cowan WM. 1987. The entorhinal cortex of the monkey: I. Cytoarchitectonic organization. J Comp Neurol 264:326–355.
7. Baleydier C, Mauguiere F. 1985. Anatomical evidence for medial pulvinar connections with the posterior cingulate cortex, the retrosplenial area, and the posterior parahippocampal gyrus in monkeys. J Comp Neurol 232:219–228.
8. Beaudin SA, Singh T, Agster KL, Burwell RD. 2013. Borders and comparative cytoarchitecture of the perirhinal and postrhinal cortices in an f1 hybrid mouse. Cereb Cortex 23:460–474.
9. Beckstead RM. 1978. Afferent connections of the entorhinal area in the rat as demonstrated by labeled cells cell-labeling with horseradish peroxidase. Brain Res 152:249–264.
10. Berendse HW, Groenewegen HJ. 1991. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42:73–102.
11. Bett D, Stevenson CH, Shires KL, Smith MT, Martin SJ, Dudchenko PA, Wood ER. 2013. The postsubiculum and spatial learning: The role of postsubicular synaptic activity and synaptic plasticity in hippocampal place cell, object, and object-location memory. J Neurosci 33:6928–6943.
12. Blackstad TW. 1956. Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105:417–537.
13. Brodmann K. 1909. Vergleichende Lokalisationslehre der Grosshirnrinde in Ihren Prinzipien Dargestellt auf Grund des Zellenbaues. Liepzig: Barth.
14. Bucci DJ, Burwell RD. 2004. Deficits in attentional orienting following damage to the perirhinal or postrhinal cortices. Behav Neurosci 118:1117–1122.
15. Burwell RD. 2000. The parahippocampal region: Corticocortical connectivity. Ann N Y Acad Sci 911:25–42.
16. Burwell RD. 2001. Borders and cytoarchitecture of the perirhinal and postrhinal cortices in the rat. J Comp Neurol 437:17–41.
17. Burwell RD, Amaral DG. 1998a. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol 398:179–205.
18. Burwell RD, Amaral DG. 1998b. Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex. J Comp Neurol 391:293–321.
19. Burwell RD, Hafeman DM. 2003. Positional firing properties of postrhinal cortex neurons. Neuroscience 119:577–588.
20. 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 5:390–408.
21. Bussey TJ, Saksida LM. 2005. The perceptual-mnemonic/feature conjunction model of perirhinal cortex function. Q J Exp Psychol B 58:269–282.
22. Canteras NS, Simerly RB, Swanson LW. 1992. Connections of the posterior nucleus of the amygdala. J Comp Neurol 324:143–179.
23. Crick FC, Koch C. 2005. What is the function of the claustrum? Philos Trans R Soc B Biol Sci 360:1271–1279.
24. de Olmos J, Hardy H, Heimer L. 1978. The afferent connections of the main and the accessory olfactory bulb formations in the rat: An experimental HRP-study. J Comp Neurol 181:213–244.
25. Deacon TW, Eichenbaum H, Rosenberg P, Eckmann KW. 1983. Afferent connections of the perirhinal cortex in the rat. J Comp Neurol 220:168–190.
26. Dolorfo CL, Amaral DG. 1998a. Entorhinal cortex of the rat: Organization of intrinsic connections. J Comp Neurol 398:49–82.
27. 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 398:25–48.
28. Eacott MJ, Machin PE, Gaffan EA. 2001. Elemental and configural visual discrimination learning following lesions to perirhinal cortex in the rat. Behav Brain Res 124:55–70.
29. Eichenbaum H. 2000. A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1:41–50.
30. Eid T, Jorritsma-Byham B, Schwarcz R, Witter MP. 1996. Afferents to the seizure-sensitive neurons in layer III of the medial entorhinal area: A tracing study in the rat. Exp Brain Res 109:209–18.
31. 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 88:181–193.
32. Eradath MK, Mogami T, Wang G, Tanaka K. 2015. Time context of cue-outcome associations represented by neurons in perirhinal cortex. J Neurosci 35:4350–4365.
33. Finch DM, Wong EE, Derian EL, Chen XH, Nowlin-Finch NL, Brothers LA. 1986. Neurophysiology of limbic system pathways in the rat: Projections from the amygdala to the entorhinal cortex. Brain Res 370:273–284.
34. Franko E, Insausti AM, Artacho-Perula E, Insausti R, Chavoix C. 2014. Identification of the human medial temporal lobe regions on magnetic resonance images. Human Brain Mapp 35:248–256.
35. Furtak SC, Wei SM, Agster KL, Burwell RD. 2007. Functional neuroanatomy of the parahippocampal region in the rat: The perirhinal and postrhinal cortices. Hippocampus 17:709–722.
36. Furtak SC, Ahmed OJ, Burwell RD. 2012. Single neuron activity and theta modulation in postrhinal cortex during performance on a visual discrimination task. Neuron 76:976–988.
37. Goll Y, Atlan G, Citri A. 2015. Attention: The claustrum. Trends Neurosci 38:486–495.
38. Goulet S, Murray EA. 2001. Neural substrates of crossmodal association memory in monkeys: The amygdala versus the anterior rhinal cortex. Behav Neurosci 115:271–284.
39. Gurdjian ES. 1925. Olfactory connections in the albino rat, with special reference to the stria medullaris and the anterior commissure. J Comp Neurol 38:127–163.
40. Haberly LB, Price JL. 1978. Association and commissural fiber systems of the olfactory cortex in the rat. I. Systems originating in the piriform cortex and adjacent areas. J Comp Neurol 178:711–740.
41. Ho JW, Burwell RD. 2014. Perirhinal and Postrhinal Functional Inputs to the Hippocampus. Space, Time and Memory in the Hippocampal Formation. Vienna: Springer. pp 55–81.
42. Ho JW, Poeta DL, Jacobson TK, Zolnik TA, Neske GT, Connors BW, Burwell RD. 2015. Bidirectional Modulation of Recognition Memory. J Neurosci 35:13323–13335.
43. Insausti R, Amaral DG, Cowan WM. 1987. The entorhinal cortex of the monkey: III. Subcortical afferents. J Comp Neurol 264:396–408.
44. Insausti R, Herrero MT, Witter MP. 1997. Entorhinal cortex of the rat: Cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7:146–183.
45. Insausti R, Tuñón T, Sobreviela T, Insausti AM, Gonsalo LM. 1995. The human entorhinal cortex: A cytoarchitectonic analysis. J Comp Neurol 355:171–198.
46. Jones EG. 1985. The Thalamus. New York: Plenum Press.
47. Kamishina H, Conte WL, Patel SS, Tai RJ, Corwin JV, Reep RL. 2009. Cortical connections of the rat lateral posterior thalamic nucleus. Brain Res 1264:39–56.
48. Kemppainen S, Jolkkonen E, Pitkanen A. 2002. Projections from the posterior cortical nucleus of the amygdala to the hippocampal formation and parahippocampal region in rat. Hippocampus 12:735–755.
49. Kent BA, Hvoslef-Eide M, Saksida LM, Bussey TJ. 2016. The representational-hierarchical view of pattern separation: Not just hippocampus, not just space, not just memory? Neurobiol Learn Mem 129:99–106.
50. Kerr KM, Agster KL, Furtak SC, Burwell RD. 2007. Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas. Hippocampus 17:697–708.
51. Kholodar-Smith DB, Allen TA, Brown TH. 2008. Fear conditioning to discontinuous auditory cues requires perirhinal cortical function. Behav Neurosci 122:1178–1185.
52. Kimura A, Donishi T, Sakoda T, Hazama M, Tamai Y. 2003. Auditory thalamic nuclei projections to the temporal cortex in the rat. Neuroscience 117:1003–1016.
53. Krettek JE, Price JL. 1978. A description of the amygdaloid complex in the rat and cat with observations of intra-amygdaloid axonal connections. J Comp Neurol 178:255–280.
54. Krieg WJS. 1946. Connections of the cerebral cortex.1. The Albino Rat.B. Structure of the cortical areas. J Comp Neurol 84:277–323.
55. Liu Z, Richmond BJ. 2000. Response differences in monkey TE and perirhinal cortex: Stimulus association related to reward schedules. J Neurophysiol 83:1677–1692.
56. Lorente de Nó R. 1933. Studies on the structure of the cerebral cortex. I. Area entorhinalis. J Psychol Neurol 45:113–177.
57. Mair RG, Burk JA, Porter MC. 1998. Lesions of the frontal cortex, hippocampus, and intralaminar thalamic nuclei have distinct effects on remembering in rats. Behav Neurosci 112:772–792.
58. Majak K, Pitkanen A. 2003. Projections from the periamygdaloid cortex to the amygdaloid complex, the hippocampal formation, and the parahippocampal region: A PHA-L study in the rat. Hippocampus 13:922–942.
59. Moga MM, Weis RP, Moore RY. 1995. Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359:221–238.
60. Moran JP, Dalrymple-Alford JC. 2003. Perirhinal cortex and anterior thalamic lesions: Comparative effects on learning and memory. Behav Neurosci 117:1326–1341.
61. Mufson EJ, Mesulam MM. 1982. Insula of the old-world monkey.2. Afferent cortical input and comments on the claustrum. J Comp Neurol 212:23–37.
62. Murray EA, Richmond BJ. 2001. Role of perirhinal cortex in object perception, memory, and associations. Curr Opin Neurobiol 11:188–193.
63. Nakamura H, Hioki H, Furuta T, Kaneko T. 2015. Different cortical projections from three subdivisions of the rat lateral posterior thalamic nucleus: A single-neuron tracing study with viral vectors. Eur J Neurosci 41:1294–1310.
64. Newman LA, Burk JA. 2005. Effects of excitotoxic thalamic intralaminar nuclei lesions on attention and working memory. Behav Brain Res 162:264–271.
65. Paxinos G, Watson C. 1998. The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.
66. Paxinos G, Watson C. 2014. The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.
67. Pearson RCA, Brodal P, Gatter KC, Powell TPS. 1982. The organization of the connections between the cortex and the claustrum in the monkey. Brain Res 234:435–441.
68. Pikkarainen M, Pitkänen A. 2001. Projections from the lateral, basal and accessory basal nuclei of the amygdala to the perirhinal and postrhinal cortices in rat. Cereb Cortex 11:1064–1082.
69. Pitkanen A, Kelly JL, Amaral DG. 2002. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the entorhinal cortex in the macaque monkey. Hippocampus 12:186–205.
70. Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A. 2000. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369–391.
71. Posner MI, Petersen SE. 1990. The attention system of the human brain. Annu Rev Neurosci 13:25–42.
72. Ranganath C, Ritchey M. 2012. Two cortical systems for memory-guided behaviour. Nat Rev Neurosci 13:713–726.
73. Romanski LM, LeDoux JE. 1992. Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning. J Neurosci 12:4501–4509.
74. Room P, Groenewegen HJ. 1986. Connections of the parahippocampal cortex. I. Cortical afferents. J Comp Neurol 251:415–450.
75. Saksida LM, Bussey TJ, Buckmaster CA, Murray EA. 2007. Impairment and facilitation of transverse patterning after lesions of the perirhinal cortex and hippocampus, respectively. Cereb Cortex 17:108–115.
76. Schmued LC, Fallon JH. 1986. Fluoro-Gold: A new fluorescent labeled cells axonal tracer with numerous unique properties. Brain Res 377:147–154.
77. Shipp S. 2004. The brain circuitry of attention. Trends Cogn Sci 8:223–230.
78. Sparta DR, Smithuis J, Stamatakis AM, Jennings JH, Kantak PA, Ung RL, Stuber GD. 2014. Inhibition of projections from the basolateral amygdala to the entorhinal cortex disrupts the acquisition of contextual fear. Front Behav Neurosci 8:129.
79. Sugase-Miyamoto Y, Richmond BJ. 2007. Cue and reward signals carried by monkey entorhinal cortex neurons during reward schedules. Exp Brain Res 181:267–276.
80. Suzuki WA, Amaral DG. 2003. Perirhinal and parahippocampal cortices of the macaque monkey: Cytoarchitectonic and chemoarchitectonic organization. J Comp Neurol 463:67–91.
81. Swanson LW. 1998. Brain Maps: Structure of the Rat Brain. Amsterdam: Elsevier.
82. Swanson LW. 2003. Brain Maps: Structure of the Rat Brain. Amsterdam: Elsevier.
83. Unal G, Pare JF, Smith Y, Pare D. 2013. Differential connectivity of short- vs. long-range extrinsic and intrinsic cortical inputs to perirhinal neurons. J Comp Neurol 521:2538–2550.
84. Van der Werf YD, Witter MP, Groenewegen HJ. 2002. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Rev 39:107–140.
85. van Groen T, Kadish I, Wyss JM. 1999. Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Rev 30:1–26.
86. Vertes RP, Crane AM, Colom LV, Bland BH. 1995. Ascending projections of the posterior nucleus of the hypothalamus: PHA-L analysis in the rat. J Comp Neurol 359:90–116.
87. Wan H, Aggleton JP, Brown MW. 1999. Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19:1142–1148.
88. Winters BD, Bussey TJ. 2005. Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J Neurosci 25:52–61.
89. Witter MP, Room P, Groenewegen HJ, Lohman AH. 1988. Reciprocal connections of the insular and piriform claustrum with limbic cortex: An anatomical study in the cat. Neuroscience 24:519–539.
90. Witter MP, Naber PA, van Haeften T, Machielsen WCM, Rombouts SARB, Barkhof F, Scheltens P, da Silva FHL. 2000. Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10:398–410.
91. Wouterlood FG. 1991. Innervation of entorhinal principal cells by neurons of the nucleus reuniens thalami. anterograde pha-l tracing combined with labeled cells fluorescent tracing and intracellular injection with lucifer yellow in the rat. Eur J Neurosci 3:641–647.
92. Zhu XO, Brown MW. 1995. Changes in neuronal activity related to the repetition and relative familiarity of visual stimuli in rhinal and adjacent cortex of the anaesthetised rat. Brain Res 689:101–110.
93. Zola-Morgan S, Squire LR, Alvarez-Royo P, Clower RP. 1991. Independence of memory functions and emotional behavior: Separate contributions of the hippocampal formation and the amygdala. Hippocampus 1:207–220.