Cholinergic modulation of a decrement in social investigation following repeated contacts between mice
Abstract
Social recognition has been inferred from a decline in olfactory investigation of conspecific intruders during repeated or protracted confrontation with a resident rat. A stimulus-response relationship defined by lack of response remains somewhat ambiguous. Since it is likely that behavior continues to be emitted by the resident animal, how behavior reorganizes as the resident becomes familiar with an intruder represents an important issue in the characterization of recognition. We examined the decline in olfactory investigation of ovariectomized females by adult male mice. The duration and frequency of olfactory investigation was measured during four 1 minute confrontations with 10-min intertrial intervals (Training trials). If the same female was presented in each trial, investigation declined to less than 50% of initial levels. Aggressive behavior gradually increased with repeated trials. No decline in investigation or increased aggression was measured when females were changed in each trial. Administration of doses of scopolamine (0.16-1.0 mg/kg, IP) blocked decrements in olfactory investigation in repeated confrontations and significantly reduced aggression. Co-administration of heptylphysostigmine (0.32-5.0 mg/kg, IP) reversed scopolamine's effects on olfactory investigation but not aggression. Acetylcholinesterase inhibitors heptylphysostigmine, galanthamine (0.63-2.5 mg/kg, IP) and tacrine (0.63-10.0 mg/kg, IP) all enhanced the rate of decrement of olfactory investiga…
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Observations of mice in these settings have shown that exposure to an unfamiliar stranger typically evokes a period of intense social sniffing, which may be followed by escalating aggressive responses or sexual behavior, dependent upon such factors as age and sex of the unfamiliar conspecific.
“Observations of mice in these settings have shown that exposure to an unfamiliar stranger typically evokes a period of intense social sniffing, which may be followed by escalating aggressive responses or sexual behavior, dependent upon such factors as age and sex of the unfamiliar conspecific (Bluthe et al. 1993;Kogan et al. 2000;Winslow & Camacho 1995).”
From Sociability and preference for social novelty in five inbred strains: an approach to assess autistic‐like behavior in mice (2004) · cites this paper as Winslow & Camacho 1995
Cholinergic signaling in the amygdala is necessary for social recognition, social memory formation, social stress responsivity, and fear learning.
“Cholinergic signaling in the amygdala is necessary for social recognition [56], social memory formation [57,58], social stress responsivity [59] and fear learning [60].”
Cites
Statistical principles in experimental design.
Winer, B. J. (1962) · McGraw-Hill Book Company · doi:10.1037/11774-000 · Cited by 27,137 · see citing works
(1982) · Trends in Neurosciences · doi:10.1016/0166-2236(82)90076-5 · Cited by 9,148 · see citing works
Statistical Principles in Experimental Design
Myers, J. L., & Winer, B. J. (1964) · The American Journal of Psychology · doi:10.2307/1419292 · Cited by 8,111 · see citing works
Statistical Principles in Experimental Design
Green, P. E., Winer, B. J., Brown, D. R., & Michels, K. M. (1992) · Journal of Marketing Research · doi:10.2307/3172747 · Cited by 4,333 · see citing works
Habituation: a model phenomenon for the study of neuronal substrates of behavior
Thompson, R. F., & Spencer, W. A. (1966) · Psychological Review · doi:10.1037/h0022681 · Cited by 2,608 · cited 1× · see citing works
“Taken together these data meet several important criteria for habituation (Thompson and Spencer 1966; Kandel et al. 1991).”
BackgroundA role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · cited 1× · see citing works
“Duration and frequency of social and non-social behaviors were recorded on an IBM PC using an exhaustive, mutually exclusive scoring strategy (Winslow et al. 1993), Olfactory investigatory behaviors included anogenital sniffing, body and tail sniffing, and head sni~ng.”
MethodSelf-citationCholinergic mechanisms in learning, memory and dementia: a review of recent evidence
Fibiger, H. C. (1991) · Trends in Neurosciences · doi:10.1016/0166-2236(91)90117-d · Cited by 599 · see citing works
Hasselmo, M. E., & Bower, J. M. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90159-j · Cited by 429 · see citing works
Social memory of the male laboratory rat.
Thor, D. H., & Holloway, W. R. (1982) · Journal of Comparative and Physiological Psychology · doi:10.1037/0735-7036.96.6.1000 · Cited by 375 · see citing works
Ethology and pharmacology of hypothalamic aggression in the rat
Kruk, M. R. (1991) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80144-7 · Cited by 166 · see citing works
Androgen-dependent vasopressinergic neurons are involved in social recognition in rats
Bluthe, R.-M., Schoenen, J., & Dantzer, R. (1990) · Brain Research · doi:10.1016/0006-8993(90)90073-k · Cited by 164 · see citing works
Scopolamine injection into the olfactory bulb impairs short-term olfactory memory in rats.
Ravel, N., Elaagouby, A., & Gervais, R. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.2.317 · Cited by 119 · see citing works
Popik, P., & van Ree, J. M. (1991) · European Neuropsychopharmacology · doi:10.1016/0924-977x(91)90010-r · Cited by 114 · see citing works
Perio, A., Terranova, J.-P., Worms, P., Bluthé, R.-M., Dantzer, R., & Bizière, K. (1989) · Psychopharmacology · doi:10.1007/bf00442261 · Cited by 111 · see citing works
Pharmacokinetics of galanthamine in humans and corresponding cholinesterase inhibition
Bickel, U., Thomsen, T., Weber, W., Fischer, J. P., Bachus, R., Nitz, M., & Kewitz, H. (1991) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.1991.159 · Cited by 94 · see citing works
Neurohypophyseal hormone receptors in the septum are implicated in social recognition in the rat
Popik, P., Vos, P. E., & Van Ree, J. M. (1992) · Behavioural Pharmacology · doi:10.1097/00008877-199208000-00011 · Cited by 93 · see citing works
Role of the vomeronasal system in vasopressinergic modulation of social recognition in rats
Bluthé, R.-M., & Dantzer, R. (1993) · Brain Research · doi:10.1016/0006-8993(93)90370-3 · Cited by 85 · see citing works
Toide, K., & Arima, T. (1989) · European Journal of Pharmacology · doi:10.1016/0014-2999(89)90510-4 · Cited by 74 · see citing works
Beninger, R. J., Jhamandas, K. H., Boegman, R. J., & El-Defrawy, S. R. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90195-4 · Cited by 74 · see citing works
Cholinesterase inhibitor effects on extracellular acetylcholine in rat striatum
Messamore, E. (1993) · Neuropharmacology · doi:10.1016/0028-3908(93)90114-i · Cited by 72 · see citing works
Cholinergic mechanisms in a simple test of olfactory learning in the rat
Hunter, A. J., & Murray, T. K. (1989) · Psychopharmacology · doi:10.1007/bf00442821 · Cited by 68 · see citing works
Differential effects of scopolamine and mecamylamine on working and reference memory in the rat
Moran, P. M. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90502-k · Cited by 67 · see citing works
Scopolamine impairs delayed matching in an olfactory task in rats
Ravel, N., Vigouroux, M., Elaagouby, A., & Gervais, R. (1992) · Psychopharmacology · doi:10.1007/bf02247720 · Cited by 66 · see citing works
Evidence for an endogenous cholecystokininergic balance in social memory
Lemaire, M., Piot, O., Roques, B. P., Böhme, G. A., & Blanchard, J. (1992) · Neuroreport · doi:10.1097/00001756-199210000-00028 · Cited by 65 · see citing works
Dluzen, D. E., & Kreutzberg, J. D. (1993) · Brain Research · doi:10.1016/0006-8993(93)90860-p · Cited by 63 · see citing works
Drug Effects on Attack, Defense and Escape in Mice
Kršiak, M., Šulcová, A., Tomašiková, Z., Dlohožková, N., Kosar, E., & Mašek, K. (1981) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(81)80010-x · Cited by 59 · see citing works
(1975) · Springer eBooks · doi:10.1007/978-1-4684-2634-2 · Cited by 54 · see citing works
Cerebral lateralization of olfactory-mediated affective processes in rats
Dantzer, R., Tazi, A., & Bluthé, R.-M. (1990) · Behavioural Brain Research · doi:10.1016/0166-4328(90)90042-d · Cited by 52 · see citing works
Bluthé, R.-M., & Dantzer, R. (1992) · Brain Research · doi:10.1016/0006-8993(92)90480-w · Cited by 47 · see citing works
Ethological study of the effects of tetrahydroaminoacridine (THA) on social recognition in rats
Gheusi, G., Bluthé, R.-M., Goodall, G., & Dantzer, R. (1994) · Psychopharmacology · doi:10.1007/bf02244996 · Cited by 38 · see citing works
The Second Generation of Cholinesterase Inhibitors: Pharmacological Aspects
Giacobini, E. (1991) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4899-6738-1_29 · Cited by 37 · see citing works
Cholinomimetic activities of minaprine
Worms, P., Kan, J. P., Steinberg, R., Terranova, J.-P., Perio, A., & Bizière, K. (1989) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00167042 · Cited by 35 · see citing works
Messamore, E., Berglund, U. W., Williams, E., & Giacobini, E. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90265-m · Cited by 29 · see citing works
Poirier, M. F., Löo, H., Dennis, T., Fur, G. L., & Scatton, B. (2009) · Neuropsychobiology · doi:10.1159/000118222 · Cited by 27 · see citing works
Factors that modulate inescapable shock-induced reductions in daily activity in the rat
Woodmansee, W. W., Silbert, L. H., & Maier, S. F. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90505-n · Cited by 26 · see citing works
The Mammalian Vomeronasal System: Its Role in Learning and Social Behaviors
Wysocki, C. J., Bean, N. J., & Beauchamp, G. K. (1986) · Springer eBooks · doi:10.1007/978-1-4613-2235-1_36 · Cited by 24 · see citing works
Age-related scopolamine effects on social and individual behaviour in rats
Soffi�, M., & Bronchart, M. (1988) · Psychopharmacology · doi:10.1007/bf00181945 · Cited by 24 · see citing works
Seoane, J. R., & Baile, C. A. (1973) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(73)90054-3 · Cited by 18 · see citing works
Retz, K. C., Forster, M. J., Frantz, N. Z., & Lal, H. (1987) · Neuropharmacology · doi:10.1016/0028-3908(87)90025-6 · Cited by 17 · see citing works
Drug effects in a radical maze designed for dissociation of cues used by mice
Beuzen, A., Belzung, C., & Roullet, P. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90492-8 · Cited by 14 · see citing works
Drugs as Research Tools in Psychology: Cholinergic Drugs and Aggression
Bell, R., Warburton, D. M., & Brown, K. (2009) · Neuropsychobiology · doi:10.1159/000118225 · Cited by 12 · see citing works
The effects of anticholinergics on the behavior of the rat in a solitary and in a social situation.
van der Poel, A. M., & Remmelts, M. (1971) · PubMed · Cited by 11 · see citing works
Physostigmine effects on activity and reactions to novelty
Hughes, R. N., & Trowland, R. (1976) · Life Sciences · doi:10.1016/0024-3205(76)90305-2 · Cited by 8 · see citing works
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Moy, S. S., Nadler, J. J., Perez, A., Barbaro, R. P., Johns, J. M., Magnuson, T. R., Piven, J., & Crawley, J. N. (2004) · Genes, Brain and Behavior · doi:10.1111/j.1601-1848.2004.00076.x · Cited by 1,545 · see citing works
Social amnesia in mice lacking the oxytocin gene
Ferguson, J. N., Young, L. J., Hearn, E. F., Matzuk, M. M., Insel, T. R., & Winslow, J. T. (2000) · Nature Genetics · doi:10.1038/77040 · Cited by 1,130 · see citing works
Self-citationOxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043 · see citing works
Oxytocin: The Great Facilitator of Life
Lee, H.-J., Macbeth, A. H., Pagani, J., & Young, W. S. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.04.001 · Cited by 1,037 · see citing works
Klinkenberg, I., & Blokland, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.04.001 · Cited by 714 · see citing works
HOW THE BRAIN PROCESSES SOCIAL INFORMATION: Searching for the Social Brain
Insel, T. R., & Fernald, R. D. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144148 · Cited by 556 · see citing works
Ohno, M., Sametsky, E. A., Younkin, L. H., Oakley, H., Younkin, S. G., Citron, M., Vassar, R., & Disterhoft, J. F. (2004) · Neuron · doi:10.1016/s0896-6273(03)00810-9 · Cited by 549 · see citing works
Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice
Anagnostaras, S., Murphy, G. G., Hamilton, S. E., Mitchell, S. L., Rahnama, N. P., Nathanson, N. M., & Silva, A. J. (2002) · Nature Neuroscience · doi:10.1038/nn992 · Cited by 543 · see citing works
Vasopressin: Behavioral roles of an “original” neuropeptide
Caldwell, H. K., Lee, H.-J., Macbeth, A. H., & Young, W. S. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.10.007 · Cited by 504 · see citing works
The neuroendocrine basis of social recognition
Ferguson, J. N., Young, L. J., & Insel, T. R. (2002) · Frontiers in Neuroendocrinology · doi:10.1006/frne.2002.0229 · Cited by 494 · see citing works
The social deficits of the oxytocin knockout mouse
Winslow, J. T., & Insel, T. R. (2002) · Neuropeptides · doi:10.1054/npep.2002.0909 · Cited by 307 · see citing works
Self-citationThe histamine H3receptor: an attractive target for the treatment of cognitive disorders
Esbenshade, T. A., Browman, K. E., Bitner, R. S., Strakhova, M. I., Cowart, M. D., & Brioni, J. D. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.147 · Cited by 302 · see citing works
Young, J. W., Powell, S. B., Risbrough, V. B., Marston, H. M., & Geyer, M. A. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.004 · Cited by 299 · see citing works
Fox, G. B., Esbenshade, T. A., Pan, J. B., Radek, R. J., Krueger, K. M., Yao, B. B., Browman, K. E., Buckley, M. J., Ballard, M. E., Komater, V. A., et al. (2005) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.104.078402 · Cited by 260 · see citing works
Prado, V. F., Martins-Silva, C., de Castro, B. M., Lima, R. F., Barros, D. M., Amaral, E., Ramsey, A. J., Sotnikova, T. D., Ramirez, M. R., Kim, H.-G., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.005 · Cited by 246 · see citing works
Scent marking behavior as an odorant communication in mice
Arakawa, H., Blanchard, D. C., Arakawa, K., Dunlap, C., & Blanchard, R. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.05.012 · Cited by 229 · see citing works
The oxytocin system in drug discovery for autism: Animal models and novel therapeutic strategies
Modi, M. E., & Young, L. J. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.010 · Cited by 218 · see citing works
Behavioral models of odor similarity.
Cleland, T. A., Morse, A., Yue, E. L., & Linster, C. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.2.222 · Cited by 208 · see citing works
Neuroendocrine basis of social recognition
Winslow, J. T., & Insel, T. R. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.009 · Cited by 180 · see citing works
Self-citationThe potential role of dopamine D3 receptor neurotransmission in cognition
Nakajima, S., Gerretsen, P., Takeuchi, H., Caravaggio, F., Chow, T. W., Foll, B. L., Mulsant, B. H., Pollock, B. G., & Graff‐Guerrero, A. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.05.006 · Cited by 179 · see citing works
Bariselli, S., Hörnberg, H., Prévost-Solié, C., Musardo, S., Hatstatt-Burklé, L., Scheiffele, P., & Bellone, C. (2018) · Nature Communications · doi:10.1038/s41467-018-05382-3 · Cited by 171 · see citing works
The main olfactory system and social learning in mammals
Sánchez-Andrade, G., & Kendrick, K. M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.021 · Cited by 166 · see citing works
AR-R 17779 improves social recognition in rats by activation of nicotinic α7 receptors
van Kampen, M., Selbach, K., Schneider, R., Schiegel, E., Boess, F., & Schreiber, R. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1668-7 · Cited by 160 · see citing works
The neural circuits of mating and fighting in male mice
Hashikawa, K., Hashikawa, Y., Falkner, A. L., & Lin, D. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.01.006 · Cited by 157 · see citing works
Arakawa, H., Cruz, S., & Deak, T. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.03.007 · Cited by 131 · see citing works
Millan, M. J., Cara, B. D., Dekeyne, A., Panayi, F., de Groote, L., Sicard, D., Cistarelli, L., Billiras, R., & Gobert, A. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04262.x · Cited by 125 · see citing works
Neural Encoding of Olfactory Recognition Memory
Sánchez-Andrade, G., James, B. M., & Kendrick, K. M. (2005) · Journal of Reproduction and Development · doi:10.1262/jrd.17031 · Cited by 120 · see citing works
Involvement of the cholinergic system in conditioning and perceptual memory
Robinson, L., Platt, B., & Riedel, G. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.01.055 · Cited by 115 · see citing works
Mouse Social Recognition and Preference
Winslow, J. T. (2003) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0816s22 · Cited by 113 · see citing works
Self-citationD’Adamo, P. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.21.2567 · Cited by 109 · see citing works
Neural correlates of olfactory learning: Critical role of centrifugal neuromodulationPreprint
Fletcher, M. L., & Chen, W. R. (2010) · Learning & Memory · doi:10.1101/lm.941510 · Cited by 106 · see citing works
Loiseau, F., Dekeyne, A., & Millan, M. J. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0934-5 · Cited by 105 · see citing works
Animal models of dementia and cognitive dysfunction
Neha, N., Sodhi, R. K., Jaggi, A. S., & Singh, N. (2014) · Life Sciences · doi:10.1016/j.lfs.2014.05.017 · Cited by 100 · see citing works
Todeschin, A. S., Duarte, E. C. W., Jacob, M., Aranda, B. C. C., Jacobs, S., Fernandes, M. D. C., Ribeiro, M. F. M., Sanvitto, G. L., & Lucion, A. B. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.03.006 · Cited by 99 · see citing works
Scopolamine-induced deficits in social memory in mice: Reversal by donepezil
Riedel, G., Kang, S. H., Choi, D.-Y., & Platt, B. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.06.012 · Cited by 97 · see citing works
Millan, M. J. (2010) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2010.06.002 · Cited by 91 · see citing works
Ultrasonic vocalizations as an index of social memory in female mice.
D'Amato, F. R., & Moles, A. (2001) · Behavioral Neuroscience · doi:10.1037//0735-7044.115.4.834 · Cited by 91 · see citing works
Biophysical alterations of hippocampal pyramidal neurons in learning, ageing and Alzheimer's disease
Disterhoft, J. F., Wu, W., & Ohno, M. (2004) · Ageing Research Reviews · doi:10.1016/j.arr.2004.07.001 · Cited by 88 · see citing works
Models of Neurodevelopmental Abnormalities in Schizophrenia
Powell, S. B. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_57 · Cited by 84 · see citing works
de Souza, M. A., Centenaro, L. A., Menegotto, P. R., Henriques, T. P., Bonini, J. S., Achaval, M., & Lucion, A. B. (2013) · Neurochemical Research · doi:10.1007/s11064-013-1049-5 · Cited by 83 · see citing works
Arakawa, H., Arakawa, K., Blanchard, D. C., & Blanchard, R. J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.009 · Cited by 80 · see citing works
Tang, A. C., Reeb, B. C., Romeo, R. D., & McEwen, B. S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08254.2003 · Cited by 78 · see citing works
Tang, A. C., Nakazawa, M., Romeo, R. D., Reeb, B. C., Sisti, H., & McEwen, B. S. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.10.010 · Cited by 78 · see citing works
Li, X., Bao, X., & Wang, R. (2015) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2015.2428 · Cited by 76 · see citing works
Arakawa, H., Blandino, P., & Deak, T. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.04.024 · Cited by 75 · see citing works
Loiseau, F., & Millan, M. J. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.07.012 · Cited by 69 · see citing works
Role of centrifugal projections to the olfactory bulb in olfactory processingPreprint
Kiselycznyk, C., Zhang, S., & Linster, C. (2006) · Learning & Memory · doi:10.1101/lm.285706 · Cited by 67 · see citing works
Wöhr, M., & Schwarting, R. K. W. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.05.004 · Cited by 65 · see citing works
Nakamura, K. T., & Kurasawa, M. (2001) · European Journal of Pharmacology · doi:10.1016/s0014-2999(01)01005-6 · Cited by 65 · see citing works
Physostigmine Enhances Performance on an Odor Mixture Discrimination Test
Doty, R. L., Bagla, R., & Kim, N. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00238-8 · Cited by 64 · see citing works
Cara, B. D., Panayi, F., Gobert, A., Dekeyne, A., Sicard, D., de Groote, L., & Millan, M. J. (2006) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145706007103 · Cited by 62 · see citing works
Cohen, O., Erb, C., Ginzberg, D., Pollak, Y., Seidman, S., Shoham, S., Yirmiya, R., & Soreq, H. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001103 · Cited by 61 · see citing works
Psychotropic and neurotropic activity
Vogel, H. G., & Vogel, W. H. (1997) · Springer eBooks · doi:10.1007/978-3-662-03333-3_5 · Cited by 60 · see citing works
Light phase testing of social behaviors: not a problem
Yang, M. (2008) · Frontiers in Neuroscience · doi:10.3389/neuro.01.029.2008 · Cited by 59 · see citing works
Vale-Martı́nez, A., Baxter, M. G., & Eichenbaum, H. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02153.x · Cited by 58 · see citing works
Exposure to extremely low-frequency electromagnetic fields improves social recognition in male rats
García, M. A. V., Elı́as-Viñas, D., Reyes-Guerrero, G., Domínguez-González, A. D., Verdugo‐Díaz, L., & Guevara‐Guzmán, R. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.06.004 · Cited by 56 · see citing works
Differential Muscarinic Modulation in the Olfactory Bulb
Smith, R. S., Hu, R., DeSouza, A., Eberly, C. L., Krahe, K., Chan, W., & Araneda, R. C. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0099-15.2015 · Cited by 50 · see citing works
Esbenshade, T. A., Browman, K. E., Miller, T. R., Krueger, K. M., Komater, V. A., Zhang, M., Fox, G. B., Rueter, L. E., Robb, H. M., Radek, R. J., et al. (2012) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.194126 · Cited by 50 · see citing works
Modulation of adenosine signaling prevents scopolamine-induced cognitive impairment in zebrafish
Bortolotto, J. W., de Melo, G. M., Cognato, G. D. P., Vianna, M. R. M. R., & Bonan, C. D. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.11.016 · Cited by 50 · see citing works
Macbeth, A. H., Edds, J. S., & Young, W. S. (2009) · Nature Protocols · doi:10.1038/nprot.2009.141 · Cited by 46 · see citing works
Eptastigmine: Ten Years of Pharmacology, Toxicology, Pharmacokinetic, and Clinical Studies
Braida, D., & Sala, M. (2001) · CNS Drug Reviews · doi:10.1111/j.1527-3458.2001.tb00205.x · Cited by 42 · see citing works
Jacobs, S., & Tsien, J. Z. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036387 · Cited by 40 · see citing works
Almeida‐Santos, A. F., Carvalho, V. R., Jaimes, L. F., de Castro, C. M., Pinto, H. P. P., Oliveira, T. P. D., Vieira, L. B., Moraes, M. F. D., & Pereira, G. S. (2019) · Scientific Reports · doi:10.1038/s41598-018-36871-6 · Cited by 38 · see citing works
Peleh, T., Ike, K. G. O., Wams, E. J., Lebois, E. P., & Hengerer, B. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.018 · Cited by 37 · see citing works
A prefrontal-thalamic circuit encodes social information for social recognition
Chen, Z., Han, Y., Ma, Z., Wang, X., Xu, S., Tang, Y. Y., Vyssotski, A. L., Si, B., & Zhan, Y. (2024) · Nature Communications · doi:10.1038/s41467-024-45376-y · Cited by 35 · see citing works
Overview of Animal Models of Schizophrenia
Powell, S. B., & Geyer, M. A. (2007) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0924s39 · Cited by 35 · see citing works
Weil, Z. M., Bowers, S., Pyter, L. M., & Nelson, R. J. (2005) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2005.05.001 · Cited by 35 · see citing works
Smith, C. P., Bores, G. M., Petko, W. W., Li, M., Selk, D. E., Rush, D. K., Camacho, F., Winslow, J. T., Fishkin, R. J., Cunningham, D., et al. (1997) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)36441-9 · Cited by 35 · see citing works
Self-citationComputerized assessment of social approach behavior in mouse
Page, D. T. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.048.2009 · Cited by 32 · see citing works
Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs
Lévy, F., Richard, P., Meurisse, M., & Ravel, N. (1997) · Psychopharmacology · doi:10.1007/s002130050166 · Cited by 31 · see citing works
Social recognition in paired, but not single, male prairie voles
Blocker, T. D., & Ophir, A. G. (2015) · Animal Behaviour · doi:10.1016/j.anbehav.2015.07.003 · Cited by 30 · see citing works
Garbugino, L., Centofante, E., & D'Amato, F. R. (2016) · Neural Plasticity · doi:10.1155/2016/5346161 · Cited by 28 · see citing works
Social recognition is context dependent in single male prairie voles
Zheng, D., Foley, L., Rehman, A., & Ophir, A. G. (2013) · Animal Behaviour · doi:10.1016/j.anbehav.2013.09.015 · Cited by 28 · see citing works
Millan, M. J., Gobert, A., Panayi, F., Rivet, J., Dekeyne, A., Brocco, M., Ortuno, J., & Cara, B. D. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708008894 · Cited by 28 · see citing works
Jacobs, S., & Tsien, J. Z. (2014) · Genes Brain & Behavior · doi:10.1111/gbb.12123 · Cited by 26 · see citing works
Social Reward and Empathy as Proximal Contributions to Altruism: The Camaraderie Effect
Lahvis, G. P. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_449 · Cited by 26 · see citing works
Adult forebrain NMDA receptors gate social motivation and social memory
Jacobs, S., & Tsien, J. Z. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.019 · Cited by 26 · see citing works
Extensive immunolesions of basal forebrain cholinergic system impair offspring recognition in sheep
Ferreira, G., Meurisse, M., Gervais, R., Ravel, N., & Lévy, F. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00265-2 · Cited by 26 · see citing works
Progesterone impairs social recognition in male rats
Bychowski, M. E., & Auger, C. J. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.02.009 · Cited by 25 · see citing works
“[PubMed: 12399951] Winslow JT, Camacho F. Cholinergic modulation of a decrement in social investigation following repeated contacts between mice.”
MethodInfluentialPehrson, A. L., Hillhouse, T. M., Haddjeri, N., Rovera, R., Porter, J. H., Mørk, A., Smagin, G. N., Song, D., Budac, D. P., Cajina, M., et al. (2016) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.116.233924 · Cited by 24 · see citing works
Lewin, A. H., Szewczyk, J. R., Wilson, J. W., & Carroll, F. I. (2005) · Tetrahedron · doi:10.1016/j.tet.2005.05.055 · Cited by 24 · see citing works
Effects of Three Lipidated Oxytocin Analogs on Behavioral Deficits in CD38 Knockout Mice
Михайлович, Ч. С., Akther, S., Nishimura, T., Shabalova, A. A., Mizuno, A., Ichinose, W., Shuto, S., Yamamoto, Y., Yokoyama, S., & Higashida, H. (2017) · Brain Sciences · doi:10.3390/brainsci7100132 · Cited by 23 · see citing works
Cholinergic transmission from the basal forebrain modulates social memory in male mice
Kljakic, O., Al‐Onaizi, M., Janíčková, H., Chen, K. S., Guzman, M. S., Prado, M. A. M., & Prado, V. F. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15400 · Cited by 22 · see citing works
Carrillo, M., Ricci, L. A., & Melloni, R. H. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.056 · Cited by 22 · see citing works
Importance of the GluN2B carboxy-terminal domain for enhancement of social memories
Jacobs, S., Wei, W., Wang, D., & Tsien, J. Z. (2015) · Learning & Memory · doi:10.1101/lm.038521.115 · Cited by 22 · see citing works
Camargo, L. C., Campos, G. A. A., Galante, P., Biolchi, A. M., Gonçalves, J. C., Lopes, K. S., & Mortari, M. R. (2017) · Neuropeptides · doi:10.1016/j.npep.2017.11.010 · Cited by 21 · see citing works
Environmental enrichment alleviates cognitive and behavioral impairments in EL mice
Suemaru, K., Yoshikawa, M., Aso, H., & Watanabe, M. (2018) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2018.06.016 · Cited by 21 · see citing works
Okada, K., Nishizawa, K., Kobayashi, T., Sakata, S., Hashimoto, K., & Kobayashi, K. (2021) · Scientific Reports · doi:10.1038/s41598-021-93045-7 · Cited by 21 · see citing works
Psychotropic and Neurotropic Activity
Vogel, H. G. (2007) · Springer eBooks · doi:10.1007/978-3-540-70995-4_6 · Cited by 20 · see citing works
Shang, Y., & Dluzen, D. E. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00120-8 · Cited by 20 · see citing works
Violent phenotype in SAL mice is inflexible and fixed in adulthood
Natarajan, D., VRIES, H. D., de Boer, S. F., & Koolhaas, J. M. (2009) · Aggressive Behavior · doi:10.1002/ab.20312 · Cited by 19 · see citing works
Martin, L. A., Iceberg, E., & Allaf, G. (2017) · Brain and Behavior · doi:10.1002/brb3.895 · Cited by 19 · see citing works
Morè, L., Lauterborn, J. C., Papaleo, F., & Brambilla, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.02.003 · Cited by 19 · see citing works
Zou, H., Xie, Q., Zhang, M., Zhang, C., Zhao, G., Jin, M., & Yu, L. (2009) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2009.04.021 · Cited by 19 · see citing works
A novel DSC approach for evaluating protectant drugs efficacy against dementia
Abarova, S., Koynova, R. D., Tancheva, L. P., & Tenchov, B. G. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.07.033 · Cited by 19 · see citing works
Low-temperature exothermic transitions in brain proteome of mice, effect of scopolamine
Tenchov, B. G., Abarova, S., Koynova, R. D., Traikov, L. L., & Tancheva, L. P. (2017) · Thermochimica Acta · doi:10.1016/j.tca.2017.01.012 · Cited by 18 · see citing works
Ferreira, G., Gervais, R., Durkin, T., & Lévy, F. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.1.136 · Cited by 18 · see citing works
A new approach for investigating neurodegenerative disorders in mice based on DSC
Tenchov, B. G., Abarova, S., Koynova, R. D., Traikov, L. L., Dragomanova, S., & Tancheva, L. P. (2016) · Journal of Thermal Analysis and Calorimetry · doi:10.1007/s10973-016-5749-3 · Cited by 17 · see citing works
Asymmetrical distributions of muscarinic receptor binding in the hippocampus of female rats
Wolff, S. C., Hruska, Z., Nguyen, L., & Dohanich, G. P. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.04.002 · Cited by 15 · see citing works
Social Recognition Memory Test in Rodents
Jacobs, S., Huang, F., Tsien, J. Z., & Wei, W. (2016) · BIO-PROTOCOL · doi:10.21769/bioprotoc.1804 · Cited by 14 · see citing works
- Authors
- Winslow, J. T., & Camacho, F.
- ORCID
- Camacho, F.
- Venue
- Psychopharmacology
- Published
- 1995-09
- Volume
- 121
- Issue
- 2
- Pages
- 164-172
- ISSN
- 0033-3158 (ISSN-L)
- 1432-2072
- OpenAlex
- W2045405667
- Cited by
- 156
- References
- 43
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 3 · 2023: 7 · 2022: 2 · 2021: 3 · 2020: 4 · 2019: 6 · 2018: 4 · 2017: 9 · 2016: 8 · 2015: 9 · 2014: 3 · 2013: 4 · 2012: 5
- FWCI
- 1.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Psychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- social recognition, habituation, cholinergic modulation, acetylcholine, scopolamine, galantamine, tacrine, acetylcholinesterase inhibitors, aggression, olfactory memory, male-female interaction
- MeSH terms
- Aggression, Animals, Behavior, Animal, Female, Interpersonal Relations, Male, Memory, Mice, Inbred Strains, Ovariectomy, Scopolamine, Smell, Tacrine, Mice
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