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Experimental Brain Research

, Volume 224, Issue 2, pp 199–209 | Cite as

Novel odour recognition memory is independent of the hippocampus in rats

  • Gavin A. Scott
  • Mbongeni Mtetwa
  • Hugo Lehmann
Research Article

Abstract

We examined the effects of hippocampal (HPC) damage on odour recognition memory, using a novel odour recognition task that was adapted from the more common novel object recognition task. Three separate experiments were conducted. In Experiment 1, we tested rats in novel odour recognition across different retention intervals (i.e. 15 min, 24 h, 1 week, 5 weeks). Given a single acquisition session, rats’ performance deteriorated after 24 h, but given multiple acquisition sessions (i.e. four sessions over 2 days), rats were able to perform well after retention intervals up to 5 weeks. In Experiment 2, we examined the possible anterograde amnesic effects of HPC damage on novel odour recognition, finding that pre-training damage to the entire HPC failed to cause amnesia for retention delays extending up to 5 weeks. In Experiment 3, we examined whether post-training HPC damage would cause retrograde amnesia, but failed to find any evidence of an impairment. The combined results suggest that the neural network supporting odour recognition is independent of the HPC.

Keywords

Amnesia Lesion Novelty preference Odour Hippocampus Recognition Rat 

Notes

Acknowledgments

We thank NSERC for funding this research as well as Dr. Deborah Saucier in providing useful comments on an earlier draft of this manuscript.

References

  1. Bekinschtein P, Katche C, Slipczuk L et al (2010) Persistence of long-term memory storage: new insights into its molecular signatures in the hippocampus and related structures. Neurotox Res 18:377–385. doi: 10.1007/s12640-010-9155-5 PubMedCrossRefGoogle Scholar
  2. Broadbent NJ, Squire LR, Clark RE (2007) Rats depend on habit memory for discrimination learning and retention. Learn Mem 14:145–151. doi: 10.1101/lm.455607 PubMedCrossRefGoogle Scholar
  3. Broadbent NJ, Gaskin S, Squire LR, Clark RE (2010) Object recognition memory and the rodent hippocampus. Learn Mem 17:794–800. doi: 10.1101/lm.1650110 CrossRefGoogle Scholar
  4. Clark RE, Squire LR (2010) An animal model of recognition memory and medial temporal lobe amnesia: history and current issues. Neuropsychologia 48:2234–2244. doi: 10.1016/j.neuropsychologia.2010.02.004 PubMedCrossRefGoogle Scholar
  5. Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853–8860PubMedGoogle Scholar
  6. Clark RE, West AN, Zola SM, Squire LR (2001) Rats with lesions of the hippocampus are impaired on the delayed nonmatching-to-sample task. Hippocampus 11:176–186PubMedCrossRefGoogle Scholar
  7. Driscoll I, Howard SR, Prusky GT, Rudy JW, Sutherland RJ (2005) Seahorse wins all races: hippocampus participates in both linear and non-linear visual discrimination learning. Behav Brain Res 164:29–35PubMedCrossRefGoogle Scholar
  8. Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav Brain Res 31:47–59PubMedCrossRefGoogle Scholar
  9. Epp J, Keith JR, Spanswick SC, Stone JC, Prusky GT, Sutherland RJ (2008) Retrograde amnesia for visual memories after hippocampal damage in rats. Learn Mem 15:214–221. doi: 10.1101/lm.788008 PubMedCrossRefGoogle Scholar
  10. Feinberg LM, Allen TA, Ly D, Fortin NJ (2012) Recognition memory for social and non-social odors: differential effects of neurotoxic lesions to the hippocampus and perirhinal cortex. Neurobiol Learn Mem 97:7–16. doi: 10.1016/j.nlm.2011.08.008 PubMedCrossRefGoogle Scholar
  11. Frankland PW, Cestari V, Filipkowski RK, McDonald RJ, Silva AJ (1998) The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 112:863–874PubMedCrossRefGoogle Scholar
  12. Gaskin S, Tremblay A, Mumby DG (2003) Retrograde and anterograde object recognition in rats with hippocampal lesions. Hippocampus 13:962–969PubMedCrossRefGoogle Scholar
  13. Glenn MJ, Lehmann H, Mumby DG, Woodside B (2005) Differential fos expression following aspiration, electrolytic, or excitotoxic lesions of the perirhinal cortex in rats. Behav Neurosci 119:806–813PubMedCrossRefGoogle Scholar
  14. Hunsaker MR, Kesner RP (2008) Dissociations across the dorsal-ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fear. Neurobiol Learn Mem 89:61–69. doi: 10.1016/j.nlm.2007.08.016 PubMedCrossRefGoogle Scholar
  15. Hunsaker MR, Fieldsted PM, Rosenberg JS, Kesner RP (2008) Dissociating the roles of dorsal and ventral CA1 for the temporal processing of spatial locations, visual objects, and odors. Behav Neurosci 122:643–650. doi: 10.1037/0735-7044.122.3.643 PubMedCrossRefGoogle Scholar
  16. Lehmann H, Carfagnini A, Yamin S, Mumby DG (2005) Context-dependent effects of hippocampal damage on memory in the shock-probe test. Hippocampus 15:18–25PubMedCrossRefGoogle Scholar
  17. Lehmann H, Lecluse V, Houle A, Mumby DG (2006) Retrograde amnesia following hippocampal lesions in the shock-probe conditioning test. Hippocampus 16:379–387PubMedCrossRefGoogle Scholar
  18. Lehmann H, Glenn MJ, Mumby DG (2007a) Consolidation of object-discrimination memory is independent of the hippocampus in rats. Exp Brain Res 180:755–764PubMedCrossRefGoogle Scholar
  19. Lehmann H, Lacanilao S, Sutherland RJ (2007b) Complete or partial hippocampal damage produces equivalent retrograde amnesia for remote contextual fear memories. Eur J Neurosci 25:1278–1286PubMedCrossRefGoogle Scholar
  20. Lehmann H, Sparks FT, O’Brien J, McDonald RJ, Sutherland RJ (2010) Retrograde amnesia for fear-potentiated startle in rats after complete, but not partial, hippocampal damage. Neuroscience 167:974–984. doi: 10.1016/j.neuroscience.2010.03.005 PubMedCrossRefGoogle Scholar
  21. Mahut H, Zola-Morgan S, Moss M (1982) Hippocampal resections impair associative learning and recognition memory in the monkey. J Neurosci 2:1214–1220PubMedGoogle Scholar
  22. Manns JR, Hopkins RO, Reed JM, Kitchener EG, Squire LR (2003) Recognition memory and the human hippocampus. Neuron 37:171–180PubMedCrossRefGoogle Scholar
  23. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931PubMedCrossRefGoogle Scholar
  24. Maren S (2008) Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. Eur J Neurosci 28:1661–1666. doi: 10.1111/j.1460-9568.2008.06485.x PubMedCrossRefGoogle Scholar
  25. Maren S, Aharonov G, Fanselow MS (1997) Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 88:261–274PubMedCrossRefGoogle Scholar
  26. Martin SJ, de Hoz L, Morris RG (2005) Retrograde amnesia: neither partial nor complete hippocampal lesions in rats result in preferential sparing of remote spatial memory, even after reminding. Neuropsychologia 43:609–624PubMedCrossRefGoogle Scholar
  27. Mouton PR (2002) Principles and practices of unbiased stereology: an introduction for bioscientists. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  28. Mumby DG, Astur RS, Weisend MP, Sutherland RJ (1999) Retrograde amnesia and selective damage to the hippocampal formation: memory for places and object discriminations. Behav Brain Res 106:97–107PubMedCrossRefGoogle Scholar
  29. Mumby DG, Gaskin S, Glenn MJ, Schramek TE, Lehmann H (2002) Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. Learn Mem 9:49–57PubMedCrossRefGoogle Scholar
  30. Mumby DG, Tremblay A, Lecluse V, Lehmann H (2005) Hippocampal damage and anterograde object-recognition in rats after long retention intervals. Hippocampus 15:1050–1056. doi: 10.1002/hipo.20122 PubMedCrossRefGoogle Scholar
  31. Mumby DG, Piterkin P, Lecluse V, Lehmann H (2007) Perirhinal cortex damage and anterograde object-recognition in rats after long retention intervals. Behav Brain Res 185:82–87. doi: 10.1016/j.bbr.2007.07.026 PubMedCrossRefGoogle Scholar
  32. O’Brien N, Lehmann H, Lecluse V, Mumby DG (2006) Enhanced context-dependency of object recognition in rats with hippocampal lesions. Behav Brain Res 170:156–162. doi: 10.1016/j.bbr.2006.02.008 PubMedCrossRefGoogle Scholar
  33. Parsons TC, Otto T (2010) Time-limited involvement of dorsal hippocampus in unimodal discriminative contextual conditioning. Neurobiol Learn Mem 94:481–487. doi: 10.1016/j.nlm.2010.08.015 PubMedCrossRefGoogle Scholar
  34. Reed JM, Squire LR (1997) Impaired recognition memory in patients with lesions limited to the hippocampal formation. Behav Neurosci 111:667–675PubMedCrossRefGoogle Scholar
  35. Rosenbaum RS, Kohler S, Schacter DL et al (2005) The case of K.C.: contributions of a memory-impaired person to memory theory. Neuropsychologia 43:989–1021. doi: 10.1016/j.neuropsychologia.2004.10.007 PubMedCrossRefGoogle Scholar
  36. Rudy JW, Sutherland RJ (1989) The hippocampal formation is necessary for rats to learn and remember configural discriminations. Behav Brain Res 34:97–109PubMedCrossRefGoogle Scholar
  37. Rudy JW, Sutherland RJ (2008) Is it systems or cellular consolidation? Time will tell. An alternative interpretation of the Morris group’s recent science paper. Neurobiol Learn Mem 89:366–369. doi: 10.1016/j.nlm.2007.07.017 PubMedCrossRefGoogle Scholar
  38. Sparks FT, Lehmann H, Sutherland RJ (2011) Between-systems memory interference during retrieval. Eur J Neurosci 34:780–786. doi: 10.1111/j.1460-9568.2011.07796.x PubMedCrossRefGoogle Scholar
  39. Sutherland RJ, Lehmann H (2011) Alternative conceptions of memory consolidation and the role of the hippocampus at the systems level in rodents. Curr Opin Neurobiol 21:446–451. doi: 10.1016/j.conb.2011.04.007 PubMedCrossRefGoogle Scholar
  40. Sutherland RJ, O’Brien J, Lehmann H (2008) Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage. HippocampusGoogle Scholar
  41. Tse D, Langston RF, Kakeyama M et al (2007) Schemas and memory consolidation. Science 316:76–82PubMedCrossRefGoogle Scholar
  42. Wible CG, Shiber JR, Olton DS (1992) Hippocampus, fimbria-fornix, amygdala, and memory: object discriminations in rats. Behav Neurosci 106:751–761PubMedCrossRefGoogle Scholar
  43. Winocur G (1990) Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions. Behav Brain Res 38:145–154PubMedCrossRefGoogle Scholar
  44. Winocur G, McDonald RM, Moscovitch M (2001) Anterograde and retrograde amnesia in rats with large hippocampal lesions. Hippocampus 11:18–26PubMedCrossRefGoogle Scholar
  45. Winters BD, Reid JM (2010) A distributed cortical representation underlies crossmodal object recognition in rats. J Neurosci: Off J Soc Neurosci 30:6253–6261. doi: 10.1523/JNEUROSCI.6073-09.2010 CrossRefGoogle Scholar
  46. Winters BD, Saksida LM, Bussey TJ (2008) Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci Biobehav Rev 32:1055–1070. doi: 10.1016/j.neubiorev.2008.04.004 PubMedCrossRefGoogle Scholar
  47. Winters BD, Saksida LM, Bussey TJ (2010) Implications of animal object memory research for human amnesia. Neuropsychologia 48:2251–2261. doi: 10.1016/j.neuropsychologia.2010.01.023 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Gavin A. Scott
    • 1
  • Mbongeni Mtetwa
    • 1
  • Hugo Lehmann
    • 1
  1. 1.Psychology DepartmentTrent UniversityPeterboroughCanada

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