Differential roles of the dorsal and ventral hippocampus in predator odor contextual fear conditioning

Hippocampus

Volumn 23, Issue 6, 2013, Pages 451-466

  Wang, Melissa E ^a   Fraize, Nicolas P ^a   Yin, Linda ^a   Yuan, Robin K ^a   Petsagourakis, Despina ^a   Wann, Ellen G ^a   Muzzio, Isabel A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Contextual fear conditioning; Dorsal and ventral hippocampus; Predator odor

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONDITIONING; COYOTE; DEFENSIVE BEHAVIOR; DORSAL HIPPOCAMPUS; FEAR; FREEZING; HIPPOCAMPUS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; ODOR; PREDATOR; PRIORITY JOURNAL; STEREOTYPY; URINE; VENTRAL HIPPOCAMPUS;

ANIMALS; CONDITIONING (PSYCHOLOGY); COYOTES; FEAR; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; ODORS;

EID: 84878165664     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22105     Document Type: Article

References (113)

1. Amaral DG, Kurz J. 1985. An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J Comp Neurol 240:37-59.
2. Amaral DG, Witter MP. 1989. The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience 31:571-591.
3. Anagnostaras SG, Gale GD, Fanselow MS. 2001. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11:8-17.
4. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS. 2005. The effects of predator odors in mammalian prey species: A review of field and laboratory studies. Neurosci Biobehav Rev 29:1123-1144.
5. Baldi E, Lorenzini CA, Bucherelli C. 2004. Footshock intensity and generalization in contextual and auditory-cued fear conditioning in the rat. Neurobiol Learn Mem 81:162-166.
6. Barrientos RM, O'Reilly RC, Rudy JW. 2002. Memory for context is impaired by injecting anisomycin into dorsal hippocampus following context exploration. Behav Brain Res 134:299-306.
7. Blanchard DC, Canteras NS, Markham CM, Pentkowski NS, Blanchard RJ. 2005. Lesions of structures showing FOS expression to cat presentation: Effects on responsivity to a Cat, Cat odor, and nonpredator threat. Neurosci Biobehav Rev 29:1243-1253.
8. Blanchard DC, Griebel G, Blanchard RJ. 2001. Mouse defensive behaviors: Pharmacological and behavioral assays for anxiety and panic. Neurosci Biobehav Rev 25:205-218.
9. Blanchard DC, Markham C, Yang M, Hubbard D, Madarang E, Blanchard RJ. 2003. Failure to produce conditioning with lowdose trimethylthiazoline or cat feces as unconditioned stimuli. Behav Neurosci 117:360-368.
10. Blanchard RJ, Blanchard DC. 1969. Crouching as an index of fear. J Comp Physiol Psychol 67:370-375.
11. Blanchard RJ, Yang M, Li CI, Gervacio A, Blanchard DC. 2001. Cue and context conditioning of defensive behaviors to cat odor stimuli. Neurosci Biobehav Rev 25:587-595.
12. Bolles RC. 1970. Species-specific defense reactions and avoidance learning. Psychol Rev 77:32-48.
13. Bolles RC, Collier AC. 1976. The effect of predictive cues on freezing in rats. Anim Learn Behav 4:6-8.
14. Bolles RC, Fanselow MS. 1980. Perceptual-defensive-recuperative model of fear and pain. Behav Brain Sci 3:291-323.
15. Bouton ME, Westbrook RF, Corcoran KA, Maren S. 2006. Contextual and temporal modulation of extinction: Behavioral and biological mechanisms. Biol Psychiatry 60:352-360.
16. Brennan PA, Keverne EB. 1997. Neural mechanisms of mammalian olfactory learning. Prog Neurobiol 51:457-481.
17. Caffe AR, van Leeuwen FW, Luiten PG. 1987. Vasopressin cells in the medial amygdala of the rat project to the lateral septum and ventral hippocampus. J Comp Neurol 261:237-252.
18. Campeau S, Miserendino MJ, Davis M. 1992. Intra-amygdala infusion of the N-methyl-D-aspartate receptor antagonist AP5 blocks acquisition but not expression of fear-potentiated startle to an auditory conditioned stimulus. Behav Neurosci 106:569-574.
19. Canteras NS. 2002. The medial hypothalamic defensive system: Hodological organization and functional implications. Pharmacol Biochem Behav 71:481-491.
20. Canteras NS, Chiavegatto S, Ribeiro do Valle LE, Swanson LW. 1997. Severe reduction of rat defensive behavior to a predator by discrete hypothalamic chemical lesions. Brain Res Bull 44:297-305.
21. Canteras NS, Ribeiro-Barbosa ER, Comoli E. 2001. Tracing from the dorsal premammillary nucleus prosencephalic systems involved in the organization of innate fear responses. Neurosci Biobehav Rev 25:661-668.
22. Canteras NS, Simerly RB, Swanson LW. 1992. Connections of the posterior nucleus of the amygdala. J Comp Neurol 324:143-179.
23. Canteras NS, Simerly RB, Swanson LW. 1995. Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J Comp Neurol 360:213-245.
24. Davis M. 1989. Sensitization of the acoustic startle reflex by footshock. Behav Neurosci 103:495-503.
25. Dielenberg RA, Carrive P, McGregor IS. 2001. The cardiovascular and behavioral response to cat odor in rats: Unconditioned and conditioned effects. Brain Res 897:228-237.
26. Dielenberg RA, Hunt GE, McGregor IS. 2001. "When a rat smells a cat": The distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 104:1085-1097.
27. Dielenberg RA, McGregor IS. 2001. Defensive behavior in rats towards predatory odors: A review. Neurosci Biobehav Rev 25:597-609.
28. Do Monte FH, Canteras NS, Fernandes D, Assreuy J, Carobrez AP. 2008. New perspectives on beta-adrenergic mediation of innate and learned fear responses to predator odor. J Neurosci 28:13296-13302.
29. Dong HW, Swanson LW, Chen L, Fanselow MS, Toga AW. 2009. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci USA 106:11794-11799.
30. Eilam D. 2005. Die hard: A blend of freezing and fleeing as a dynamic defense-implications for the control of defensive behavior. Neurosci Biobehav Rev 29:1181-1191.
31. Endres T, Fendt M. 2007. Conditioned behavioral responses to a context paired with the predator odor trimethylthiazoline. Behav Neurosci 121:594-601.
32. Endres T, Fendt M. 2009. Aversion- vs fear-inducing properties of 2,4,5-trimethyl-3-thiazoline, a component of fox odor, in comparison with those of butyric acid. J Exp Biol 212:2324-2327.
33. Fanselow MS. 1980. Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15:177-182.
34. Fanselow MS. 1982. The postshock activity burst. Anim Learn Behav 10:448-454.
35. Fanselow MS. 1986. Associative vs topographical accounts of the immediate shock freezing deficit in rats: Implications for the response selection rules governing species-specific defensive reactions. Learn Motiv 17:16-39.
36. Fanselow MS. 2000. Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110:73-81.
37. Fanselow MS, Bolles RC. 1979. Naloxone and shock-elicited freezing in the rat. J Comp Physiol Psychol 93:736-744.
38. Fanselow MS, Dong HW. 2010. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19.
39. Fendt M. 2006. Exposure to urine of canids and felids, but not of herbivores, induces defensive behavior in laboratory rats. J Chem Ecol 32:2617-2627.
40. Fendt M, Endres T. 2008. 2,3,5-Trimethyl-3-thiazoline (TMT), a component of fox odor-Just repugnant or really fear-inducing? Neurosci Biobehav Rev 32:1259-1266.
41. Ferrero DM, Lemon JK, Fluegge D, Pashkovski SL, Korzan WJ, Datta SR, Spehr M, Fendt M, Liberles SD. 2011. Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci USA 108:11235-11240.
42. Fletcher BR, Calhoun ME, Rapp PR, Shapiro ML. 2006. Fornix lesions decouple the induction of hippocampal arc transcription from behavior but not plasticity. J Neurosci 26:1507-1515.
43. Gage FH, Thompson RG. 1980. Differential distribution of norepinephrine and serotonin along the dorsal-ventral axis of the hippocampal formation. Brain Res Bull 5:771-773.
44. Gewirtz JC, McNish KA, Davis M. 2000. Is the hippocampus necessary for contextual fear conditioning? Behav Brain Res 110:83-95.
45. Grant EC, Mackintosh JH. 1963. A comparison of the social postures of some common laboratory rodents. Behaviour 21:246-259.
46. Henke PG. 1990. Hippocampal pathway to the amygdala and stress ulcer development. Brain Res Bull 25:691-695.
47. Herz RS. 1998. Are odors the best cues to memory? A cross-modal comparison of associative memory stimuli. Ann NY Acad Sci USA 855:670-674.
48. Herz RS, Cupchik GC. 1995. The emotional distinctiveness of odorevoked memories. Chem Senses 20:517-528.
49. Jacobson L, Sapolsky R. 1991. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118-134.
50. Ji J, Maren S. 2007. Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17:749-758.
51. Jung MW, Wiener SI, McNaughton BL. 1994. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14:7347-7356.
52. Kanoski SE, Hayes MR, Greenwald HS, Fortin SM, Gianessi CA, Gilbert JR, Grill HJ. 2011. Hippocampal leptin signaling reduces food intake and modulates food-related memory processing. Neuropsychopharmacology 36:1859-1870.
53. Kehoe EJ, White NE. 2002. Extinction revisited: Similarities between extinction and reductions in US intensity in classical conditioning of the rabbit's nictitating membrane response. Anim Learn Behav 30:96-111.
54. Kemppainen S, Jolkkonen E, Pitkänen A. 2002. Projections from the posterior cortical nucleus of the amygdala to the hippocampal formation and parahippocampal region in rat. Hippocampus 12:735-755.
55. 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.
56. Kim JJ, Fanselow MS. 1992. Modality-specific retrograde amnesia of fear. Science 256:675-677.
57. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser MB. 2008. Finite scale of spatial representation in the hippocampus. Science 321:140-143.
58. 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.
59. Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, Mori K, Sakano H. 2007. Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503-508.
60. Kohler C, Schultzberg M, Radesater AC. 1987. Distribution of neuropeptide Y receptors in the rat hippocampal region. Neurosci Lett 75:141-146.
61. Lasseter HC, Xie X, Ramirez DR, Fuchs RA. 2010. Sub-region specific contribution of the ventral hippocampus to drug contextinduced reinstatement of cocaine-seeking behavior in rats. Neuroscience 171:830-839.
62. Luo M, Fee MS, Katz LC. 2003. Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299:1196-1201.
63. Maguire EA, Frackowiak RS, Frith CD. 1997. Recalling routes around london: Activation of the right hippocampus in taxi drivers. J Neurosci 17:7103-7110.
64. 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.
65. Majchrzak M, Ferry B, Marchand AR, Herbeaux K, Seillier A, Barbelivien A. 2006. Entorhinal cortex lesions disrupt fear conditioning to background context but spare fear conditioning to a tone in the rat. Hippocampus 16:114-124.
66. Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, Frankland PW, Kida S. 2009. Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci 29:402-413.
67. Maren S, Aharonov G, Fanselow MS. 1997. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 88:261-274.
68. Maren S, Holt W. 2000. The hippocampus and contextual memory retrieval in Pavlovian conditioning. Behav Brain Res 110:97-108.
69. 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.
70. Maren S, Quirk GJ. 2004. Neuronal signalling of fear memory. Nat Rev Neurosci 5:844-852.
71. Martin LK, Riess D. 1969. Effects of US intensity during previous discrete delay conditioning on conditioned acceleration during avoidance extinction. J Comparative Physiol Psychol 69:196-200.
72. Matus-Amat P, Higgins EA, Barrientos RM, Rudy JW. 2004. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci 24:2431-2439.
73. McGregor IS, Hargreaves GA, Apfelbach R, Hunt GE. 2004. Neural correlates of cat odor-induced anxiety in rats: Region-specific effects of the benzodiazepine midazolam. J Neurosci 24:4134-4144.
74. McGregor IS, Schrama L, Ambermoon P, Dielenberg RA. 2002. Not all 'predator odours' are equal: Cat odour but not 2,4,5 trimethylthiazoline (TMT; fox odour) elicits specific defensive behaviours in rats. Behav Brain Res 129:1-16.
75. McNaughton BL, Barnes CA, O'Keefe J. 1983. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52:41-49.
76. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB. 2006. Path integration and the neural basis of the 'cognitive map'. Nat Rev Neurosci 7:663-678.
77. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
78. Moser E, Moser MB, Andersen P. 1993. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci 13:3916-3925.
79. Moser MB, Moser EI. 1998. Functional differentiation in the hippocampus. Hippocampus 8:608-619.
80. Moser MB, Moser EI, Forrest E, Andersen P, Morris RG. 1995. Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci USA 92:9697-9701.
81. O'keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map. Oxford University Press.
82. Osborne FH, Mattingly BA, Redmon WK, Osborne JS. 1975. Factors affecting the measurement of classically conditioned fear in rats following exposure to escapable versus inescapable signaled shock. J Exp Psychol Anim Behav Process 1:364-373.
83. Pavlov IP. 1927. Conditioned Reflexes. London: Oxford University Press. Pazos A, Cortes R, Palacios JM. 1985. Quantitative autoradiographic mapping of serotonin receptors in the rat brain. II. Serotonin-2 receptors. Brain Res 346:231-249.
84. Pentkowski NS, Blanchard DC, Lever C, Litvin Y, Blanchard RJ. 2006. Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur J Neurosci 23:2185-2196.
85. Petrovich GD, Canteras NS, Swanson LW. 2001. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Brain Res Rev 38:247-289.
86. Phillips RG, LeDoux JE. 1992. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285.
87. Phillips RG, LeDoux JE. 1994. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learn Mem 1:34-44.
88. Pitkanen 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 NY Acad Sci 911:369-391.
89. Powers MM, Clark G. 1955. An evaluation of cresyl echt violet acetate as a Nissl stain. Stain Technol 30:83-88.
90. Quirk GJ, Pare D, Richardson R, Herry C, Monfils MH, Schiller D, Vicentic A. 2010. Erasing fear memories with extinction training. J Neurosci 30:14993-14997.
91. Radulovic J, Kammermeier J, Spiess J. 1998. Relationship between fos production and classical fear conditioning: Effects of novelty, latent inhibition, and unconditioned stimulus preexposure. J Neurosci 18:7452-7461.
92. Restrepo D, Arellano J, Oliva AM, Schaefer ML, Lin W. 2004. Emerging views on the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice. Horm Behav 46:247-256.
93. Rosen JB. 2004. The neurobiology of conditioned and unconditioned fear: A neurobehavioral system analysis of the amygdala. Behav Cogn Neurosci Rev 3:23-41.
94. Rosen JB, Pagani JH, Rolla KL, Davis C. 2008. Analysis of behavioral constraints and the neuroanatomy of fear to the predator odor trimethylthiazoline: A model for animal phobias. Neurosci Biobehav Rev 32:1267-1276.
95. Royer S, Sirota A, Patel J, Buzsaki G. 2010. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J Neurosci 30:1777-1787.
96. Rudy JW, Barrientos RM, O'Reilly RC. 2002. Hippocampal formation supports conditioning to memory of a context. Behav Neurosci 116:530-538.
97. Rudy JW, Matus-Amat P. 2005. The ventral hippocampus supports a memory representation of context and contextual fear conditioning: Implications for a unitary function of the hippocampus. Behav Neurosci 119:154-163.
98. Samuelsen CL, Meredith M. 2009. The vomeronasal organ is required for the male mouse medial amygdala response to chemical-communication signals, as assessed by immediate early gene expression. Neuroscience 164:1468-1476.
99. Shapiro M. 2001. Plasticity, hippocampal place cells, and cognitive maps. Arch Neurol 58:874-881.
100. Siegel A, Tassoni JP. 1971. Differential efferent projections from the ventral and dorsal hippocampus of the cat. Brain Behav Evol 4:185-1200.
101. Sigmundi RA, Bouton ME, Bolles RC. 1980. Conditioned freezing in the rat as a function of shock intensity and CS modality. Bull Psychonomic Soc 15:254-256.
102. Sotres-Bayon F, Bush DE, LeDoux JE. 2004. Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn Mem 11:525-535.
103. 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.
104. Suzuki A, Mukawa T, Tsukagoshi A, Frankland PW, Kida S. 2008. Activation of LVGCCs and CB1 receptors required for destabilization of reactivated contextual fear memories. Learn Mem 15:426-433.
105. Takahashi LK, Nakashima BR, Hong H, Watanabe K. 2005. The smell of danger: A behavioral and neural analysis of predator odorinduced fear. Neurosci Biobehav Rev 29:1157-1167.
106. Takahashi LK, Hubbard DT, Lee I, Dar Y, Sipes SM. 2007. Predator odor-induced conditioned fear involves the basolateral and medial amygdala. Behav Neurosci 121:100-110.
107. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, Cusick A, Riley ZL, Sunkin SM, Bernard A, Puchalski RB, Gage FH, Jones AR, Bajic VB, Hawrylycz MJ, Lein ES. 2008. Genomic anatomy of the hippocampus. Neuron 60:1010-1021.
108. Tronson NC, Schrick C, Guzman YF, Huh KH, Srivastava DP, Penzes P, Guedea AL, Gao C, Radulovic J. 2009. Segregated populations of hippocampal principal CA1 neurons mediating conditioning and extinction of contextual fear. J Neurosci 29:3387-3394.
109. Vann SD, Brown MW, Erichsen JT, Aggleton JP. 2000. Using Fos imaging in the rat to reveal the anatomical extent of the disruptive effects of fornix lesions. J Neurosci 20:8144-8152.
110. Vermetten E, Schmahl C, Southwick SM, Bremner JD. 2007. Positron tomographic emission study of olfactory induced emotional recall in veterans with and without combat-related posttraumatic stress disorder. Psychopharmacol Bull 40:8-30.
111. Verney C, Baulac M, Berger B, Alvarez C, Vigny A, Helle KB. 1985. Morphological evidence for a dopaminergic terminal field in the hippocampal formation of young and adult rat. Neuroscience 14:1039-1052.
112. Wallace KJ, Rosen JB. 2000. Predator odor as an unconditioned fear stimulus in rats: Elicitation of freezing by trimethylthiazoline, a component of fox feces. Behav Neurosci 114:912-922.
113. Young SL, Fanselow MS. 1992. Associative regulation of Pavlovian fear conditioning: unconditional stimulus intensity, incentive shifts, and latent inhibition. J Exp Psychol Anim Behav Process 18: 400-413.