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Assessing recent and remote associative olfactory memory in rats using the social transmission of food preference paradigm

Nature Protocols volume 12, pages 1415–1436 (2017)Cite this article

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Abstract

Rats have the ability to learn about potential food sources by sampling their odors on the breath of conspecifics. Although this ethologically based social behavior has been transposed to the laboratory to probe nonspatial associative olfactory memory, only a few studies have taken full advantage of its unique features to examine the organization of recently and remotely acquired information. We provide a set of standardized procedures and technical refinements that are particularly useful in achieving this goal while minimizing confounding factors. These procedures, built upon a three-stage protocol (odor exposure, social interaction and preference test), are designed to optimize performance across variable retention delays, thus enabling the reliable assessment of recent and remote memory, and underlying processes, including encoding, consolidation, retrieval and forgetting. The different variants of the social transmission of food preference paradigm, which take a few days to several weeks to perform, make it an attractive and versatile tool that can be coupled to many applications in CNS research. The paradigm can be easily implemented in a typical rodent facility by personnel with standard animal behavioral expertise.

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Figure 1: The social transmission of food preference procedure relies on three main stages.
Figure 2: Equipment required for the protocol.
Figure 3
Figure 4: Schematic diagram illustrating key parameters and experimental designs that can be used with the STFP procedure.
Figure 5: Automated recording and scoring of the behavior of one demonstrator–observer dyad during the social interaction phase.
Figure 6: Typical results showing associative olfactory memory performance of experimental (EXP) and food preference (FP) control Sprague–Dawley rats as measured in the STFP procedure.
Figure 7: The associative nature of the STFP procedure makes memory long-lasting.
Figure 8: Persistence of associative olfactory memory is dependent on initial memory strength.

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References

  1. Galef, B.G. & Wigmore, S.W. Transfer of information concerning distant foods: a laboratory investigation of the 'information-centre' hypothesis. Anim. Behav. 31, 748–758 (1983).

    Article  Google Scholar 

  2. Posadas-Andrews, A. & Roper, T.J. Social transmission of food-preferences in adult rats. Anim. Behav. 31, 265–271 (1983).

    Article  Google Scholar 

  3. Strupp, B.J. & Levitsky, D.E. Social transmission of food preferences in adult hooded rats (Rattus norvegicus). J. Comp. Psychol. 98, 257–266 (1984).

    Article  Google Scholar 

  4. Galef, B.G. A case study in behavioral analysis, synthesis and attention to detail: social learning of food preferences. Behav. Brain Res. 231, 266–271 (2012).

    Article  PubMed  Google Scholar 

  5. Galef, B.G. et al. Familiarity and relatedness: effects on social learning about foods by Norway rats and Mongolian gerbils. Anim. Learn. Behav. 26, 448–454 (1998).

    Article  Google Scholar 

  6. Valsecchi, P. & Galef, B.G. Social influences on the food preferences of house mice (Mus Musculus). Inter. J. Comp. Psychol. 2, 245–256 (1989).

    Google Scholar 

  7. Clark, R.E., Broadbent, N.J., Zola, S.M. & Squire, L.R. Anterograde amnesia and temporally graded retrograde amnesia for a nonspatial memory task after lesions of hippocampus and subiculum. J. Neurosci. 22, 4663–4669 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ross, R.S. & Eichenbaum, H. Dynamics of hippocampal and cortical activation during consolidation of a nonspatial memory. J. Neurosci. 26, 4852–4859 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Winocur, G., Moscovitch, M. & Sekeres, M. Memory consolidation or transformation: context manipulation and hippocampal representations of memory. Nat. Neurosci. 10, 555–557 (2007).

    Article  CAS  PubMed  Google Scholar 

  10. Galef, B.G. Jr. & Whiskin, E.E. Socially transmitted food preferences can be used to study long-term memory in rats. Learn. Behav. 31, 160–164 (2003).

    Article  PubMed  Google Scholar 

  11. Lesburguères, E. et al. Early tagging of cortical networks is required for the formation of enduring associative memory. Science 331, 924–928 (2011).

    Article  PubMed  CAS  Google Scholar 

  12. Gerlai, R. Behavioral tests of hippocampal function: simple paradigms complex problems. Behav. Brain Res. 125, 269–277 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Cohen, S.J. & Stackman, R.W. Jr. Assessing rodent hippocampal involvement in the novel object recognition task. A review. Behav. Brain Res. 285, 105–117 (2015).

    Article  PubMed  Google Scholar 

  14. Morellini, F. Spatial memory tasks in rodents: what do they model? Cell Tissue Res. 354, 273–286 (2013).

    Article  PubMed  Google Scholar 

  15. Alvarez, P., Lipton, P.A., Melrose, R. & Eichenbaum, H. Differential effects of damage within the hippocampal region on memory for a natural, nonspatial odor-odor association. Learn. Mem. 8, 79–86 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Alvarez, P., Wendelken, L. & Eichenbaum, H. Hippocampal formation lesions impair performance in an odor-odor association task independently of spatial context. Neurobiol. Learn. Mem. 78, 470–476 (2002).

    Article  PubMed  Google Scholar 

  17. Eichenbaum, H. & Fortin, N.J. The neurobiology of memory based predictions. Philos Trans. R. Soc. Lond. B. Biol. Sci. 364, 1183–1191 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Bunsey, M. & Eichenbaum, H. Selective damage to the hippocampal region blocks long-term retention of a natural and nonspatial stimulus-stimulus association. Hippocampus 5, 546–556 (1995).

    Article  CAS  PubMed  Google Scholar 

  19. Winocur, G. Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions. Behav. Brain Res. 38, 145–154 (1990).

    Article  CAS  PubMed  Google Scholar 

  20. Frankland, P.W. & Bontempi, B. The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119–130 (2005).

    Article  CAS  PubMed  Google Scholar 

  21. Maren, S., Phan, K.L. & Liberzon, I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 14, 417–428 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Brightwell, J.J., Smith, C.A., Countryman, R.A., Neve, R.L. & Colombo, P.J. Hippocampal overexpression of mutant creb blocks long-term, but not short-term memory for a socially transmitted food preference. Learn. Mem. 12, 12–17 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Dudai, Y. The restless engram: consolidations never end. Annu. Rev. Neurosci. 35, 227–247 (2012).

    Article  CAS  PubMed  Google Scholar 

  24. Squire, L.R. & Bayley, P.J. The neuroscience of remote memory. Curr. Opin. Neurobiol. 17, 185–196 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Wang, S.H. & Morris, R.G. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu. Rev. Psychol. 61, 49–79 (2010).

    Article  PubMed  Google Scholar 

  26. Wiltgen, B.J. & Tanaka, K.Z. Systems consolidation and the content of memory. Neurobiol. Learn. Mem. 106, 365–371 (2013).

    Article  PubMed  Google Scholar 

  27. Galef, B.G. Jr. & Clark, M.M. Mother's milk and adult presence: two factors determining initial dietary selection by weanling rats. J. Comp. Physiol. Psychol. 78, 220–225 (1972).

    Article  PubMed  Google Scholar 

  28. Heiderstadt, K.M., McLaughlin, R.M., Wright, D.C., Walker, S.E. & Gomez-Sanchez, C.E. The effect of chronic food and water restriction on open-field behaviour and serum corticosterone levels in rats. Lab. Anim. 34, 20–28 (2000).

    Article  CAS  PubMed  Google Scholar 

  29. Toth, L.A. & Gardiner, T.W. Food and water restriction protocols: physiological and behavioral considerations. Contemp. Top. Lab. Anim. Sci. 39, 9–17 (2000).

    CAS  PubMed  Google Scholar 

  30. Johansson, A. et al. The relative impact of chronic food restriction and acute food deprivation on plasma hormone levels and hypothalamic neuropeptide expression. Peptides 29, 1588–1595 (2008).

    Article  CAS  PubMed  Google Scholar 

  31. Pesic, V. et al. Changes of behavioral parameters during long-term food restriction in middle-aged Wistar rats. Physiol. Behav. 101, 672–678 (2010).

    Article  CAS  PubMed  Google Scholar 

  32. Alvarenga, T.A., Andersen, M.L., Papale, L.A., Antunes, I.B. & Tufik, S. Influence of long-term food restriction on sleep pattern in male rats. Brain Res. 1057, 49–56 (2005).

    Article  CAS  PubMed  Google Scholar 

  33. Roky, R., Kapas, L., Taishi, T.P., Fang, J. & Krueger, J.M. Food restriction alters the diurnal distribution of sleep in rats. Physiol. Behav. 67, 697–703 (1999).

    Article  CAS  PubMed  Google Scholar 

  34. Deacon, R.M. Housing, husbandry and handling of rodents for behavioral experiments. Nat. Protoc. 1, 936–946 (2006).

    Article  PubMed  Google Scholar 

  35. Prager, E.M., Bergstrom, H.C., Grunberg, N.E. & Johnson, L.R. The importance of reporting housing and husbandry in rat research. Front. Behav. Neurosci. 5, 38 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kilkenny, C., Browne, W.J., Cuthill, I.C., Emerson, M. & Altman, D.G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. J. Pharmacol. Pharmacother. 1, 94–99 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Gritton, H.J., Kantorowski, A., Sarter, M. & Lee, T.M. Bidirectional interactions between circadian entrainment and cognitive performance. Learn. Mem. 19, 126–141 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Galef, B.G. & Whiskin, E.E. Social transmission of information about multiflavored foods. Anim. Learn. Behav. 20, 56–62 (1992).

    Article  Google Scholar 

  39. Galef, B.G. Jr., Mason, J.R., Preti, G. & Bean, N.J. Carbon disulfide: a semiochemical mediating socially-induced diet choice in rats. Physiol. Behav. 42, 119–124 (1988).

    Article  CAS  PubMed  Google Scholar 

  40. Witt, R.M., Galligan, M.M., Despinoy, J.R. & Segal, R. Olfactory behavioral testing in the adult mouse. J. Vis. Exp. 23, 949 (2009).

    Google Scholar 

  41. Shors, T.J. Learning during stressful times. Learn. Mem. 11, 137–144 (2004).

    Article  PubMed  Google Scholar 

  42. van Ruiven, R. et al. The influence of transportation stress on selected nutritional parameters to establish the necessary minimum period for adaptation in rat feeding studies. Lab. Anim. 32, 446–456 (1998).

    Article  CAS  PubMed  Google Scholar 

  43. Hall, F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit. Rev. Neurobiol. 12, 129–162 (1998).

    Article  CAS  PubMed  Google Scholar 

  44. Maier, J.X., Blankenship, M.L., Barry, N.C., Richards, S.E. & Katz, D.B. Stability and flexibility of the message carried by semiochemical stimuli, as revealed by devaluation of carbon disulfide followed by social transmission of food preference. Behav. Neurosci. 128, 413–418 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Wrenn, C.C. Social transmission of food preference in mice. Curr. Protoc. Neurosci. Chapter 8, Unit 8.5G (2004).

  46. Wrenn, C.C., Harris, A.P., Saavedra, M.C. & Crawley, J.N. Social transmission of food preference in mice: methodology and application to galanin-overexpressing transgenic mice. Behav. Neurosci. 117, 21–31 (2003).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank A. Hambucken for comments on the manuscript. This work was supported by the Fondation pour la Recherche Médicale ((FRM) grant DEQ20130326468 to B. Bontempi), by a LabEx BRAIN ((Bordeaux Region Aquitaine Initiative for Neuroscience) PhD extension grant to B. Bessières), by the Agence Nationale pour la Recherche (grant ANR-14-CE13-0017-01, project MemoryTrack, to B. Bontempi) and by funding from the Fondation France Alzheimer, Fondation de France and CNRS (UMR 5293).

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Authors and Affiliations

  1. Institut des Maladies Neurodégénératives,

    Benjamin Bessières, Olivier Nicole & Bruno Bontempi

  2. CNRS, Bordeaux, France

    Benjamin Bessières, Olivier Nicole & Bruno Bontempi

  3. Institut des Maladies Neurodégénératives,

    Benjamin Bessières, Olivier Nicole & Bruno Bontempi

  4. Université de Bordeaux, Bordeaux, France

    Benjamin Bessières, Olivier Nicole & Bruno Bontempi

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  1. Benjamin Bessières
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Contributions

B. Bontempi designed the general STFP procedure for measuring recent and remote memory. B. Bessières and O. Nicole designed the automated procedure for recording social interaction. B. Bessières, B. Bontempi and O. Nicole. performed the experiments and analyzed the data conjointly. B. Bontempi wrote the manuscript with input from B. Bessières and O. Nicole.

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Correspondence to Bruno Bontempi.

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Bessières, B., Nicole, O. & Bontempi, B. Assessing recent and remote associative olfactory memory in rats using the social transmission of food preference paradigm. Nat Protoc 12, 1415–1436 (2017). https://doi.org/10.1038/nprot.2017.050

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