Double dissociation of function within the hippocampus: Spatial memory and hyponeophagia

Behavioral Neuroscience

Volumn 116, Issue 5, 2002, Pages 884-901

  Bannerman, D M ^a   Deacon, R M J ^a   Offen, S ^a   Friswell, J ^a   Grubb, M ^a   Rawlins, J N P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE DERIVATIVE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BODY WEIGHT; BRAIN FUNCTION; BRAIN INJURY; CONTROLLED STUDY; HIPPOCAMPUS; HISTOLOGY; LOCOMOTION; MALE; MAZE TEST; MEMORY; NONHUMAN; RAT; REWARD; SOCIAL BEHAVIOR; SOCIAL INTERACTION;

EID: 0036786050     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.116.5.884     Document Type: Article

References (56)

1. Aggleton, J. P., Blindt, H. S., & Rawlins J. N. P. (1989). Effects of amygdaloid and amygdaloid-hippocampal lesions on object recognition and spatial working memory in rats. Behavioral Neuroscience, 103, 962-974.
2. Andrews, N., & File, S. E. (1993). Handling history of rats modifies behavioural effects of drugs in the elevated plus-maze test of anxiety. European Journal of Pharmacology, 235, 109-112.
3. Bannerman, D. M., Yee, B. K., Good, M. A., Heupel, M. J., Iversen, S. D., & Rawlins, J. N. P. (1999). Double dissociation of function within the hippocampus: A comparison of dorsal, ventral, and complete hippocampal cytotoxic lesions. Behavioral Neuroscience, 113, 1170-1188.
4. Britton, D. R., & Britton, K. T. (1981). A sensitive open field measure of anxiolytic drug activity. Pharmacology Biochemistry and Behavior, 15, 577-582.
5. Colombo, M., Fernandez, T., Nakamura, K., & Gross, C. G. (1998). Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. Journal of Neurophysiology, 80, 1002-1005.
6. Crabbe, J. C., Wahlsten, D., & Dudek, B. C. (1999, June 4). Genetics of mouse behavior: Interactions with laboratory environment. Science, 284, 1670-1672.
7. Dawson, G. R., & Tricklebank, M. D. (1995). Use of the elevated plusmaze in the search for novel anxiolytic agents. Trends in Pharmacological Sciences, 16, 33-36.
8. Deacon, R. M. J., Bannerman, D. M., & Rawlins, J. N. P. (2001). Anxiolytic effects of cytotoxic hippocampal lesions in rats. Behavioral Neuroscience, 115, 43-57.
9. Douglas, R. J., & Isaacson, R. L. (1964). Hippocampal lesions and activity. Psychonomic Science, 1, 187-188.
10. File, S. E. (1980). The use of social interaction as a method for detecting anxiolytic activity of chlordiazepoxide-like drugs. Journal of Neuroscience Methods, 2, 219-238.
11. File, S. E. (1992). Behavioral detection of anxiolytic action. In J. M. Elliot, D. J. Heal, & C. A. Marsden (Eds.), Experimental approaches to anxiety and depression (pp. 25-44). London: Wiley.
12. Gonzalez, L. E., Ouagazzal, A. M., & File, S. E. (1998). Stimulation of benzodiazepine receptors in the dorsal hippocampus and median raphe reveals differential GABAergic control in two animal tests of anxiety. European Journal of Neuroscience, 10, 3673-3680.
13. Gray, J. A. (1982). The neuropsychology of anxiety (1st ed.). Oxford, England: Oxford University Press.
14. Gray, J. A., & McNaughton, N. (2000). The neuropsychology of anxiety (2nd ed.). Oxford, England: Oxford University Press.
15. Handley, S. L., & Mithani, S. (1984). Effects of alpha-adrenoreceptor agonists and antagonists in a maze exploration model of 'fear'-motivated behavior. Naunyn-Schmiedeberg's Archives of Pharmacology, 327, 1-5.
16. Herman, J. P., Cullinan, W. E., Morano, M. I., Akil, H., & Watson, S. J. (1995). Contribution of the ventral subiculum to inhibitory regulation of the hypothalamo-pituitary-adrenocortical axis. Journal of Neuroendocrinology, 7, 475-482.
17. Herman, J. P., Cullinan, W. E., Young, E. A., Akil, H., & Watson, S. J. (1992). Selective forebrain fiber tract lesions implicate ventral hippocampal structures in tonic regulation of paraventricular nucleus corticotropin-releasing hormone (CRH) and arginine vasopressin (AVP) mRNA expression. Brain Research, 592, 228-238.
18. Hock, B. J., Jr., & Bunsey, M. D. (1998). Differential effects of dorsal and ventral hippocampal lesions. Journal of Neuroscience, 18, 7027-7032.
19. Hogg, S. (1996). A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacology Biochemistry and Behavior, 54, 21-30.
20. Jacobsen, L., & Sapolsky, R. (1991). The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocrine Reviews, 12, 118-134.
21. Jarrard, L. E. (1968). Behavior of hippocampal-lesioned rats in home cage and novel situations. Physiology & Behavior, 3, 65-70.
22. Jarrard, L. E. (1989). On the use of ibotenic acid to lesion selectively different components of the hippocampal formation. Journal of Neuroscience Methods, 29, 251-259.
23. Jung, M. W., Wiener, S. I., & McNaughton, B. L. (1994). Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. Journal of Neuroscience, 14, 7347-7356.
24. Kolb, B., & Nonneman, A. J. (1974). Frontolimbic lesions and social behavior in the rat. Physiology & Behavior, 13, 637-643.
25. Krane, R. V., Sinnamon, H. M., & Thomas, G. J. (1976). Conditioned taste aversions and neophobia in rats with hippocampal lesions. Journal of Comparative and Physiological Psychology, 90, 680-693.
26. Maguire, E. A., Gadian, D. G., Johnsrude, I. S., Good, C. D., Ashburner, J., Frackowiak, R. S. J., & Frith, C. D. (2000). Navigation-related structural change in the hippocampi of taxi drivers. Proceedings of the Natural Academy of Sciences, USA, 97, 4398-4403.
27. Maren, S. (1999). Neurotoxic or electrolytic lesions of the ventral subiculum produce deficits in the acquisition and expression of Pavlovian fear conditioning in rats. Behavioral Neuroscience, 113, 283-290.
28. Maren, S., Aharonov, G., & Fanselow, M. S. (1997). Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behavioural Brain Research, 88, 261-274.
29. Menard, J., & Treit, D. (1996a). Does tolerance develop to the anxiolytic effects of septal lesions? Physiology & Behavior, 59, 311-318.
30. Menard, J., & Treit, D. (1996b). Lateral and medial septal lesions reduce anxiety in the plus-maze and probe-burying tests. Physiology & Behavior, 60, 845-853.
31. Miller, J. S., Nonneman, A. J., Kelly, K. S., Neisewander, J. L., & Isaac, W. L. (1986). Disruption of neophobia, conditioned odor aversion, and conditioned taste aversion in rats with hippocampal lesions. Behavioral and Neural Biology, 45, 240-253.
32. Morris, R. G. M. (1981). Spatial localisation does not depend on the presence of local cues. Learning and Motivation, 12, 239-269.
33. Morris, R. G. M. (1984). Developments of a water maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods, 11, 47-60.
34. Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982, June 24). Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681-683.
35. Morris, R. G. M., Schenk, F., Tweedie, F., & Jarrard, L. E. (1990). Ibotenate lesions of the hippocampus and/or subiculum: Dissociating components of allocentric spatial learning. European Journal of Neuroscience, 2, 1016-1028.
36. Moser, M.-B., & Moser, E. I. (1998). Functional differentiation in the hippocampus. Hippocampus, 8, 608-619.
37. Moser, M.-B., Moser, E. I., Forrest, E., Andersen, P., & Morris, R. G. M. (1995). Spatial learning with a minislab in the dorsal hippocampus. Proceedings of the National Academy of Sciences, USA, 92, 9697-9701.
38. O'Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford, England: Oxford University Press.
39. Paxinos, G., & Watson, C. (1986). The rat brain in stereotaxic coordinates (2nd ed.). San Diego, CA: Academic Press.
40. Paxinos, G., & Watson, C. (1998). The rat brain in stereotaxic coordinates (4th ed.). San Diego, CA: Academic Press.
41. Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985). Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. Journal of Neuroscience Methods, 14, 149-167.
42. Pesold, C., & Treit, D. (1992). Excitotoxic lesions of the septum produce anxiolytic effects in the elevated plus-maze and the shock-probe burying tests. Physiology & Behavior, 52, 37-47.
43. Ramos, A., Berton, O., Mormede, P., & Chauloff, F. (1997). A multipletest study of anxiety-related behaviors in six inbred rat strains. Behavioural Brain Research, 85, 57-69.
44. Richmond, M. A., Yee, B. K., Pouzet, B., Veenman, L., Rawlins, J. N. P., Feldon, J., & Bannerman, D. M. (1999). Dissociating context and space within the hippocampus: Effects of complete, dorsal and ventral excitotoxic lesions on conditioned freezing and spatial learning. Behavioral Neuroscience, 113, 1189-1203.
45. Shephard, R. A., & Broadhurst, P. L. (1982). Effects of diazepam and picrotoxin on hyponeophagia in rats. Neuropharmacology, 21, 771-773.
46. Shephard, R. A., & Estall, L. B. (1984). Effects of chlordiazepoxide and of valproate on hyponeophagia in rats: Evidence for a mutual antagonism between their anxiolytic properties. Neuropharmacology, 23, 677-681.
47. Shephard, R. A., Jackson, H. F., Broadhurst, P. L, & Deakin, J. F. (1984). Relationships between hyponeophagia, diazepam sensitivity and benzodiazepine receptor binding in eighteen rat genotypes. Pharmacology Biochemistry and Behavior, 20, 845-847.
48. Shepherd, J., Grewal, S. S., Fletcher, A., Bill, D. J., & Dourish, C. T. (1994). Behavioral and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology (Berlin), 116, 56-64.
49. Steele, R. J., & Morris, R. G. M. (1999). Delay-dependent impairment of a matching to place task with chronic and intrahippocampal infusion of the NMDA antagonist D-AP5. Hippocampus, 9, 118-136.
50. Teitelbaum, H., & Milner, P. (1963). Activity changes following partial hippocampal lesions in rats. Journal of Comparative Physiology and Psychology, 56, 284-289.
51. Tonkiss, J., Feldon, J., & Rawlins, J. N. P. (1990). Section of the descending columns of the fornix produces delay- and interference-dependent working memory deficits. Behavioural Brain Research, 36, 113-126.
52. Treit, D., & Menard, J. (1997). Dissociations among the anxiolytic effects of septal, hippocampal and amygdaloid lesions. Behavioral Neuroscience, 111, 653-658.
53. Treit, D., Pesold, C., & Rotzinger, S. (1993). Dissociating the anti-fear effects of septal and amygdala lesions using two pharmacologically validated models of rat anxiety. Behavioral Neuroscience, 107, 770-785.
54. Vann, S. D., Brown, M. W., Erichsen, J. T., & Aggleton, J. P. (2000). Fos imaging reveals differential patterns of hippocampal and parahippocampal subfield activation in rats in response to different spatial memory tests. Journal of Neuroscience, 20, 2711-2718.
55. Whishaw, I. Q., & Mittleman, G. (1991). Hippocampal modulation of nucleus accumbens: Behavioral evidence from amphetamine-induced activity profiles. Behavioral and Neural Biology, 55, 289-306.
56. Wilkinson, L. S., Mittleman, G., Torres, E., Humby, T., Hall, F. S., &Robbins, T. W. (1993). Enhancement of amphetamine-induced locomotor activity and dopamine release in nucleus accumbens following excitotoxic lesions of the hippocampus. Behavioural Brain Research, 55, 143-150.