Temporary inactivation of dorsal hippocampus attenuates explicitly nonspatial, unimodal, contextual fear conditioning

Neurobiology of Learning and Memory

Volumn 90, Issue 1, 2008, Pages 261-268

  Parsons, Teresa Camille ^a   Otto, Tim ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Contextual conditioning; Fear conditioning; Hippocampus; Olfaction; Pavlovian conditioning; Spatial learning; Temporary inactivation

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; MUSCIMOL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; CONDITIONED REFLEX; CONDITIONING; CONTROLLED STUDY; DEPTH PERCEPTION; DORSAL HIPPOCAMPUS; FEAR; GROOMING; HIPPOCAMPUS; MALE; MOBILIZATION; NONHUMAN; RAT; REARING; SMELLING; SPRAGUE DAWLEY RAT; STIMULUS RESPONSE;

ACOUSTIC STIMULATION; ANIMALS; CONDITIONING, CLASSICAL; FEAR; FREEZING REACTION, CATALEPTIC; GABA AGONISTS; HIPPOCAMPUS; MALE; MUSCIMOL; ODORS; RATS; RATS, SPRAGUE-DAWLEY; SMELL; SPACE PERCEPTION;

EID: 44649143147     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2008.03.007     Document Type: Article

References (62)

1. Anagnostaras S.G., Gale G.D., and Fanselow M.S. The hippocampus and contextual fear conditioning: Recent controversies and advances. Hippocampus 11 (2001) 8-17
2. Anagnostaras S.G., Maren S., and Fanselow M.S. Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: Within-subjects examination. Journal of Neuroscience 19 (1999) 1106-1114
3. Anderson M.I., Killing S., Morris C., O'Donoghue A., Onyiagha D., Stevenson R., Verriotis M., and Jeffrey K.J. Behavioral correlates of the distributed coding of spatial context. Hippocampus 16 (2006) 730-742
4. Bailey D.J., Kim J.J., Sun W., Thompson R.F., and Helmstetter F.J. Acquisition of fear conditioning in rats requires the synthesis of mRNA in the amygdala. Behavioral Neuroscience 113 (1999) 276-282
5. Balsam P.D., and Tomie A. Context and learning (1985), Erlbaum, Hillsdale, NJ
6. Bannerman D.M., Deacon R.M.I., Offen S., Friswell J., Grubb M., and Rawlins J.N.P. A double dissociation of function within the hippocampus: Spatial memory and hyponeophagia. Behavioral Neuroscience 116 (2002) 884-901
7. Bannerman D.M., Rawlins J.N.P., and Good M.A. The drugs don't work-or do they? Pharmacological and transgenic studies of the contribution of NMDA and GluR-A-containing AMPA receptors to hippocampal-dependent memory. Psychopharmacology 188 (2006) 552-566
8. Bannerman D.M., Rawlins J.N.P., McHugh S.B., Deacon R.M.J., Yee B.K., Bast T., Zhang W.-N., Pothuizen H.J., and Feldon J. Regional dissociations within the hippocampus--memory and anxiety. Neuroscience and Biobehavioral Reviews 28 (2004) 273-283
9. Barry C., Lever C., Hayman R., Hartley R., Burton S., O'Keefe J., Jeffrey K.J., and Burgess N. The boundary vector cell model of place cell firing and spatial memory. Reviews in Neuroscience 17 (2006) 71-97
10. Beylin A.V., Gandhi C.C., Wood G.E., Talk A.C., Matzel L.D., and Shors T.J. The role of the hippocampus in trace conditioning: Temporal discontinuity or task difficulty?. Neurobiology of Learning and Memory 76 (2001) 447-461
11. Blanchard D.C., and Blanchard R.J. Innate and conditioned reactions to threat in rats with amygdaloid lesions. Journal of Comparative Physiology and Psychology 81 (1972) 281-290
12. Chang S.D., Chen D.Y., and Liang K.C. Infusion of lidocaine in to the dorsal hippocampus before or after the shock training phase impaired conditioned freezing in a two-phase training task of contextual fear conditioning. Neurobiology of Learning and Memory 89 (2008) 95-105
13. Chan-Palay V. Quantitative visualization of gamma-aminobutyric acid receptors in hippocampus and area dentata demonstrated by 3H muscimol autoradiography. Proceedings of the National Academy of Science 75 (1978) 2516-2520
14. Chen J., Kitanishi T., Ikeda T., Matsuki N., and Yamada M.K. Contextual learning induces an increase in the number of hippocampal CA1 neurons expressing high levels of BDNF. Neurobiology of Learning and Memory 88 (2007) 409-415
15. Corcoran K.A., and Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. Journal of Neuroscience 21 (2001) 1720-1728
16. Cousens G., and Otto T. Both pre- and post-training lesions of the basolateral amygdala abolish the expression of olfactory and contextual fear conditioning. Behavioral Neuroscience 112 (1998) 1092-1103
17. Da Silva W.C., Bonini J.S., Bevilaqua L.R.M., Medina J.H., Izquierdo I., and Cammarota M. Inhibition of mRNA synthesis in the hippocampus impairs consolidation and reconsolidation of spatial memory. Hippocampus 18 (2008) 29-39
18. Dalla C., Bangasser D.A., Edgecomb C., and Shors T.J. Neurogenesis and learning: Acquisition and asymptotic performance predict how many new cells survive in the hippocampus. Neurobiology of Learning and Memory 88 (2007) 143-148
19. Davidson T.L., and Jarrard L.E. A role for the hippocampus is the utilization of hunger signals. Behavioral and Neural Biology 59 (1993) 167-171
20. Edeline J., Hars B., Hennevin E., and Cotillon N. Muscimol diffusion after intracerebral microinjections: A reevaluation based on electrophysiological and autoradiographic quantifications. Neurobiology of Learning and Memory 78 (2002) 100-124
21. Eichenbaum H., Otto T., and Cohen N.J. Two functional components of the hippocampal memory system. Behavioral and Brain Sciences 17 (1994) 449-517
22. Fanselow M. Conditional and unconditional components of post shock freezing in rats. Pavlovian Journal of Biological Science 15 (1980) 177-182
23. Fendt M., and Fanselow M.S. The neuroanatomical and neurochemical basis of conditioned fear. Neuroscience and Biobehavioral Reviews 23 (1999) 743-760
24. Goodrich-Hunsaker N.J., Hunsaker M.R., and Kesner R.P. The interactions and dissociations of the dorsal hippocampus subregions: How the dentate gyrus, CA3, and CA1 process spatial information. Behavioral Neuroscience 122 (2008) 16-26
25. Hein A.M., Stutzman D.L., Bland S.T., Barrientos R.M., Watkins L.R., Rudy J.W., and Maier S.F. Prostaglandins are necessary and sufficient to induce contextual fear learning impairments after interleukin-1 beta injections into the dorsal hippocampus. Neuroscience 150 (2007) 754-763
26. Helmstetter F.J. Contribution of the amygdala to learning and performance of conditional fear. Physiology and Behavior 51 (1992) 1271-1276
27. Helmstetter F.J., and Bellgowan P.S. Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats. Behavioral Neuroscience 108 (1994) 1005-1009
28. Herzog C., and Otto T. Odor-guided fear conditioning. II. Lesions of anterior perirhinal cortex disrupt fear conditioned to the explicit CS but not to the training context. Behavioral Neuroscience 111 (1997) 1265-1274
29. Herzog C.D., and Otto T. Contributions of anterior perirhinal cortex to olfactory and contextual fear conditioning. Neuroreport 9 (1998) 1855-1859
30. Hock B.J., and Bunsey M.D. Differential effects of dorsal and ventral hippocampal lesions. Journal of Neuroscience 18 (1998) 7027-7032
31. Holt W., and Maren S. Muscimol inactivation of the dorsal hippocampus impairs contextual retrieval of fear memory. Journal of Neuroscience 19 (1999) 9054-9062
32. Hubbard D.T., Nakashima B.R., Lee I., and Takahashi L.K. Activation of basolateral amygdala corticotropin-releasing factor 1 receptors modulates the consolidation of contextual fear. Neuroscience 150 (2007) 818-821
33. Hulse S.H., Cynx J., and Humpal J. Absolute and relative pitch discrimination in serial pitch perception by birds. Journal of Experimental Psychology: General 113 (1984) 38-54
34. Jarrard L.E. Selective hippocampal lesions and behavior: Effects of kainic acid lesions on performance of place and cue tasks. Behavioral Neuroscience 97 (1983) 251-259
35. Jones P.M., Pearce J.M., Davies V.J., Good M.A., and McGregor A. Impaired processing of local geometric features during navigation in a water maze following hippocampal lesions in rats. Behavioral Neuroscience 121 (2007) 1258-1271
36. Kim J.J., and Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 256 (1992) 657-677
37. Kim J.J., Rison R.A., and Fanselow M.S. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behavioral Neuroscience 197 (1993) 1093-1098
38. Levy W.B. A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 6 (1996) 579-591
39. Lopez-Fernandez M., Montaron M., Varea E., Rougon G., Venero C., Abrous D.N., and Sandi C. Upregulation of polysialylated neural cell adhesion molecule in the dorsal hippocampus after contextual fear conditioning is involved in long-term memory formation. Journal of Neuroscience 27 (2007) 4552-4561
40. Maren S., Aharonov G., and Fanselow M.S. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behavioral Brain Research 88 (1997) 261-274
41. Maren S., and Fanselow M.S. Electrolytic lesions of the dorsal hippocampus, fimbria-fornix, or entorhinal cortex produce anterograde deficits in contextual fear conditioning in rats. Neurobiology of Learning and Memory 67 (1997) 142-149
42. Martin J.H. Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neuroscience Letters 127 (1991) 160-164
43. Matus-Amat P., Higgins E.A., Barrientos R.M., and Rudy J. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. Journal of Neuroscience 24 (2004) 2431-2439
44. Moita M.A., Rosis S., Zhou Y., LeDoux J.E., and Blair H.T. Putting fear in its place: Remapping of hippocampal place cells during fear conditioning. Journal of Neuroscience 24 (2004) 7015-7023
45. Moser E., Moser M.B., and Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but it is hardly present following ventral lesions. Journal of Neuroscience 13 (1993) 3916-3925
46. Moyer Jr. J.R., Deyo R.A., and Disterhoft J.F. Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience 104 (1990) 243-252
47. Otto T., Cousens G.A., and Rajewski K. Odor-guided fear conditioning in rats: Acquisition, retention, and latent inhibition. Behavioral Neuroscience 111 (1997) 1257-1264
48. Otto T., and Poon P. Dorsal hippocampal contributions to unimodal contextual conditioning. The Journal of Neuroscience 26 (2006) 6603-6609
49. Overton D.A. State-dependent or "dissociated" learning produced with pentobarbital. Journal of Comparative and Physiological Psychology 5 (1964) 3-12
50. Phillips R., and LeDoux J. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 106 (1992) 274-285
51. Randrich A., and Ross R.T. Contextual stimuli mediate the effects of pre- and post-exposure to the unconditioned stimulus on conditioned suppression. In: Balsam P.D., and Tomie A. (Eds). Context and learning (1985), Erlbaum, Hillsdale, NJ 105-132
52. Richmond M.A., Yee B.K., Pouzet B., Veenan L., Rawlins J.N.P., Feldon J., and Bannerman D.M. Dissociating context and space within the hippocampus: Effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behavioral Neuroscience 113 (1999) 1189-1203
53. Schafe G.E., Nader K., Blair H.T., and LeDoux J.E. Memory consolidation of Pavlovian fear conditioning: A cellular and molecular perspective. Trends in Neuroscience 24 (2001) 540-546
54. Schettino L.F., and Otto T. Patterns of Fos expression in the amygdala and ventral perirhinal cortex induced by training in an olfactory fear conditioning paradigm. Behavioral Neuroscience 115 (2001) 1257-1272
55. Solomon P.R., Vander Schaaf E.R., Thompson R.F., and Weisz D.J. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behavioral Neuroscience 100 (1986) 729-744
56. Steele R.J., and Morris R.G. Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus 9 (1999) 118-136
57. Thomas D.R. Contextual stimulus control of operant responding in pigeons. In: Balsam P.D., and Tomie A. (Eds). Context and learning (1985), Erlbaum, Hillsdale, NJ 295-321
58. Wallenstein G.V., Eichenbaum H., and Hasselmo M.E. The hippocampus as an associator of discontiguous events. Trends in Neuroscience 21 (1998) 317-323
59. Wallenstein G.V., and Hasselmo M.E. GABAergic modulation of hippocampal population activity: Sequence learning, place field development, and the phase precession effect. Journal of Neurophysiology 78 (1997) 393-408
60. Yoon T., and Otto T. Contributions of the dorsal and ventral hippocampus to trace fear conditioning in rats. Society for Neuroscience Abstracts 89 (2001) 14
61. Yoon T., and Otto T. Differential contributions of dorsal vs. ventral hippocampus to auditory trace fear conditioning. Neurobiology of Learning and Memory 87 (2007) 464-475
62. Young S.L., Bohenek D.L., and Fanselow M.S. NMDA processes mediate anterograde amnesia of contextual fear conditioning induced by hippocampal damage: Immunization against amnesia by context preexposure. Behavioral Neuroscience 108 (1994) 19-29