Long‐term memory underlying hippocampus‐dependent social recognition in mice

The ability to learn and remember individuals is critical for the stability of social groups. Social recognition reflects the ability of mice to identify and remember conspecifics. Social recognition is assessed as a decrease in spontaneous investigation behaviors observed in a mouse reexposed to a familiar conspecific. Our results demonstrate that group‐housed mice show social memory for a familiar juvenile when tested immediately, 30 min, 24 h, 3 days, and 7 days after a single 2‐min‐long interaction. Interestingly, chronic social isolation disrupts long‐term, but not 30‐min, social memory. Even a 24‐h period of isolation disrupts long‐term social memory, a result that may explain why previous investigators only observed short‐term social memory in individually housed rodents. Although it has no obvious configural, relational, or spatial characteristics, here we show that social memory shares characteristics of other hippocampus‐dependent memories. Ibotenic acid lesions of the hippocampus disrupt social recognition at 30 min, but not immediately after training. Furthermore, long‐term, but not short‐term social memory is dependent on protein synthesis and cyclic AMP responsive element binding protein (CREB) function. These results outline behavioral, systems, and molecular determinants of social recognition in mice, and they suggest that it is a powerful paradigm to investigate hippocampal learning and memory. Hippocampus 2000;10:47–56. © 2000 Wiley‐Liss, Inc.

[1]  E. Kandel,et al.  C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia , 1994, Cell.

[2]  T. Tully,et al.  CREB and the formation of long-term memory , 1996, Current Opinion in Neurobiology.

[3]  Alcino J. Silva,et al.  Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein , 1994, Cell.

[4]  R. Dantzer,et al.  Chronic intracerebral infusions of vasopressin and vasopressin antagonist modulate social recognition in rat , 1992, Brain Research.

[5]  F. Bronson,et al.  Life History AND BIOECONOMY OF THE House Mouse , 1992, Biological reviews of the Cambridge Philosophical Society.

[6]  B. J. Morrison Effect of Delay between Group Housing and Testing on Reduction of Emotionality , 1969, Psychological reports.

[7]  J. Oehler,et al.  Dynamic Alterations of Serotonergic Metabolism and Receptors During Social Isolation of Low- and High-Active Mice , 1998, Pharmacology Biochemistry and Behavior.

[8]  J L McGaugh,et al.  Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Dantzer,et al.  Septal vasopressin modulates social memory in male rats , 1988, Brain Research.

[10]  R. Sutherland,et al.  Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia , 1989, Psychobiology.

[11]  J. W. Rudy,et al.  Postconditioning isolation disrupts contextual conditioning: an experimental analysis. , 1996, Behavioral neuroscience.

[12]  Alcino J. Silva,et al.  Spaced training induces normal long-term memory in CREB mutant mice , 1997, Current Biology.

[13]  R. Dantzer,et al.  Social recognition does not involve vasopressinergic neurotransmission in female rats , 1990, Brain Research.

[14]  P. Popik,et al.  RECOGNITION CUE IN THE RAT'S SOCIAL MEMORY PARADIGM , 1991, Journal of basic and clinical physiology and pharmacology.

[15]  J. Koolhaas,et al.  Lateral septal vasopressin in rats: role in social and object recognition? , 1997, Brain Research.

[16]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[17]  J. Matochik Role of the main olfactory system in recognition between individual spiny mice , 1988, Physiology & Behavior.

[18]  D. Dluzen,et al.  The effects of infusion of arginine vasopressin, oxytocin, or their antagonists into the olfactory bulb upon social recognition responses in male rats , 1998, Peptides.

[19]  J. Feldon,et al.  The Disruption of Prepulse Inhibition by Social Isolation in the Wistar Rat: How Robust Is the Effect? , 1998, Pharmacology Biochemistry and Behavior.

[20]  T. W. Greidanus,et al.  The role of limbic vasopressin and oxytocin in social recognition , 1996, Brain Research.

[21]  R. Dantzer,et al.  Androgen-dependent vasopressinergic neurons are involved in social recognition in rats , 1990, Brain Research.

[22]  H. Maaswinkel,et al.  Roles of the basolateral amygdala and hippocampus in social recognition in rats , 1996, Physiology & Behavior.

[23]  J. Koolhaas,et al.  Differential modulation of lateral septal vasopressin receptor blockade in spatial learning, social recognition, and anxiety-related behaviors in rats , 1999, Behavioural Brain Research.

[24]  L. B. Flexner,et al.  Memory in Mice as Affected by Intracerebral Puromycin , 1963, Science.

[25]  D. Blanchard,et al.  Mouse aggression increases after 24 hours of isolation or housing with females. , 1981, Behavioral and neural biology.

[26]  Y. Dudai,et al.  cAMP Response Element-Binding Protein in the Amygdala Is Required for Long- but not Short-Term Conditioned Taste Aversion Memory , 1997, The Journal of Neuroscience.

[27]  M. Debray,et al.  Isolation impairs place preference conditioning to morphine but not aversive learning in mice , 1997, Psychopharmacology.

[28]  L. Valzelli,et al.  Biochemical and behavioural changes induced by isolation in rats. , 1972, Neuropharmacology.

[29]  H. Matthies,et al.  In search of cellular mechanisms of memory , 1989, Progress in Neurobiology.

[30]  P. Luiten,et al.  Vasopressin cells in the medial amygdala of the rat project to the lateral septum and ventral hippocampus , 1987, The Journal of comparative neurology.

[31]  G. Wolterink,et al.  Short duration of retroactive facilitation of social recognition in rats , 1991, Physiology & Behavior.

[32]  R. Dantzer,et al.  Centrally injected arginine vasopressin (AVP) facilitates social memory in rats , 1987, Neuroscience Letters.

[33]  Alcino J. Silva,et al.  CREB and memory. , 1998, Annual review of neuroscience.

[34]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[35]  Prim B. Singh,et al.  MHC antigens in urine as olfactory recognition cues , 1987, Nature.

[36]  H. Eichenbaum Is the rodent hippocampus just for ‘place’? , 1996, Current Opinion in Neurobiology.

[37]  Mary Chen,et al.  Aplysia CREB2 represses long-term facilitation: Relief of repression converts transient facilitation into long-term functional and structural change , 1995, Cell.

[38]  D. Dluzen,et al.  1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) disrupts social memory/recognition processes in the male mouse , 1993, Brain Research.

[39]  R. Dantzer,et al.  Gonadal steroids influence the involvement of arginine vasopressin in social recognition in mice , 1993, Psychoneuroendocrinology.

[40]  J. M. Ree,et al.  Analysis of the influence of vasopressin neuropeptides on social recognition of rats , 1991, European Neuropsychopharmacology.

[41]  G. Winocur Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions , 1990, Behavioural Brain Research.

[42]  W. Quinn,et al.  Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila , 1994, Cell.

[43]  Eric R. Kandel,et al.  Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation , 1990, Nature.

[44]  Nikonov Av The isolation syndrome , 1988 .

[45]  E R Kandel,et al.  Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. , 1998, Learning & memory.

[46]  J. Sinden,et al.  Early rearing environment and dorsal hippocampal ibotenic acid lesions: long-term influences on spatial learning and altenation in the rat , 1989, Behavioural Brain Research.

[47]  R. Landgraf,et al.  Microdialysis administration of vasopressin into the septum improves social recognition in Brattleboro rats , 1994, Physiology & Behavior.

[48]  Wolfgang Schmid,et al.  Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[49]  P. Brain What does individual housing mean to a mouse? , 1975, Life sciences.

[50]  E. Alleva,et al.  A description of the ontogeny of mouse agonistic behavior. , 1998, Journal of comparative psychology.

[51]  Postconditioning isolation disrupts contextual conditioning: an experimental analysis. , 1996, Behavioral neuroscience.

[52]  H Eichenbaum,et al.  Selective damage to the hippocampal region blocks long‐term retention of a natural and nonspatial stimulus‐stimulus association , 1995, Hippocampus.

[53]  Ted Abel,et al.  Positive and negative regulatory mechanisms that mediate long-term memory storage 1 Published on the World Wide Web on 13 January 1998. 1 , 1998, Brain Research Reviews.

[54]  T. F. Sawyer,et al.  Chemosensory and hormonal mediation of social memory in male rats. , 1984, Behavioral neuroscience.

[55]  J. Juraska,et al.  Differential rearing experience, gender, and radial maze performance. , 1984, Developmental psychobiology.

[56]  D. H. Thor,et al.  Social memory of the male laboratory rat. , 1982 .

[57]  G. Beauchamp,et al.  Distinctive urinary odors governed by the major histocompatibility locus of the mouse. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[58]  L. Squire,et al.  Protein synthesis and memory: a review. , 1984, Psychological bulletin.

[59]  S. Corkin Lasting Consequences of Bilateral Medial Temporal Lobectomy: Clinical Course and Experimental Findings in H.M. , 1984 .

[60]  H. Eichenbaum,et al.  Conservation of hippocampal memory function in rats and humans , 1996, Nature.

[61]  W. Potts,et al.  Untrained mice discriminate MHC-determined odors , 1998, Physiology & Behavior.

[62]  S. S. Winans,et al.  The differential projections of the olfactory bulb and accessory olfactory bulb in mammals , 1975, The Journal of comparative neurology.

[63]  David Wood,et al.  Luddites must not block progress in genetics , 1999, Nature.

[64]  N. Ryba,et al.  Molecular aspects of pheromonal communication via the vomeronasal organ of mammals , 1998, Trends in Neurosciences.

[65]  R. Dantzer,et al.  Role of the vomeronasal system in vasopressinergic modulation of social recognition in rats , 1993, Brain Research.

[66]  W. Essman The development of activity differences in isolated and aggregated mice. , 1966, Animal behaviour.