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Mammalian social memory relies on neuromodulation in the olfactory bulb

  • Hajime Suyama

    Hajime Suyama is a postdoctoral fellow in Prof. Veronica Egger’s lab in Regensburg. He is interested in vasopressinergic actions in the rat olfactory bulb in the context of social memory. During his research, he carries out in vitro patch-clamp recordings and Ca2+ imaging as well as in vivo behavioral analysis and immunohistochemical assays of neural activation. He joined the lab of Prof. Dr. Veronica Egger as a Ph.D. student and finished his doctoral study in 2021 under the supervision of Dr. Michael Lukas at the University of Regensburg, after he finished his veterinary medicine (D.V.M.) study in 2017 at the Azabu University in Japan.

     ORCID logo     , Veronica Egger

    Toward the end of her studies of physics at TU Munich, Veronica Egger was enthralled by the neurosciences. After obtaining her Ph.D. thesis on the representation of whiskers in the rodent somatosensory cortex in Heidelberg (with Bert Sakmann, 1999), she started to work on synaptic processing in the olfactory bulb, with a focus on the reciprocal synapse between mitral cells and granule cells, as a postdoc at the Cold Spring Harbor Laboratory (with Zach Mainen and Karel Svoboda). In 2011, she became a junior research group leader (BMBF), and in 2013, she was appointed full professor at Regensburg University. By now, her lab could achieve experimental proof of the concept of the reciprocal spine operating as a “mini-neuron”.

     ORCID logo     and Michael Lukas

    Michael Lukas is a senior postdoc in Professor Veronica Egger’s lab in Regensburg. He is interested in the actions of social neuropeptides like vasopressin and oxytocin on neuronal networks involved in social communication, including olfaction. During his research, he carries out in vitro patch-clamp recordings and Ca2+ imaging as well as in vivo behavioral analysis and immunohistochemical assays of neural activation. He performed his Ph.D. thesis in the behavioral pharmacology lab of Prof. Inga Neumann, investigating the effects of vasopressin and oxytocin on social memory and anxiety, and finishing in 2011. He graduated as a biologist from the University of Regensburg in 2008.

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Published/Copyright: June 21, 2022
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Neuroforum
From the journal Neuroforum Volume 28 Issue 3

Abstract

In this review, we aim to integrate our recent findings on the vasopressin system and its role in social discrimination with other known neuromodulatory mechanisms in the olfactory bulb that are involved in different experimental models of social memory. Behavioral paradigms commonly used to investigate odor-related social memory are individual social memory in rodents, lamb recognition in sheep, and the Bruce effect in female mice. All three cases involve neuromodulation in the main and/or the accessory olfactory bulb, the first centers for olfactory processing. As a large diversity of neuromodulators participate in social memory formation, here, we focus primarily on shared neuromodulatory systems and their physiological effects, in particular, the social neuropeptides, vasopressin and oxytocin, and the arousal-related modulators, acetylcholine and noradrenaline.

Zusammenfassung

In dieser Übersicht wollen wir unsere Erkenntnisse zum Vasopressin-System und seine Rolle bei der sozialen Diskriminierung mit anderen neuromodulatorischen Mechanismen im Bulbus olfaktorius verbinden, die an verschiedenen experimentellen Modellen des sozialen Gedächtnisses beteiligt sind. Paradigmen für geruchsbezogenes soziales Gedächtnis sind die soziale Diskriminierung bei Nagern, die Lammerkennung bei Schafen und der Bruce-Effekt bei weiblichen Mäusen. In allen drei Fällen ist eine Neuromodulation im Haupt- und/oder im akzessorischen Bulbus olfaktorius beteiligt. Da viele verschiedene Neuromodulatoren an der Bildung des sozialen Gedächtnisses beteiligt sind, konzentrieren wir uns hier auf gemeinsame neuromodulatorische Systeme, wie die sozialen Neuropeptide Vasopressin, Oxytocin und die erregungsabhängigen Modulatoren Acetylcholin und Noradrenalin.

Keywords: bruce effect; noradrenaline; olfactory bulb; social memory; vasopressin
Schlüsselwörter: Vasopressin; Soziales Gedächtnis; Bruce Effekt; Olfaktorischer Bulbus; Noradrenalin
Corresponding author: Michael Lukas, Neurophysiology, Institute of Zoology, University of Regensburg, Regensburg, Germany, E-mail:

About the authors

Hajime Suyama

Hajime Suyama is a postdoctoral fellow in Prof. Veronica Egger’s lab in Regensburg. He is interested in vasopressinergic actions in the rat olfactory bulb in the context of social memory. During his research, he carries out in vitro patch-clamp recordings and Ca2+ imaging as well as in vivo behavioral analysis and immunohistochemical assays of neural activation. He joined the lab of Prof. Dr. Veronica Egger as a Ph.D. student and finished his doctoral study in 2021 under the supervision of Dr. Michael Lukas at the University of Regensburg, after he finished his veterinary medicine (D.V.M.) study in 2017 at the Azabu University in Japan.

Veronica Egger

Toward the end of her studies of physics at TU Munich, Veronica Egger was enthralled by the neurosciences. After obtaining her Ph.D. thesis on the representation of whiskers in the rodent somatosensory cortex in Heidelberg (with Bert Sakmann, 1999), she started to work on synaptic processing in the olfactory bulb, with a focus on the reciprocal synapse between mitral cells and granule cells, as a postdoc at the Cold Spring Harbor Laboratory (with Zach Mainen and Karel Svoboda). In 2011, she became a junior research group leader (BMBF), and in 2013, she was appointed full professor at Regensburg University. By now, her lab could achieve experimental proof of the concept of the reciprocal spine operating as a “mini-neuron”.

Michael Lukas

Michael Lukas is a senior postdoc in Professor Veronica Egger’s lab in Regensburg. He is interested in the actions of social neuropeptides like vasopressin and oxytocin on neuronal networks involved in social communication, including olfaction. During his research, he carries out in vitro patch-clamp recordings and Ca2+ imaging as well as in vivo behavioral analysis and immunohistochemical assays of neural activation. He performed his Ph.D. thesis in the behavioral pharmacology lab of Prof. Inga Neumann, investigating the effects of vasopressin and oxytocin on social memory and anxiety, and finishing in 2011. He graduated as a biologist from the University of Regensburg in 2008.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: The work was supported by the German research foundation (DFG LU2164/1-1 and EG 135/5-1).

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Abraham, N.M., Egger, V., Shimshek, D.R., Renden, R., Fukunaga, I., Sprengel, R., Seeburg, P.H., Klugmann, M., Margrie, T.W., Schaefer, A.T., et al.. (2010). Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 65, 399–411, https://doi.org/10.1016/j.neuron.2010.01.009.Search in Google Scholar

Binns, K.E. and Brennan, P.A. (2005). Changes in electrophysiological activity in the accessory olfactory bulb and medial amygdala associated with mate recognition in mice. Eur. J. Neurosci. 21, 2529–2537, https://doi.org/10.1111/j.1460-9568.2005.04090.x.Search in Google Scholar

Brennan, P.A., Kendrick, K.M., and Keverne, E.B. (1995). Neurotransmitter release in the accessory olfactory bulb during and after the formation of an olfactory memory in mice. Neuroscience 69, 1075–1086, https://doi.org/10.1016/0306-4522(95)00309-7.Search in Google Scholar

Breton-Provencher, V., Drummond, G.T., and Sur, M. (2021). Locus coeruleus norepinephrine in learned behavior: Anatomical modularity and spatiotemporal integration in targets. Front. Neural Circ. 15, 638007, https://doi.org/10.3389/fncir.2021.638007.Search in Google Scholar

Bruce, H.M. (1959). An exteroceptive block to pregnancy in the mouse. Nature 184, 105, https://doi.org/10.1038/184105a0.Search in Google Scholar

Brunert, D. and Rothermel, M. (2021). Extrinsic neuromodulation in the rodent olfactory bulb. Cell Tissue Res. 383, 507–524, https://doi.org/10.1007/s00441-020-03365-9.Search in Google Scholar

Dantzer, R., Bluthe, R.M., Koob, G.F., and Le Moal, M. (1987). Modulation of social memory in male rats by neurohypophyseal peptides. Psychopharmacology (Berl.) 91, 363–368, https://doi.org/10.1007/bf00518192.Search in Google Scholar

Dantzer, R., Koob, G.F., Bluthe, R.M., and Le Moal, M. (1988). Septal vasopressin modulates social memory in male rats. Brain Res. 457, 143–147, https://doi.org/10.1016/0006-8993(88)90066-2.Search in Google Scholar

Dantzer, R., Tazi, A., and Bluthe, R.M. (1990). Cerebral lateralization of olfactory-mediated affective processes in rats. Behav. Brain Res. 40, 53–60, https://doi.org/10.1016/0166-4328(90)90042-d.Search in Google Scholar

Devore, S. and Linster, C. (2012). Noradrenergic and cholinergic modulation of olfactory bulb sensory processing. Front. Behav. Neurosci. 6, 52, https://doi.org/10.3389/fnbeh.2012.00052.Search in Google Scholar PubMed PubMed Central

Dluzen, D.E., Muraoka, S., Engelmann, M., Ebner, K., and Landgraf, R. (2000). Oxytocin induces preservation of social recognition in male rats by activating alpha-adrenoceptors of the olfactory bulb. Eur. J. Neurosci. 12, 760–766, https://doi.org/10.1046/j.1460-9568.2000.00952.x.Search in Google Scholar

Dluzen, D.E., Muraoka, S., Engelmann, M., and Landgraf, R. (1998a). The effects of infusion of arginine vasopressin, oxytocin, or their antagonists into the olfactory bulb upon social recognition responses in male rats. Peptides 19, 999–1005, https://doi.org/10.1016/s0196-9781(98)00047-3.Search in Google Scholar

Dluzen, D.E., Muraoka, S., and Landgraf, R. (1998b). Olfactory bulb norepinephrine depletion abolishes vasopressin and oxytocin preservation of social recognition responses in rats. Neurosci. Lett. 254, 161–164, https://doi.org/10.1016/s0304-3940(98)00691-0.Search in Google Scholar

Endevelt-Shapira, Y., Perl, O., Ravia, A., Amir, D., Eisen, A., Bezalel, V., Rozenkrantz, L., Mishor, E., Pinchover, L., Soroka, T., et al.. (2018). Altered responses to social chemosignals in autism spectrum disorder. Nat. Neurosci. 21, 111–119, https://doi.org/10.1038/s41593-017-0024-x.Search in Google Scholar

Engelmann, M., Hadicke, J., and Noack, J. (2011). Testing declarative memory in laboratory rats and mice using the nonconditioned social discrimination procedure. Nat. Protoc. 6, 1152–1162, https://doi.org/10.1038/nprot.2011.353.Search in Google Scholar

Engelmann, M., Wotjak, C.T., and Landgraf, R. (1995). Social discrimination procedure: An alternative method to investigate juvenile recognition abilities in rats. Physiol. Behav. 58, 315–321, https://doi.org/10.1016/0031-9384(95)00053-l.Search in Google Scholar

Fang, L.Y., Quan, R.D., and Kaba, H. (2008). Oxytocin facilitates the induction of long-term potentiation in the accessory olfactory bulb. Neurosci. Lett. 438, 133–137, https://doi.org/10.1016/j.neulet.2007.12.070.Search in Google Scholar PubMed

Gielow, M.R., and Zaborszky, L. (2017). The input-output relationship of the cholinergic basal forebrain. Cell Rep. 18, 1817–1830, https://doi.org/10.1016/j.celrep.2017.01.060.Search in Google Scholar PubMed PubMed Central

Goodson, J.L. (2005). The vertebrate social behavior network: Evolutionary themes and variations. Horm. Behav. 48, 11–22, https://doi.org/10.1016/j.yhbeh.2005.02.003.Search in Google Scholar PubMed PubMed Central

Halász, N. (1990). The Vertebrate Olfactory System: Chemical Neuroanatomy, Function and Development (Budapest: Akadémiai Kiadó).Search in Google Scholar

Hansen, N. (2017). The longevity of hippocampus-dependent memory is orchestrated by the locus coeruleus-noradrenergic system. Neural Plast. 2017, 2727602, https://doi.org/10.1155/2017/2727602.Search in Google Scholar PubMed PubMed Central

Haskal de la Zerda, S., Netser, S., Magalnik, H., Briller, M., Marzan, D., Glatt, S., Abergel, Y., and Wagner, S. (2020). Social recognition in rats and mice requires integration of olfactory, somatosensory and auditory cues. Available at SSRN: https://ssrn.com/abstract=3838994 or https://doi.org/10.2139/ssrn.3838994.Search in Google Scholar

Huang, G.Z., Taniguchi, M., Zhou, Y.B., Zhang, J.J., Okutani, F., Murata, Y., Yamaguchi, M., and Kaba, H. (2018). Alpha2-adrenergic receptor activation promotes long-term potentiation at excitatory synapses in the mouse accessory olfactory bulb. Learn. Mem. 25, 147–157, https://doi.org/10.1101/lm.046391.117.Search in Google Scholar

Kaba, H. (2010). Neurobiology of mammalian olfactory learning that occurs during sensitive periods. Curr. Zool. 56, 819–833, https://doi.org/10.1093/czoolo/56.6.819.Search in Google Scholar

Kaba, H. and Keverne, E.B. (1988). The effect of microinfusions of drugs into the accessory olfactory-bulb on the olfactory block to pregnancy. Neuroscience 25, 1007–1011, https://doi.org/10.1016/0306-4522(88)90053-x.Search in Google Scholar

Kendrick, K., Lévy, F., and Keverne, E.B. (1992). Changes in the sensory processing of olfactory signals induced by birth in sleep. Science 256, 833–836, https://doi.org/10.1126/science.1589766.Search in Google Scholar

Kendrick, K.M., Da Costa, A.P., Broad, K.D., Ohkura, S., Guevara, R., Levy, F., and Keverne, E.B. (1997a). Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res. Bull. 44, 383–395, https://doi.org/10.1016/s0361-9230(97)00218-9.Search in Google Scholar

Kendrick, K.M., Guevara-Guzman, R., Zorrilla, J., Hinton, M.R., Broad, K.D., Mimmack, M., and Ohkura, S. (1997b). Formation of olfactory memories mediated by nitric oxide. Nature 388, 670–674, https://doi.org/10.1038/41765.Search in Google Scholar

Kendrick, K.M., Keverne, E.B., Chapman, C., and Baldwin, B.A. (1988). Microdialysis measurement of oxytocin, aspartate, gamma-aminobutyric acid and glutamate release from the olfactory bulb of the sheep during vaginocervical stimulation. Brain Res. 442, 171–174, https://doi.org/10.1016/0006-8993(88)91447-3.Search in Google Scholar

Kobayashi, K. and Yasoshima, Y. (2001). The central noradrenaline system and memory consolidation. Neuroscientist 7, 371–376, https://doi.org/10.1177/107385840100700506.Search in Google Scholar PubMed

Lenschow, C. and Brecht, M. (2015). Barrel cortex membrane potential dynamics in social touch. Neuron 85, 718–725, https://doi.org/10.1016/j.neuron.2014.12.059.Search in Google Scholar PubMed

Lévy, F., Gervais, R., Kindermann, U., Orgeur, P., and Piketty, V. (1990). Importance of β-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behav. Neurosci. 104, 464–469, https://doi.org/10.1037//0735-7044.104.3.464.Search in Google Scholar

Lévy, F., Guevara-Guzman, R., Hinton, M., Kendrick, K., and Keverne, E. (1993). Effects of parturition and maternal experience on noradrenaline and acetylcholine release in the olfactory bulb of sheep. Behav. Neurosci. 107, 662–668, https://doi.org/10.1037//0735-7044.107.4.662.Search in Google Scholar

Lévy, F., Kendrick, K., Goode, J., Guevara-Guzman, R., and Keverne, E. (1995). Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: Changes with maternal experience and effects on acetylcholine, γ-aminobutyric acid, glutamate and noradrenaline release. Brain Res. 669, 197–206, https://doi.org/10.1016/0006-8993(94)01236-b.Search in Google Scholar

Lévy, F., Richard, P., Meurisse, M., and Ravel, N. (1997). Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs. Psychopharmacology (Berl.) 129, 85–90, https://doi.org/10.1007/s002130050166.Search in Google Scholar PubMed

Lukas, M. and de Jong, T.R. (2015). Conspecific interactions in adult laboratory rodents: Friends or foes? Social Behavior from Rodents to Humans. (Springer), pp. 3–24.10.1007/7854_2015_428Search in Google Scholar PubMed

Lukas, M., Suyama, H., and Egger, V. (2019). Vasopressin cells in the rodent olfactory bulb resemble non-bursting superficial tufted cells and are primarily inhibited upon olfactory nerve stimulation. eNeuro 6, ENEURO.0431-0418.2019, https://doi.org/10.1523/ENEURO.0431-18.2019.Search in Google Scholar PubMed PubMed Central

Mandairon, N. and Linster, C. (2009). Odor perception and olfactory bulb plasticity in adult mammals. J. Neurophysiol. 101, 2204–2209, https://doi.org/10.1152/jn.00076.2009.Search in Google Scholar PubMed

Marlin, B.J., Mitre, M., D’Amour, J.A., Chao, M.V., and Froemke, R.C. (2015). Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520, 499–504, https://doi.org/10.1038/nature14402.Search in Google Scholar PubMed PubMed Central

Matsutani, S. (2010). Trajectory and terminal distribution of single centrifugal axons from olfactory cortical areas in the rat olfactory bulb. Neuroscience 169, 436–448, https://doi.org/10.1016/j.neuroscience.2010.05.001.Search in Google Scholar PubMed

Matsutani, S. and Yamamoto, N. (2008). Centrifugal innervation of the mammalian olfactory bulb. Anat. Sci. Int. 83, 218–227, https://doi.org/10.1111/j.1447-073x.2007.00223.x.Search in Google Scholar PubMed

Moura, P.J., Meirelles, S.T., and Xavier, G.F. (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, 663–676, https://doi.org/10.1590/s0100-879x2010007500047.Search in Google Scholar

Müller, M., Schwarz, I., Pavlova, I., Schweihoff, J., Musacchio, F., Mittag, M., Fuhrmann, M., and Schwarz, M.K. (2021). The diagonal band of broca regulates olfactory-mediated behaviors by modulating odor-evoked responses within the olfactory bulb. Available at SSRN: https://ssrn.com/abstract=3927424 or https://doi.org/10.2139/ssrn.3927424.Search in Google Scholar

Oettl, L.L., Ravi, N., Schneider, M., Scheller, M.F., Schneider, P., Mitre, M., da Silva Gouveia, M., Froemke, R.C., Chao, M.V., Young, W.S., et al.. (2016). Oxytocin enhances social recognition by modulating cortical control of early olfactory processing. Neuron 90, 609–621, https://doi.org/10.1016/j.neuron.2016.03.033.Search in Google Scholar

Ojima, H., Yamasaki, T., Kojima, H., and Akashi, A. (1988). Cholinergic innervation of the main and the accessory olfactory bulbs of the rat as revealed by a monoclonal antibody against choline acetyltransferase. Anat. Embryol. (Berl.) 178, 481–488, https://doi.org/10.1007/bf00305035.Search in Google Scholar

Okutani, F., Kaba, H., Takahashi, S., and Seto, K. (1998). The biphasic effects of locus coeruleus noradrenergic activation on dendrodendritic inhibition in the rat olfactory bulb. Brain Res. 783, 272–279, https://doi.org/10.1016/s0006-8993(97)01371-1.Search in Google Scholar

Poindron, P. and Neindre, P.L. (1980). Endocrine and sensory regulation of maternal behavior in the ewe. Advances in the Study of Behavior. J. S. Rosenblatt, R. A. Hinde, C. Beer, and M.-C. Busnel, eds. (Academic Press), pp. 75–119.10.1016/S0065-3454(08)60115-1Search in Google Scholar

Roberts, E.K., Lu, A., Bergman, T.J., and Beehner, J.C. (2012). A bruce effect in wild geladas. Science 335, 1222–1225, https://doi.org/10.1126/science.1213600.Search in Google Scholar

Rosser, A.E. and Keverne, E.B. (1985). The importance of central noradrenergic neurones in the formation of an olfactory memory in the prevention of pregnancy block. Neuroscience 15, 1141–1147, https://doi.org/10.1016/0306-4522(85)90258-1.Search in Google Scholar

Rozenkrantz, L., Weissgross, R., Weiss, T., Ravreby, I., Frumin, I., Shushan, S., Gorodisky, L., Reshef, N., Holzman, Y., Pinchover, L., et al.. (2020). Unexplained repeated pregnancy loss is associated with altered perceptual and brain responses to men’s body-odor. eLife 9, e55305, https://doi.org/10.7554/eLife.55305.Search in Google Scholar PubMed PubMed Central

Sanchez-Andrade, G. and Kendrick, K.M. (2009). The main olfactory system and social learning in mammals. Behav. Brain Res. 200, 323–335, https://doi.org/10.1016/j.bbr.2008.12.021.Search in Google Scholar PubMed

Shipley, M.T. and Ennis, M. (1996). Functional organization of olfactory system. J. Neurobiol. 30, 123–176, https://doi.org/10.1002/(sici)1097-4695(199605)30:1<123::aid-neu11>3.0.co;2-n.10.1002/(SICI)1097-4695(199605)30:1<123::AID-NEU11>3.0.CO;2-NSearch in Google Scholar

Singer, A.G., Beauchamp, G.K., and Yamazaki, K. (1997). Volatile signals of the major histocompatibility complex in male mouse urine. Proc. Natl. Acad. Sci. U. S. A. 94, 2210–2214, https://doi.org/10.1073/pnas.94.6.2210.Search in Google Scholar

Sun, C., Yin, Z., Li, B.Z., Du, H., Tang, K., Liu, P., Hang Pun, S., Lei, T.C., and Li, A. (2021). Oxytocin modulates neural processing of mitral/tufted cells in the olfactory bulb. Acta Physiol. (Oxf.) 231, e13626, https://doi.org/10.1111/apha.13626.Search in Google Scholar

Suyama, H., Egger, V., and Lukas, M. (2021). Top-down acetylcholine signaling via olfactory bulb vasopressin cells contributes to social discrimination in rats. Commun. Biol. 4, 603, https://doi.org/10.1038/s42003-021-02129-7.Search in Google Scholar

Terranova, J.P., Perio, A., Worms, P., Le Fur, G., and Soubrie, P. (1994). Social olfactory recognition in rodents: Deterioration with age, cerebral ischaemia and septal lesion. Behav. Pharmacol. 5, 90–98, https://doi.org/10.1097/00008877-199402000-00010.Search in Google Scholar

Thor, D.H. and Holloway, W.R. (1982). Social memory of the male laboratory rat. J. Comp. Physiol. Psychol. 96, 1000–1006, https://doi.org/10.1037/0735-7036.96.6.1000.Search in Google Scholar

Tobin, V.A., Hashimoto, H., Wacker, D.W., Takayanagi, Y., Langnaese, K., Caquineau, C., Noack, J., Landgraf, R., Onaka, T., Leng, G., et al.. (2010). An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 464, 413–417, https://doi.org/10.1038/nature08826.Search in Google Scholar

Tschanz, B. (1962). Über die Beziehung zwischen Muttertier und Jungen beim Mufflon (Ovis aries musimon, Pall). Experientia 18, 187–190, doi:https://doi.org/10.1007/BF02151723.Search in Google Scholar

Vinera, J., Kermen, F., Sacquet, J., Didier, A., Mandairon, N., and Richard, M. (2015). Olfactory perceptual learning requires action of noradrenaline in the olfactory bulb: Comparison with olfactory associative learning. Learn. Mem. 22, 192–196, https://doi.org/10.1101/lm.036608.114.Search in Google Scholar

Wersinger, S.R., Temple, J.L., Caldwell, H.K., and Young, W.S.3rd (2008). Inactivation of the oxytocin and the vasopressin (avp) 1b receptor genes, but not the avp 1a receptor gene, differentially impairs the bruce effect in laboratory mice (mus musculus). Endocrinology 149, 116–121, https://doi.org/10.1210/en.2007-1056.Search in Google Scholar

Wilson, D.A., Fletcher, M.L., and Sullivan, R.M. (2004). Acetylcholine and olfactory perceptual learning. Learn. Mem. 11, 28–34, https://doi.org/10.1101/lm.66404.Search in Google Scholar PubMed PubMed Central

Published Online: 2022-06-21
Published in Print: 2022-08-26

© 2022 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Editorial
  3. Editorial
  4. Review articles
  5. Perireceptor events and peripheral modulation of olfactory signals in the olfactory epithelium of vertebrates
  6. Mammalian social memory relies on neuromodulation in the olfactory bulb
  7. How the body rules the nose
  8. Information about space from time: how mammals navigate the odour landscape
  9. Functional role of the anterior olfactory nucleus in sensory information processing
  10. How the sense of smell influences cognition throughout life
  11. Presentation of scientific institutions
  12. The “MultiSensE” consortium
  13. Nachrichten aus der Gesellschaft
  14. Nachrichten aus der Gesellschaft
https://doi.org/10.1515/nf-2022-0004
Keywords for this article
bruce effect; noradrenaline; olfactory bulb; social memory; vasopressin

Articles in the same Issue

  1. Frontmatter
  2. Editorial
  3. Editorial
  4. Review articles
  5. Perireceptor events and peripheral modulation of olfactory signals in the olfactory epithelium of vertebrates
  6. Mammalian social memory relies on neuromodulation in the olfactory bulb
  7. How the body rules the nose
  8. Information about space from time: how mammals navigate the odour landscape
  9. Functional role of the anterior olfactory nucleus in sensory information processing
  10. How the sense of smell influences cognition throughout life
  11. Presentation of scientific institutions
  12. The “MultiSensE” consortium
  13. Nachrichten aus der Gesellschaft
  14. Nachrichten aus der Gesellschaft
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