Skip to main content

Recognizing Others: Rodent’s Social Memories

  • Chapter
  • First Online:
Book cover Social Behavior from Rodents to Humans

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 30))

Abstract

We provide in this chapter a brief overview of the present knowledge about social memory in laboratory rodents with a focus on mice and rats. We discuss in the first part the relevance of the processing of olfactory cues for social recognition in these animals and present information about the brain areas involved in the generation of a long-term social memory including cellular mechanisms thought to underlie memory consolidation. In the second part, we suggest that sensory modalities beyond olfaction may also be important in contributing to the long-term social memory trace including audition and taction (and vision). The exposure to stimuli activating the auditory system and taction is able to produce interference phenomena at defined time points during the consolidation of social memory. This ability of such—nonsocial—stimuli may provide a new approach to dissect the brain processes underlying the generation of the social memory trace in further studies.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alkire MT, Gorski LA (2004) Relative amnesic potency of five inhalational anesthetics follows the Meyer–Overton rule. Anesthesiology 101(2):417–429

    Article  CAS  PubMed  Google Scholar 

  • Bannerman DM, Lemaire M, Beggs S, Rawlins JN, Iversen SD (2001) Cytotoxic lesions of the hippocampus increase social investigation but do not impair social-recognition memory. Exp Brain Res 138(1):100–109

    Article  CAS  PubMed  Google Scholar 

  • Boillat M, Challet L, Rossier D, Kan C, Carleton A, Rodriguez I (2015) The vomeronasal system mediates sick conspecific avoidance. Curr Biol 25(2):251–255

    Article  CAS  PubMed  Google Scholar 

  • Borelli KG, Blanchard DC, Javier LK, Defensor EB, Brandao ML, Blanchard RJ (2009) Neural correlates of scent marking behavior in C57BL/6J mice: detection and recognition of a social stimulus. Neuroscience 162(4):914–923

    Article  CAS  PubMed  Google Scholar 

  • Burman OH, Mendl M (2000) Short-term social memory in the laboratory rat: its susceptibility to disturbance. Appl Anim Behav Sci. 67(3):241–254

    Article  CAS  PubMed  Google Scholar 

  • Burman OH, Mendl M (2002) Recognition of conspecific odors by laboratory rats (Rattus norvegicus) does not show context specificity. J Comp Psychol 116(3):247–252

    Article  PubMed  Google Scholar 

  • Burman O, Mendl M (2006) Long-term social memory in the laboratory rat (Rattus norvegicus) Anim Welf 15(4):379–382

    Google Scholar 

  • Carter CS, DeVries AC, Getz LL (1995) Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 19(2):303–314

    Article  CAS  PubMed  Google Scholar 

  • Curtis JT, Liu Y, Wang Z (2001) Lesions of the vomeronasal organ disrupt mating-induced pair bonding in female prairie voles (Microtus ochrogaster). Brain Res 901(1–2):167–174

    Article  CAS  PubMed  Google Scholar 

  • Dantzer R, Bluthe RM, Koob GF, Le Moal M (1987) Modulation of social memory in male rats by neurohypophyseal peptides. Psychopharmacology 91(3):363–368

    Article  CAS  PubMed  Google Scholar 

  • Dutton RC, Maurer AJ, Sonner JM, Fanselow MS, Laster MJ, Eger EI 2nd (2001) The concentration of isoflurane required to suppress learning depends on the type of learning. Anesthesiology 94(3):514–519

    Article  CAS  PubMed  Google Scholar 

  • Eibl-Eibesfeldt I (1950) Beiträge zur Biologie der Haus—und Ährenmaus nebst einigen Beobachtungen an anderen Nagern. Z Tierpsychol 7:558–587

    Article  Google Scholar 

  • Eibl-Eibesfeldt I (1952) Ethologische Unterschiede zwischen Hausratte und Wanderratte. Verh Deutsch Zool Ges Freiburg, pp 169–180

    Google Scholar 

  • Engelmann M (2009) Competition between two memory traces for long-term recognition memory. Neurobiol Learn Mem 91(1):58–65

    Article  PubMed  Google Scholar 

  • Engelmann M, Wotjak CT, Landgraf R (1995) Social discrimination procedure: an alternative method to investigate juvenile recognition abilities in rats. Physiol Behav 58(2):315–321

    Article  CAS  PubMed  Google Scholar 

  • Engelmann M, Ebner K, Wotjak CT, Landgraf R (1998) Endogenous oxytocin is involved in short-term olfactory memory in female rats. Behav Brain Res 90(1):89–94

    Article  CAS  PubMed  Google Scholar 

  • Engelmann M, Hadicke J, Noack J (2011) Testing declarative memory in laboratory rats and mice using the nonconditioned social discrimination procedure. Nat Protoc 6(8):1152–1162

    Article  CAS  PubMed  Google Scholar 

  • 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(1):7–16

    Article  CAS  PubMed  Google Scholar 

  • Ferguson JN, Aldag JM, Insel TR, Young LJ (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21(20):8278–8285

    CAS  PubMed  Google Scholar 

  • Ferguson JN, Young LJ, Insel TR (2002) The neuroendocrine basis of social recognition. Front Neuroendocrinol 23(2):200–224

    Article  CAS  PubMed  Google Scholar 

  • Fidalgo AR, Cibelli M, White JP, Nagy I, Wan Y, Ma D (2012) Isoflurane causes neocortical but not hippocampal-dependent memory impairment in mice. Acta Anaesthesiol Scand 56(8):1052–1057

    Article  CAS  PubMed  Google Scholar 

  • Hammock EA (2015) Developmental perspectives on oxytocin and vasopressin. Neuropsychopharmacology 40(1):24–42

    Article  CAS  PubMed  Google Scholar 

  • Haseneder R, Kratzer S, von Meyer L, Eder M, Kochs E, Rammes G (2009) Isoflurane and sevoflurane dose-dependently impair hippocampal long-term potentiation. Eur J Pharmacol 623(1–3):47–51

    Article  CAS  PubMed  Google Scholar 

  • Heiss E, Natchev N, Rabanser A, Weisgram J, Hilgers H (2009) Three types of cutaneous glands in the skin of the salamandrid Pleurodeles waltl. A histological and ultrastructural study. J Morphol 270(7):892–902

    Article  PubMed  Google Scholar 

  • Hitti FL, Siegelbaum SA (2014) The hippocampal CA2 region is essential for social memory. Nature 508(7494):88–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isles AR, Baum MJ, Ma D, Keverne EB, Allen ND (2001) Urinary odour preferences in mice. Nature 409(6822):783–784

    Article  CAS  PubMed  Google Scholar 

  • Kaut KP, Bunsey MD (2001) The effects of lesions to the rat hippocampus or rhinal cortex on olfactory and spatial memory: retrograde and anterograde findings. Cogn Affect Behav Neurosci 1(3):270–286

    Article  CAS  PubMed  Google Scholar 

  • Kogan JH, Frankland PW, Silva AJ (2000) Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10(1):47–56

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Marcos A (2009) On the organization of olfactory and vomeronasal cortices. Prog Neurobiol 87(1):21–30

    Article  PubMed  Google Scholar 

  • Mendl M (1999) Performing under pressure: stress and cognitive function. Appl Anim Behav Sci 65(3):221–244

    Article  Google Scholar 

  • Meredith M, Westberry JM (2004) Distinctive responses in the medial amygdala to same-species and different-species pheromones. J Neurosci 24(25):5719–5725

    Article  CAS  PubMed  Google Scholar 

  • Moles A, Costantini F, Garbugino L, Zanettini C, D’Amato FR (2007) Ultrasonic vocalizations emitted during dyadic interactions in female mice: a possible index of sociability? Behav Brain Res 182(2):223–230

    Article  PubMed  Google Scholar 

  • Moura PJ, Meirelles ST, Xavier GF (2010) Long-term social recognition memory in adult male rats: factor analysis of the social and non-social behaviors. Braz J Med Biol Res 43(7):663–676

    Article  CAS  PubMed  Google Scholar 

  • Moura PJ, Venkitaramani DV, Tashev R, Lombroso PJ, Xavier GF (2011) Transport of animals between rooms: a little-noted aspect of laboratory procedure that may interfere with memory. Behav Process 88(1):12–19

    Article  Google Scholar 

  • Natynczuk SE, Macdonald DW (1994) Scent, sex, and the self-calibrating rat. J Chem Ecol 20(8):1843–1857

    Article  CAS  PubMed  Google Scholar 

  • Neumann ID, Landgraf R (2012) Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci 35(11):649–659

    Article  CAS  PubMed  Google Scholar 

  • Noack J, Richter K, Laube G, Haghgoo HA, Veh RW, Engelmann M (2010) Different importance of the volatile and non-volatile fractions of an olfactory signature for individual social recognition in rats versus mice and short-term versus long-term memory. Neurobiol Learn Mem 94(4):568–575

    Article  CAS  PubMed  Google Scholar 

  • Noack J, Murau R, Engelmann M (2015) Consequences of temporary inhibition of the medial amygdala on social recognition memory performance in mice. Front Neurosci 9:152

    PubMed  PubMed Central  Google Scholar 

  • Pena RR, Pereira-Caixeta AR, Moraes MF, Pereira GS (2014) Anisomycin administered in the olfactory bulb and dorsal hippocampus impaired social recognition memory consolidation in different time-points. Brain Res Bull 109:151–157

    Article  CAS  PubMed  Google Scholar 

  • Perna JC, Wotjak CT, Stork O, Engelmann M (2015) Timing of presentation and nature of stimuli determine retroactive interference with social recognition memory in mice. Physiol Behav 143:10–14

    Article  CAS  PubMed  Google Scholar 

  • Petrulis A, Eichenbaum H (2003) The perirhinal-entorhinal cortex, but not the hippocampus, is critical for expression of individual recognition in the context of the Coolidge effect. Neuroscience 122(3):599–607

    Article  CAS  PubMed  Google Scholar 

  • Petrulis A, Alvarez P, Eichenbaum H (2005) Neural correlates of social odor recognition and the representation of individual distinctive social odors within entorhinal cortex and ventral subiculum. Neuroscience 130(1):259–274

    Article  CAS  PubMed  Google Scholar 

  • Popik P, Vetulani J, Bisaga A, van Ree JM (1991) Recognition cue in the rat’s social memory paradigm. J Basic Clin Physiol Pharmacol 2(4):315–327

    Article  CAS  PubMed  Google Scholar 

  • Richter K, Wolf G, Engelmann M (2005a) Social recognition memory requires two stages of protein synthesis in mice. Learn Mem 12(4):407–413

    Article  PubMed  PubMed Central  Google Scholar 

  • Richter K, Wolf G, Engelmann M (2005b) Social recognition memory requires two stages of protein synthesis in mice. Learn Memory. 12(4):407–413

    Article  Google Scholar 

  • Samuelsen CL, Meredith M (2011) Oxytocin antagonist disrupts male mouse medial amygdala response to chemical-communication signals. Neuroscience 180:96–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawyer TF, Hengehold AK, Perez WA (1984) Chemosensory and hormonal mediation of social memory in male rats. Behav Neurosci 98(5):908–913

    Article  CAS  PubMed  Google Scholar 

  • Sekiguchi R, Wolterink G, van Ree JM (1991) Short duration of retroactive facilitation of social recognition in rats. Physiol Behav 50(6):1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Shahar-Gold H, Gur R, Wagner S (2013) Rapid and reversible impairments of short- and long-term social recognition memory are caused by acute isolation of adult rats via distinct mechanisms. PLoS ONE 8(5):e65085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squires AS, Peddle R, Milway SJ, Harley CW (2006) Cytotoxic lesions of the hippocampus do not impair social recognition memory in socially housed rats. Neurobiol Learn Mem 85(1):95–101

    Article  PubMed  Google Scholar 

  • Stranahan AM, Khalil D, Gould E (2006) Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 9(4):526–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thor DH, Holloway WR (1982) Social memory of the male laboratory rat. J Comp Physiol Psychol 96(6):1000–1006

    Article  Google Scholar 

  • Uekita T, Okanoya K (2011) Hippocampus lesions induced deficits in social and spatial recognition in Octodon degus. Behav Brain Res 219(2):302–309

    Article  PubMed  Google Scholar 

  • van der Kooij MA, Sandi C (2012) Social memories in rodents: methods, mechanisms and modulation by stress. Neurosci Biobehav Rev 36(7):1763–1772

    Article  PubMed  Google Scholar 

  • Wacker DW, Ludwig M (2012) Vasopressin, oxytocin, and social odor recognition. Horm Behav 61(3):259–265

    Article  CAS  PubMed  Google Scholar 

  • Wanisch K, Wotjak CT, Engelmann M (2008) Long-lasting second stage of recognition memory consolidation in mice. Behav Brain Res 186(2):191–196

    Article  PubMed  Google Scholar 

  • Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33(3):161–253

    Google Scholar 

  • Zhao X, Sun L, Jia H, Meng Q, Wu S, Li N et al (2009) Isolation rearing induces social and emotional function abnormalities and alters glutamate and neurodevelopment-related gene expression in rats. Prog Neuropsychopharmacol Biol Psychiatry 33(7):1173–1177

    Article  CAS  PubMed  Google Scholar 

  • Zheng DJ, Foley L, Rehman A, Ophir AG (2013) Social recognition is context dependent in single male prairie voles. Anim Behav 86(5):1085–1095

    Google Scholar 

Download references

Acknowledgments

We thank Rita Murau for expert technical assistance. J.C.P was supported by stipends from the Leibniz Graduate School and the Medical Faculty Otto-von-Guericke-Universität Magdeburg.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Judith Camats Perna .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Camats Perna, J., Engelmann, M. (2015). Recognizing Others: Rodent’s Social Memories. In: Wöhr, M., Krach, S. (eds) Social Behavior from Rodents to Humans. Current Topics in Behavioral Neurosciences, vol 30. Springer, Cham. https://doi.org/10.1007/7854_2015_413

Download citation

Publish with us

Policies and ethics