Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat

Hippocampus

Volumn 17, Issue 10, 2007, Pages 957-976

  Jones, Bethany F ^a,b   Witter, Menno P ^a,c  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Anterograde tracing; Hippocampus; Learning and memory; Prefrontal cortex; Retrosplenial cortex

Indexed keywords

DEXTRAN; DEXTRAN AMINE; LEUKOAGGLUTININ; TRACER; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CINGULATE GYRUS; ENTORHINAL CORTEX; FEMALE; HIPPOCAMPUS; LEARNING; MEMORY; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SUBICULUM;

AFFERENT PATHWAYS; ANIMALS; BIOTIN; BRAIN MAPPING; DEXTRANS; FEMALE; GYRUS CINGULI; HIPPOCAMPUS; IONTOPHORESIS; PARAHIPPOCAMPAL GYRUS; PHYTOHEMAGGLUTININS; RATS; RATS, WISTAR;

EID: 35348874381     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20330     Document Type: Article

References (84)

1. Antoniadis EA, McDonald RJ. 2006. Fornix, medial prefrontal cortex, nucleus accumbens, and mediodorsal thalamic nucleus: Roles in a fear-based context discrimination task. Neurobiol Learn Mem 85:71-85.
2. Beckstead RM. 1979. An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat. J Comp Neurol 184:43-62.
3. Bressler SL. 1995. Large-scale cortical networks and cognition. Brain Res Brain Res Rev 20:288-304.
4. Bucci DJ, Saddoris MP, Burwell RD. 2002. Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. Behav Neurosci 116:479-488.
5. Burwell RD. 2000. The parahippocampal region: Corticocortical connectivity. Ann NY Acad Sci 911:25-42.
6. Burwell RD. 2001. Borders and cytoarchitecture of the perirhinal and postrhinal cortices in the rat. J Comp Neurol 437:17-41.
7. Burwell RD, Amaral DG. 1998a. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol 398:179-205.
8. 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.
9. Burwell RD, Hafeman DM. 2003. Positional firing properties of postrhinal cortex neurons. Neuroscience 119:577-588.
10. Bussey TJ, Muir JL, Everitt BJ, Robbins TW. 1996. Dissociable effects of anterior and posterior cingulate cortex lesions on the acquisition of a conditional visual discrimination: Facilitation of early learning vs. impairment of late learning. Behav Brain Res 82:45-56.
11. 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.
12. Chen LL, Lin LH, Barnes CA, McNaughton BL. 1994. Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp Brain Res 101:24-34.
13. Cooper BG, Mizumori SJ. 1999. Retrosplenial cortex inactivation selectively impairs navigation in darkness. Neuroreport 10:625-630.
14. Degenetais E, Thierry AM, Glowinski J, Gioanni Y. 2003. Synaptic influence of hippocampus on pyramidal cells of the rat prefrontal cortex: An in vivo intracellular recording study. Cereb Cortex 13:782-792.
15. Dias R, Aggleton JP. 2000. Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-place in the T-maze in the rat: Differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur J Neurosci 12:4457-4466.
16. Fisk GD, Wyss JM. 1997. Pressor and depressor sites are intermingled in the cingulate cortex of the rat. Brain Res 754:204-212.
17. Floresco SB, Seamans JK, Phillips AG. 1997. Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 17:1880-1890.
18. Freeman JH Jr, Cuppernell C, Flannery K, Gabriel M. 1996. Limbic thalamic, cingulate cortical and hippocampal neuronal correlates of discriminative approach learning in rabbits. Behav Brain Res 80:123-136.
19. Friston K. 2002. Beyond phrenology: What can neuroimaging tell us about distributed circuitry? Annu Rev Neurosci 25:221-250.
20. Frysztak RJ, Neafsey EJ. 1991. The effect of medial frontal cortex lesions on respiration, "freezing," and ultrasonic vocalizations during conditioned emotional responses in rats. Cereb Cortex 1:418-425.
21. Funahashi M, Stewart M. 1997. Presubicular and parasubicular cortical neurons of the rat: Functional separation of deep and superficial neurons in vitro. J Physiol 501 (Part 2):387-403.
22. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. 2004. Spatial representation in the entorhinal cortex. Science 305:1258-1264.
23. Gabriel M. 1990. Functions of anterior and posterior cingulate cortex during avoidance learning in rabbits. Prog Brain Res 85:467-482.
24. Gabriel M. 1993. Discriminative avoidance learning: A model system. In: Vogt BA, Gabriel M, editors. Neurobiology of the Cingulate Cortex and Limbic Thalamus. Boston: Birkhauser. pp 476-523.
25. Gabriel M, Sparenborg S. 1987. Posterior cingulate cortical lesions eliminate learning-related unit activity in the anterior cingulate cortex. Brain Res 409:151-157.
26. Gabriel M, Sparenborg SP, Stolar N. 1987. Hippocampal control of cingulate cortical and anterior thalamic information processing during learning in rabbits. Exp Brain Res 67:131-152.
27. Gabriel M, Kubota Y, Sparenborg S, Straube K, Vogt BA. 1991. Effects of cingulate cortical lesions on avoidance learning and training-induced unit activity in rabbits. Exp Brain Res 86:585-600.
28. Hannesson DK, Howland JG, Phillips AG. 2004. Interaction between perirhinal and medial prefrontal cortex is required for temporal order but not recognition memory for objects in rats. J Neurosci 24:4596-4604.
29. Hargreaves EL, Rao G, Lee I, Knierim JJ. 2005. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308:1792-1794.
30. Honda Y, Ishizuka N. 2004. Organization of connectivity of the rat presubiculum. I. Efferent projections to the medial entorhinal cortex. J Comp Neurol 473:463-484.
31. Horwitz B. 2003. The elusive concept of brain connectivity. Neuroimage 19:466-470.
32. Hurley KM, Herbert H, Moga MM, Saper CB. 1991. Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308:249-276.
33. 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.
34. Jay TM, Witter MP. 1991. 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.
35. Jones BF, Witter MP. 1999. Cingulate projections to the (para)hippocampal area in the rat: An anatomical tracer study. Soc Neurosci Abstr 357.16.
36. Jones BF, Groenewegen HJ, Witter MP. 2005. Intrinsic connections of the cingulate cortex in the rat suggest the existence of multiple functionally segregated networks. Neuroscience 133:193-207.
37. Kesner RP, Giles R. 1998. Neural circuit analysis of spatial working memory: Role of pre- and parasubiculum, medial and lateral entorhinal cortex. Hippocampus 8:416-423.
38. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB. 2002. Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci USA 99:10825-10830.
39. Kloosterman F, Van Haeften T, Witter MP, Lopes da Silva FH. 2003a. Electrophysiological characterization of interlaminar entorhinal connections: An essential link for re-entrance in the hippocampalentorhinal system. Eur J Neurosci 18:3037-3052.
40. Kloosterman F, Witter MP, Van Haeften T. 2003b. Topographical and laminar organization of subicular projections to the parahippocampal region of the rat. J Comp Neurol 455:156-171.
41. Kohler C. 1985. Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J Comp Neurol 236:504-522.
42. Lavenex P, Amaral DG. 2000. Hippocampal-neocortical interaction: A hierarchy of associativity. Hippocampus 10:420-430.
43. Maren S, Holt WG. 2004. Hippocampus and Pavlovian fear conditioning in rats: Muscimol infusions into the ventral, but not dorsal, hippocampus impair the acquisition of conditional freezing to an auditory conditional stimulus. Behav Neurosci 118:97-110.
44. Markowitsch HJ, Guldin WO. 1983. Heterotopic interhemispheric cortical connections in the rat. Brain Res Bull 10:805-810.
45. Moser MB, Moser EI. 1998. Functional differentiation in the hippocampus. Hippocampus. 8:608-619.
46. Naber PA, Witter MP. 1998. Subicular efferents are organized mostly as parallel projections: A double-labeling, retrograde-tracing study in the rat. J Comp Neurol 393:284-297.
47. Naber PA, Witter MP, Lopez da Silva FH. 1999. Perirhinal cortex input to the hippocampus in the rat: Evidence for parallel pathways, both direct and indirect. A combined physiological and anatomical study. Eur J Neurosci 11:4119-4133.
48. Naber PA, Lopes da Silva FH, Witter MP. 2001. 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.
49. Neafsey EJ. 1990. Prefrontal cortical control of the autonomic nervous system: Anatomical and physiological observations. Prog Brain Res 85:147-165.
50. Pastor J, Lafon M, Trave-Massuyes L, Demonet JF, Doyon B, Celsis P. 2000. Information processing in large-scale cerebral networks: The causal connectivity approach. Biol Cybern 82:49-59.
51. Paxinos C, Watson G. 1998. Tha Rat Brain in Stereotactic Co-ordinates. Sydney: Academinc Press.
52. Risterucci C, Terramorsi D, Nieoullon A, Amalric M. 2003. Excitotoxic lesions of the prelimbic-infralimbic areas of the rodent prefrontal cortex disrupt motor preparatory processes. Eur J Neurosci 17:1498-1508.
53. 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.
54. Scharfman HE, Witter MP, Schwarcz R. 2000. Preface to: The parahippocampal region. Implications for neurological and psychiatric diseases. Ann NY Acad Sci 911:R1-R111.
55. Sesack SR, Deutch AY, Roth RH, Bunney BS. 1989. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213-242.
56. Shibata H. 1994. Terminal distribution of projections from the retrosplenial area to the retrohippocampal region in the rat, as studied by anterograde transport of biotinylated dextran amine. Neurosci Res 20:331-336.
57. Simons JS, Spiers HJ. 2003. Prefrontal and medial temporal lobe interactions in long-term memory. Nat Rev Neurosci 4:637-648.
58. Steffenach HA, Witter M, Moser MB, Moser EI. 2005. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45:301-313.
59. Swanson LW, Kohler C. 1986. Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J Neurosci 6:3010-3023.
60. Takagishi M, Chiba T. 1991. Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: An anterograde tracer PHA-L study. Brain Res 566:26-39.
61. Takenouchi K, Nishijo H, Uwano T, Tamura R, Takigawa M, Ono T. 1999. Emotional and behavioural correlates of the anterior cingulate cortex during associative learning in rats. Neuroscience 93:1271-1287.
62. Taube JS, Kesslak JP, Cotman CW. 1992. Lesions of the rat postsubiculum impair performance on spatial tasks. Behav Neural Biol 57:131-143.
63. van Groen T, Wyss JM. 1990a. Connections of the retrosplenial granular a cortex in the rat. J Comp Neurol 300:593-606.
64. van Groen T, Wyss JM. 1990b. The connections of presubiculum and parasubiculum in the rat. Brain Res 518:227-243.
65. van Groen T, Wyss JM. 1990c. The postsubicular cortex in the rat: Characterization of the fourth region of the subicular cortex and its connections. Brain Res 529:165-177.
66. van Groen T, Wyss JM. 1992. Connections of the retrosplenial dysgranular cortex in the rat. J Comp Neurol 315:200-216.
67. van Groen T, Wyss JM. 2003. Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463:249-263.
68. Vann SD, Aggleton JP. 2002. Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory. Behav Neurosci 116:85-94.
69. Vann SD, Aggleton JP. 2004. Testing the importance of the retrosplenial guidance system: Effects of different sized retrosplenial cortex lesions on heading direction and spatial working memory. Behav Brain Res 155:97-108.
70. Vann SD, Brown MW, Aggleton JP. 2000a. Fos expression in the rostral thalamic nuclei and associated cortical regions in response to different spatial memory tests. Neuroscience 101:983-991.
71. Vann SD, Brown MW, Erichsen JT, Aggleton JP. 2000b. Using fos imaging in the rat to reveal the anatomical extent of the disruptive effects of fornix lesions. J Neurosci 20:8144-8152.
72. Vann SD, Kristina Wilton LA, Muir JL, Aggleton JP. 2003. Testing the importance of the caudal retrosplenial cortex for spatial memory in rats. Behav Brain Res 140:107-118.
73. Vertes RP. 2004. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58.
74. Vogt BA, Miller MW. 1983. Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 216:192-210.
75. Vogt BA, Peters A. 1981. Form and distribution of neurons in the rat cingulate cortex: Areas 32, 24 and 29. J Comp Neur 195:603-625.
76. Walton ME, Bannerman DM, Alterescu K, Rushworth MF. 2003. Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. J Neurosci 23:6475-6479.
77. Warburton EC, Aggleton JP, Muir JL. 1998. Comparing the effects of selective cingulate cortex lesions and cingulum bundle lesions on water maze performance by rats. Eur J Neurosci 10:622-634.
78. Whishaw IQ, Maaswinkel H, Gonzalez CL, Kolb B. 2001. Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions. Behav Brain Res 118:67-76.
79. Witter MP, Amaral DG. 2004. Hippocampal formation. The Rat Nervous System. Elsevier Academic Press. p 635-704.
80. Witter MP, Ostendorf RH, Groenewegen HJ. 1990. Heterogeneity in the dorsal subiculum of the rat. Distinct neuronal zones project to different cortical and subcortical targets. Eur J Neurosci 2:718-725.
81. Witter MP, Naber PA, Van Haeften T, Machielsen WC, Rombouts SA, Barkhof F, Scheltens P, Lopes da Silva FH. 2000a. Corticohippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10:398-410.
82. Witter MP, Wouterlood FG, Naber PA, Van Haeften T. 2000b. Anatomical organization of the parahippocampal-hippocampal network. Ann NY Acad Sci 911:1-24.
83. Wyss JM, van Groen T. 1992. Connections between the retrosplenial cortex and the hippocampal formation in the rat: A review. Hippocampus 2:1-11.
84. Zilles K, Zilles B, Schleicher A. 1980. A quantitative approach to cytoarchitectonics. VI. The areal pattern of the cortex of the albino rat. Anat Embryol (Berl) 159:335-360.