Skip to main content
SpringerLink
Log in

Oxytocin and Olfaction

  • Chapter
  • First Online:
Behavioral Pharmacology of Neuropeptides: Oxytocin

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 35))

Abstract

Social signals are identified through processing in sensory systems to trigger appropriate behavioral responses. Social signals are received primarily in most mammals through the olfactory system. Individuals are recognized based on their unique blend of odorants. Such individual recognition is critical to distinguish familiar conspecifics from intruders and to recognize offspring. Social signals can also trigger stereotyped responses like mating behaviors. Specific sensory pathways for individual recognition and eliciting stereotyped responses have been identified both in the early olfactory system and its connected cortices. Oxytocin is emerging as a major state modulator of sensory processing with distinct functions in early and higher olfactory brain regions. The brain state induced through Oxytocin influences social perception. Oxytocin acting on different brain regions can promote either exploration and recognition towards same- or other-sex conspecifics, or association learning. Region-specific deletion of Oxytocin receptors suffices to disrupt these behaviors. Together, these recent insights highlight that Oxytocin’s function in social behaviors cannot be understood without considering its actions on sensory processing.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

  • Alonso M, Lepousez G, Sebastien W, Bardy C, Gabellec MM, Torquet N, Lledo PM (2012) Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 15:897–904

    Article  PubMed  CAS  Google Scholar 

  • Angelo K, Rancz EA, Pimentel D, Hundahl C, Hannibal J, Fleischmann A, Pichler B, Margrie TW (2012) A biophysical signature of network affiliation and sensory processing in mitral cells. Nature 488:375–378

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arzi A, Rozenkrantz L, Holtzman Y, Secundo L, Sobel N (2014) Sniffing patterns uncover implicit memory for undetected odors. Curr Biol 24:R263–R264

    Article  PubMed  CAS  Google Scholar 

  • Balu R, Strowbridge BW (2007) Opposing inward and outward conductances regulate rebound discharges in olfactory mitral cells. J Neurophysiol 97:1959–1968

    Article  PubMed  CAS  Google Scholar 

  • Balu R, Pressler RT, Strowbridge BW (2007) Multiple modes of synaptic excitation of olfactory bulb granule cells. J Neurosci 27:5621–5632

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Barlow HB (1961) Possible principles underlying the transformations of sensory messages. In: Rosenblith WA (ed) Sensory communication. M.I.T. Press, Massachusetts Institute of Technology, Cambridge, pp 217–234

    Google Scholar 

  • Baum MJ, Keverne EB (2002) Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Horm Behav 41:213–219

    Article  PubMed  CAS  Google Scholar 

  • Benelli A, Bertolini A, Poggioli R, Menozzi B, Basaglia R, Arletti R (1995) Polymodal dose-response curve for oxytocin in the social recognition test. Neuropeptides 28:251–255

    Article  PubMed  CAS  Google Scholar 

  • Blanchard RJ, Flannelly KJ, Blanchard DC (1988) Life-span studies of dominance and aggression in established colonies of laboratory rats. Physiol Behav 43:1–7

    Article  PubMed  CAS  Google Scholar 

  • Bluthe RM, Dantzer R (1990) Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res 535:301–304

    Article  PubMed  CAS  Google Scholar 

  • Boyd AM, Sturgill JF, Poo C, Isaacson JS (2012) Cortical feedback control of olfactory bulb circuits. Neuron 76:1161–1174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond Ser B Biol Sci 361:2061–2078

    Article  CAS  Google Scholar 

  • Brennan PA, Zufall F (2006) Pheromonal communication in vertebrates. Nature 444:308–315

    Article  PubMed  CAS  Google Scholar 

  • Bridges RS, Mann PE, Coppeta JS (1999) Hypothalamic involvement in the regulation of maternal behaviour in the rat: inhibitory roles for the ventromedial hypothalamus and the dorsal/anterior hypothalamic areas. J Neuroendocrinol 11:259–266

    Article  PubMed  CAS  Google Scholar 

  • Broad K, Levy F, Evans G, Kimura T, Keverne E, Kendrick K (1999) Previous maternal experience potentiates the effect of parturition on oxytocin receptor mRNA expression in the paraventricular nucleus. Eur J Neurosci 11:3725–3737

    Article  PubMed  CAS  Google Scholar 

  • Brunjes PC, Illig KR, Meyer EA (2005) A field guide to the anterior olfactory nucleus (cortex). Brain Res Brain Res Rev 50:305–335

    Article  PubMed  Google Scholar 

  • Cajal SRY (1911) Histologie du système nerveux de l’homme & des vertĂ©brĂ©s, vol 2. Maloine, Paris

    Google Scholar 

  • Calcagnoli F, de Boer SF, Beiderbeck DI, Althaus M, Koolhaas JM, Neumann ID (2014) Local oxytocin expression and oxytocin receptor binding in the male rat brain is associated with aggressiveness. Behav Brain Res 261:315–322

    PubMed  CAS  Google Scholar 

  • von Campenhausen H, Mori K (2000) Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse. Eur J Neurosci 12:33–46

    Article  Google Scholar 

  • Canteras NS, Simerly RB, Swanson LW (1995) Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 360:213–245

    Article  PubMed  CAS  Google Scholar 

  • Choe HK, Reed MD, Benavidez N, Montgomery D, Soares N, Yim YS, Choi GB (2015) Oxytocin mediates entrainment of sensory stimuli to social cues of opposing valence. Neuron 87:152–163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choleris E, Gustafsson JA, Korach KS, Muglia LJ, Pfaff DW, Ogawa S (2003) An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-alpha and -beta knockout mice. Proc Natl Acad Sci U S A 100:6192–6197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choleris E, Little SR, Mong JA, Puram SV, Langer R, Pfaff DW (2007) Microparticle-based delivery of oxytocin receptor antisense DNA in the medial amygdala blocks social recognition in female mice. Proc Natl Acad Sci U S A 104:4670–4675

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cohen-Tannoudji J, Lavenet C, Locatelli A, Tillet Y, Signoret JP (1989) Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour. J Reprod Fertil 86:135–144

    Article  PubMed  CAS  Google Scholar 

  • Da Costa AP, Guevara-Guzman RG, Ohkura S, Goode JA, Kendrick KM (1996) The role of oxytocin release in the paraventricular nucleus in the control of maternal behaviour in the sheep. J Neuroendocrinol 8:163–177

    Article  PubMed  Google Scholar 

  • Del Punta K, Leinders-Zufall T, Rodriguez I, Jukam D, Wysocki CJ, Ogawa S, Zufall F, Mombaerts P (2002) Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419:70–74

    Article  PubMed  CAS  Google Scholar 

  • Devore S, Linster C (2012) Noradrenergic and cholinergic modulation of olfactory bulb sensory processing. Front Behav Neurosci 6:52

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dluzen DE, Muraoka S, Engelmann M, Landgraf R (1998) 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

    Article  PubMed  CAS  Google Scholar 

  • Dolen G, Darvishzadeh A, Huang KW, Malenka RC (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501:179–184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dorries KM, Adkins-Regan E, Halpern BP (1995) Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig. Physiol Behav 57:255–259

    Article  PubMed  CAS  Google Scholar 

  • Doty RL (1986) Odor-guided behavior in mammals. Experientia 42:257–271

    Article  PubMed  CAS  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 90:89–94

    Article  PubMed  CAS  Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW (1985) Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526–532

    Article  CAS  PubMed  Google Scholar 

  • Febo M, Numan M, Ferris CF (2005) Functional magnetic resonance imaging shows oxytocin activates brain regions associated with mother-pup bonding during suckling. J Neurosci 25:11637–11644

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25:284–288

    Article  PubMed  CAS  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 21:8278–8285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferris CF, Yee JR, Kenkel WM, Dumais KM, Moore K, Veenema AH, Kulkarni P, Perkybile AM, Carter CS (2015) Distinct BOLD activation profiles following central and peripheral oxytocin Administration in Awake Rats. Front Behav Neurosci 9:245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fleming AS, Rosenblatt JS (1974a) Olfactory regulation of maternal behavior in rats. I Effects of olfactory bulb removal in experienced and inexperienced lactating and cycling females. J Comp Physiol Psychol 86:221–232

    Article  PubMed  CAS  Google Scholar 

  • Fleming AS, Rosenblatt JS (1974b) Olfactory regulation of maternal behavior in rats. II Effects of peripherally induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins. J Comp Physiol Psychol 86:233–246

    Article  PubMed  CAS  Google Scholar 

  • Fleming A, Vaccarino F, Tambosso L, Chee P (1979) Vomeronasal and olfactory system modulation of maternal behavior in the rat. Science 203:372–374

    Article  PubMed  CAS  Google Scholar 

  • Fleming AS, Vaccarino F, Luebke C (1980) Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol Behav 25:731–743

    Article  PubMed  CAS  Google Scholar 

  • Fleming AS, Cheung U, Myhal N, Kessler Z (1989) Effects of maternal hormones on “timidity” and attraction to pup-related odors in female rats. Physiol Behav 46:449–453

    Article  PubMed  CAS  Google Scholar 

  • Gur R, Tendler A, Wagner S (2014) Long-term social recognition memory is mediated by oxytocin-dependent synaptic plasticity in the medial amygdala. Biol Psychiatry 76:377–386

    Article  PubMed  CAS  Google Scholar 

  • Haswell CC, Izawa J, Dowell LR, Mostofsky SH, Shadmehr R (2009) Representation of internal models of action in the autistic brain. Nat Neurosci 12:970–972

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huber D, Veinante P, Stoop R (2005) Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 308:245–248

    Article  PubMed  CAS  Google Scholar 

  • Insel TR, Shapiro LE (1992) Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc Natl Acad Sci U S A 89:5981–5985

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Insel TR, Young LJ (2001) The neurobiology of attachment. Nat Rev Neurosci 2:129–136

    Article  CAS  PubMed  Google Scholar 

  • Jakupovic J, Kang N, Baum MJ (2008) Effect of bilateral accessory olfactory bulb lesions on volatile urinary odor discrimination and investigation as well as mating behavior in male mice. Physiol Behav 93:467–473

    Article  PubMed  CAS  Google Scholar 

  • Jemiolo B, Andreolini F, Xie TM, Wiesler D, Novotny M (1989) Puberty-affecting synthetic analogs of urinary chemosignals in the house mouse, Mus Domesticus. Physiol Behav 46:293–298

    Article  PubMed  CAS  Google Scholar 

  • Kang N, Baum MJ, Cherry JA (2009) A direct main olfactory bulb projection to the “vomeronasal” amygdala in female mice selectively responds to volatile pheromones from males. Eur J Neurosci 29:624–634

    Article  PubMed  PubMed Central  Google Scholar 

  • Kay LM, Laurent G (1999) Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci 2:1003–1009

    Article  PubMed  CAS  Google Scholar 

  • Keller M, Douhard Q, Baum MJ, Bakker J (2006) Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chem Senses 31:315–323

    Article  PubMed  Google Scholar 

  • Kendrick K (1994) Neurobiological correlates of visual and olfactory recognition in sheep. Behav Process 33:89–111

    Article  CAS  Google Scholar 

  • Kendrick KM, Keverne EB (1992) Control of synthesis and release of oxytocin in the sheep Brain. Ann N Y Acad Sci 652:102–121

    Article  PubMed  CAS  Google Scholar 

  • Kendrick KM, LĂ©vy F, Keverne EB (1991) Importance of vaginocervical stimulation for the formation of maternal bonding in primiparous and multiparous parturient ewes. Physiol Behav 50:595–600

    Article  PubMed  CAS  Google Scholar 

  • Kendrick KM, Levy F, Keverne EB (1992) Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256:833–836

    Article  PubMed  CAS  Google Scholar 

  • Kendrick KM, Da Costa AP, Broad KD, Ohkura S, Guevara R, Levy F, Keverne EB (1997) Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res Bull 44:383–395

    Article  CAS  PubMed  Google Scholar 

  • Keverne EB (2004) Importance of olfactory and vomeronasal systems for male sexual function. Physiol Behav 83:177–187

    Article  PubMed  CAS  Google Scholar 

  • Keverne E, Levy F, Guevara-Guzman R, Kendrick K (1993) Influence of birth and maternal experience on olfactory bulb neurotransmitter release. Neuroscience 56:557–565

    Article  PubMed  CAS  Google Scholar 

  • Kim Y, Venkataraju KU, Pradhan K, Mende C, Taranda J, Turaga SC, Arganda-Carreras I, Ng L, Hawrylycz MJ, Rockland KS et al (2015) Mapping social behavior-induced brain activation at cellular resolution in the mouse. Cell Rep 10:292–305

    Article  PubMed  CAS  Google Scholar 

  • Knobloch HS, Charlet A, Hoffmann LC, Eliava M, Khrulev S, Cetin AH, Osten P, Schwarz MK, Seeburg PH, Stoop R et al (2012) Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73:553–566

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kristal MB, Graber GC (1976) Placentophagia in nonpregnant rats: influence of estrous cycle stage and birthplace. Physiol Behav 17:599–605

    Article  PubMed  CAS  Google Scholar 

  • Larrazolo-Lopez A, Kendrick KM, Aburto-Arciniega M, Arriaga-Avila V, Morimoto S, Frias M, Guevara-Guzman R (2008) Vaginocervical stimulation enhances social recognition memory in rats via oxytocin release in the olfactory bulb. Neuroscience 152:585–593

    Article  PubMed  CAS  Google Scholar 

  • Larriva-Sahd J (2008) The accessory olfactory bulb in the adult rat: a cytological study of its cell types, neuropil, neuronal modules, and interactions with the main olfactory system. J Comp Neurol 510:309–350

    Article  PubMed  Google Scholar 

  • Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792–796

    Article  PubMed  CAS  Google Scholar 

  • Leinders-Zufall T, Brennan P, Widmayer P, S PC, Maul-Pavicic A, Jager M, Li XH, Breer H, Zufall F, Boehm T (2004) MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306:1033–1037

    Article  PubMed  CAS  Google Scholar 

  • Levy F, Keller M (2009) Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res 200:336–345

    Article  PubMed  Google Scholar 

  • Levy F, Poindron P, Le Neindre P (1983) Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition. Physiol Behav 31:687–692

    Article  PubMed  CAS  Google Scholar 

  • LĂ©vy F, Kendrick KM, Keverne EB, Piketty V, Poindron P (1992) Intracerebral oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anesthesia. Behav Neurosci 106:427–432

    Article  PubMed  Google Scholar 

  • Levy F, Kendrick KM, Goode JA, Guevara-Guzman R, Keverne EB (1995a) Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: changes with maternal experience and effects on acetylcholine, gamma-aminobutyric acid, glutamate and noradrenaline release. Brain Res 669:197–206

    Article  PubMed  CAS  Google Scholar 

  • Levy F, Locatelli A, Piketty V, Tillet Y, Poindron P (1995b) Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Physiol Behav 57:97–104

    Article  PubMed  CAS  Google Scholar 

  • Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735–769

    Article  PubMed  CAS  Google Scholar 

  • Lukas M, Neumann ID (2013) Oxytocin and vasopressin in rodent behaviors related to social dysfunctions in autism spectrum disorders. Behav Brain Res 251:85–94

    Article  PubMed  CAS  Google Scholar 

  • Lukas M, Toth I, Reber SO, Slattery DA, Veenema AH, Neumann ID (2011) The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice. Neuropsychopharmacology 36:2159–2168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lukas M, Toth I, Veenema AH, Neumann ID (2013) Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 38:916–926

    Article  PubMed  CAS  Google Scholar 

  • Luo M, Fee MS, Katz LC (2003) Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299:1196–1201

    Article  PubMed  CAS  Google Scholar 

  • Luskin MB, Price JL (1983) The laminar distribution of intracortical fibers originating in the olfactory cortex of the rat. J Comp Neurol 216:292–302

    Article  PubMed  CAS  Google Scholar 

  • Ma D, Allen ND, Van Bergen YC, Jones CM, Baum MJ, Keverne EB, Brennan PA (2002) Selective ablation of olfactory receptor neurons without functional impairment of vomeronasal receptor neurons in OMP-ntr transgenic mice. Eur J Neurosci 16:2317–2323

    Article  PubMed  Google Scholar 

  • Mandairon N, Poncelet J, Bensafi M, Didier A (2009) Humans and mice express similar olfactory preferences. PLoS One 4:e4209

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Margrie TW, Sakmann B, Urban NN (2001) Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb. Proc Natl Acad Sci U S A 98:319–324

    Article  PubMed  CAS  Google Scholar 

  • Markopoulos F, Rokni D, Gire DH, Murthy VN (2012) Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76:1175–1188

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marlin BJ, Mitre M, D’Amour JA, Chao MV, Froemke RC (2015) Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520:499–504

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meddle SL, Bishop VR, Gkoumassi E, van Leeuwen FW, Douglas AJ (2007) Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain. Endocrinology 148:5095–5104

    Article  PubMed  CAS  Google Scholar 

  • Mitre M, Marlin BJ, Schiavo JK, Morina E, Norden SE, Hackett TA, Aoki CJ, Chao MV, Froemke RC (2016) A distributed network for social cognition enriched for oxytocin receptors. J Neurosci 36:2517–2535

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer, New York

    Google Scholar 

  • Numan M, Numan MJ, English JB (1993) Excitotoxic amino acid injections into the medial amygdala facilitate maternal behavior in virgin female rats. Horm Behav 27:56–81

    Article  PubMed  CAS  Google Scholar 

  • Oettl LL, Ravi N, Schneider M, Scheller MF, Schneider P, Mitre M, da Silva Gouveia M, Froemke RC, Chao MV, Young WS et al (2016) Oxytocin enhances social recognition by modulating cortical control of early olfactory processing. Neuron 90:609–621

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Olazabal DE, Young LJ (2006) Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Horm Behav 49:681–687

    Article  CAS  PubMed  Google Scholar 

  • Owen SF, Tuncdemir SN, Bader PL, Tirko NN, Fishell G, Tsien RW (2013) Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature 500:458–462

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pankevich DE, Baum MJ, Cherry JA (2004) Olfactory sex discrimination persists, whereas the preference for urinary odorants from estrous females disappears in male mice after vomeronasal organ removal. J Neurosci 24:9451–9457

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pankevich DE, Cherry JA, Baum MJ (2006) Effect of vomeronasal organ removal from male mice on their preference for and neural Fos responses to female urinary odors. Behav Neurosci 120:925–936

    Article  PubMed  PubMed Central  Google Scholar 

  • Pedersen CA, Prange AJ Jr (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci U S A 76:6661–6665

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ Jr (1985) Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides 6:175–182

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JS, Lehrman D (1963) Maternal behavior of the laboratory rat. In: Rheingold HL (ed) Maternal behavior in mammals, Wiley, New York, pp 8–57

    Google Scholar 

  • Rosenblatt JS, Mayer AD (1995) An analysis of approach/withdrawal processes in the initiation of maternal behavior in the laboratory rat. In: Hood KE, Greenberg E, Tobach E (eds) Behavioral development, concepts of approach/withdrawal and integrative levels. Garland Press, New York, pp 177–230

    Google Scholar 

  • Rozenkrantz L, Zachor D, Heller I, Plotkin A, Weissbrod A, Snitz K, Secundo L, Sobel N (2015) A mechanistic link between olfaction and autism spectrum disorder. Curr Biol 25:1904–1910

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanchez-Andrade G, Kendrick KM (2009) The main olfactory system and social learning in mammals. Behav Brain Res 200:323–335

    Article  PubMed  Google Scholar 

  • Scalia F, Winans SS (1975) The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol 161:31–55

    Article  PubMed  CAS  Google Scholar 

  • Shamay-Tsoory SG, Abu-Akel A (2016) The social salience hypothesis of oxytocin. Biol Psychiatry 79:194–202

    Article  PubMed  CAS  Google Scholar 

  • Slotnick BM, Carpenter ML, Fusco R (1973) Initiation of maternal behavior in pregnant nulliparous rats. Horm Behav 4:53–59

    Article  Google Scholar 

  • Spehr M, Kelliher KR, Li XH, Boehm T, Leinders-Zufall T, Zufall F (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J Neurosci 26:1961–1970

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Takayanagi Y, Yoshida M, Bielsky IF, Ross HE, Kawamata M, Onaka T, Yanagisawa T, Kimura T, Matzuk MM, Young LJ et al (2005) Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A 102:16096–16101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Uchida N, Kepecs A, Mainen ZF (2006) Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat Rev Neurosci 7:485–491

    Article  PubMed  CAS  Google Scholar 

  • Vaccari C, Lolait SJ, Ostrowski NL (1998) Comparative distribution of vasopressin V1b and oxytocin receptor messenger ribonucleic acids in brain. Endocrinology 139:5015–5033

    Article  PubMed  CAS  Google Scholar 

  • Viviani D, Charlet A, van den Burg E, Robinet C, Hurni N, Abatis M, Magara F, Stoop R (2011) Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science 333:104–107

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wacker DW, Tobin VA, Noack J, Bishop VR, Duszkiewicz AJ, Engelmann M, Meddle SL, Ludwig M (2010) Expression of early growth response protein 1 in vasopressin neurones of the rat anterior olfactory nucleus following social odour exposure. J Physiol 588:4705–4717

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc Natl Acad Sci U S A 104:16681–16684

    Article  PubMed  PubMed Central  Google Scholar 

  • Wamboldt MZ, Insel TR (1987) The ability of oxytocin to induce short latency maternal behavior is dependent on peripheral anosmia. Behav Neurosci 101:439–441

    Article  CAS  PubMed  Google Scholar 

  • Wesson DW (2013) Sniffing behavior communicates social hierarchy. Curr Biol 23:575–580

    Article  PubMed  CAS  Google Scholar 

  • Wesson DW, Keller M, Douhard Q, Baum MJ, Bakker J (2006) Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm Behav 49:580–586

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wiesner BP, Sheard NM (1933) Maternal behaviour in the rat. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Xu F, Schaefer M, Kida I, Schafer J, Liu N, Rothman DL, Hyder F, Restrepo D, Shepherd GM (2005) Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J Comp Neurol 489:491–500

    Article  PubMed  Google Scholar 

  • Yu GZ, Kaba H, Okutani F, Takahashi S, Higuchi T (1996) The olfactory bulb: a critical site of action for oxytocin in the induction of maternal behaviour in the rat. Neuroscience 72:1083–1088

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Medical Faculty Mannheim, Central Institute of Mental Health, Heidelberg University, Heidelberg, Germany

    Lars-Lennart Oettl & Wolfgang Kelsch

Authors
  1. Lars-Lennart Oettl
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wolfgang Kelsch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wolfgang Kelsch .

Editor information

Editors and Affiliations

  1. Department of Psychiatry, University of Bonn, Bonn, Nordrhein-Westfalen, Germany

    Rene Hurlemann

  2. Schaller Research Group on Neuropeptides German Cancer Research Center, University of Heidelberg, Heidelberg, BW, Germany

    Valery Grinevich

  3. Central Institute of Mental Health, University of Heidelberg, Mannheim, BW, Germany

    Valery Grinevich

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Oettl, LL., Kelsch, W. (2017). Oxytocin and Olfaction. In: Hurlemann, R., Grinevich, V. (eds) Behavioral Pharmacology of Neuropeptides: Oxytocin. Current Topics in Behavioral Neurosciences, vol 35. Springer, Cham. https://doi.org/10.1007/7854_2017_8

Download citation

Publish with us

Policies and ethics

Search

Navigation