Oxytocin and Olfaction

  • Lars-Lennart Oettl
  • Wolfgang KelschEmail author
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 35)


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.


Amygdala Anterior olfactory nucleus Mice Oxytocin Olfactory bulb Pheromone Piriform cortex Rats Sheep 


  1. 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 15:897–904PubMedCrossRefGoogle Scholar
  2. 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 488:375–378PubMedPubMedCentralCrossRefGoogle Scholar
  3. Arzi A, Rozenkrantz L, Holtzman Y, Secundo L, Sobel N (2014) Sniffing patterns uncover implicit memory for undetected odors. Curr Biol 24:R263–R264PubMedCrossRefGoogle Scholar
  4. Balu R, Strowbridge BW (2007) Opposing inward and outward conductances regulate rebound discharges in olfactory mitral cells. J Neurophysiol 97:1959–1968PubMedCrossRefGoogle Scholar
  5. Balu R, Pressler RT, Strowbridge BW (2007) Multiple modes of synaptic excitation of olfactory bulb granule cells. J Neurosci 27:5621–5632PubMedCrossRefGoogle Scholar
  6. 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 217–234Google Scholar
  7. Baum MJ, Keverne EB (2002) Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Horm Behav 41:213–219PubMedCrossRefGoogle Scholar
  8. 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 28:251–255PubMedCrossRefGoogle Scholar
  9. Blanchard RJ, Flannelly KJ, Blanchard DC (1988) Life-span studies of dominance and aggression in established colonies of laboratory rats. Physiol Behav 43:1–7PubMedCrossRefGoogle Scholar
  10. Bluthe RM, Dantzer R (1990) Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res 535:301–304PubMedCrossRefGoogle Scholar
  11. Boyd AM, Sturgill JF, Poo C, Isaacson JS (2012) Cortical feedback control of olfactory bulb circuits. Neuron 76:1161–1174PubMedPubMedCentralCrossRefGoogle Scholar
  12. Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond Ser B Biol Sci 361:2061–2078CrossRefGoogle Scholar
  13. Brennan PA, Zufall F (2006) Pheromonal communication in vertebrates. Nature 444:308–315PubMedCrossRefGoogle Scholar
  14. 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 11:259–266PubMedCrossRefGoogle Scholar
  15. 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 11:3725–3737PubMedCrossRefGoogle Scholar
  16. Brunjes PC, Illig KR, Meyer EA (2005) A field guide to the anterior olfactory nucleus (cortex). Brain Res Brain Res Rev 50:305–335PubMedCrossRefGoogle Scholar
  17. Cajal SRY (1911) Histologie du système nerveux de l’homme & des vertébrés, vol 2. Maloine, ParisGoogle Scholar
  18. 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 261:315–322PubMedPubMedCentralGoogle Scholar
  19. 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 12:33–46CrossRefGoogle Scholar
  20. 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 360:213–245PubMedCrossRefGoogle Scholar
  21. 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 87:152–163PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 100:6192–6197PubMedPubMedCentralCrossRefGoogle Scholar
  23. 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 104:4670–4675PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 86:135–144PubMedCrossRefGoogle Scholar
  25. 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 8:163–177PubMedCrossRefGoogle Scholar
  26. 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 419:70–74PubMedCrossRefGoogle Scholar
  27. Devore S, Linster C (2012) Noradrenergic and cholinergic modulation of olfactory bulb sensory processing. Front Behav Neurosci 6:52PubMedPubMedCentralGoogle Scholar
  28. 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 19:999–1005PubMedCrossRefGoogle Scholar
  29. Dolen G, Darvishzadeh A, Huang KW, Malenka RC (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501:179–184PubMedPubMedCentralCrossRefGoogle Scholar
  30. Dorries KM, Adkins-Regan E, Halpern BP (1995) Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig. Physiol Behav 57:255–259PubMedCrossRefGoogle Scholar
  31. Doty RL (1986) Odor-guided behavior in mammals. Experientia 42:257–271PubMedCrossRefGoogle Scholar
  32. Engelmann M, Ebner K, Wotjak CT, Landgraf R (1998) Endogenous oxytocin is involved in short-term olfactory memory in female rats. Behav Brain Res 90:89–94PubMedCrossRefGoogle Scholar
  33. Fahrbach SE, Morrell JI, Pfaff DW (1985) Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526–532CrossRefPubMedGoogle Scholar
  34. 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 25:11637–11644PubMedCrossRefGoogle Scholar
  35. Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25:284–288PubMedPubMedCentralCrossRefGoogle Scholar
  36. Ferguson JN, Aldag JM, Insel TR, Young LJ (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21:8278–8285CrossRefPubMedGoogle Scholar
  37. 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 9:245PubMedPubMedCentralCrossRefGoogle Scholar
  38. 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 86:221–232PubMedCrossRefGoogle Scholar
  39. 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 86:233–246PubMedCrossRefGoogle Scholar
  40. Fleming A, Vaccarino F, Tambosso L, Chee P (1979) Vomeronasal and olfactory system modulation of maternal behavior in the rat. Science 203:372–374PubMedCrossRefGoogle Scholar
  41. Fleming AS, Vaccarino F, Luebke C (1980) Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol Behav 25:731–743PubMedCrossRefGoogle Scholar
  42. 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 46:449–453PubMedCrossRefGoogle Scholar
  43. 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 76:377–386PubMedCrossRefGoogle Scholar
  44. Haswell CC, Izawa J, Dowell LR, Mostofsky SH, Shadmehr R (2009) Representation of internal models of action in the autistic brain. Nat Neurosci 12:970–972PubMedPubMedCentralCrossRefGoogle Scholar
  45. Huber D, Veinante P, Stoop R (2005) Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 308:245–248PubMedPubMedCentralCrossRefGoogle Scholar
  46. Insel TR, Shapiro LE (1992) Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc Natl Acad Sci U S A 89:5981–5985PubMedPubMedCentralCrossRefGoogle Scholar
  47. Insel TR, Young LJ (2001) The neurobiology of attachment. Nat Rev Neurosci 2:129–136CrossRefPubMedGoogle Scholar
  48. 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 93:467–473PubMedCrossRefGoogle Scholar
  49. 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 46:293–298PubMedCrossRefGoogle Scholar
  50. 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 29:624–634PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kay LM, Laurent G (1999) Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci 2:1003–1009PubMedCrossRefGoogle Scholar
  52. 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 31:315–323PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kendrick K (1994) Neurobiological correlates of visual and olfactory recognition in sheep. Behav Process 33:89–111CrossRefGoogle Scholar
  54. Kendrick KM, Keverne EB (1992) Control of synthesis and release of oxytocin in the sheep Brain. Ann N Y Acad Sci 652:102–121PubMedCrossRefGoogle Scholar
  55. Kendrick KM, Lévy F, Keverne EB (1991) Importance of vaginocervical stimulation for the formation of maternal bonding in primiparous and multiparous parturient ewes. Physiol Behav 50:595–600PubMedCrossRefGoogle Scholar
  56. Kendrick KM, Levy F, Keverne EB (1992) Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256:833–836PubMedCrossRefGoogle Scholar
  57. 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 44:383–395CrossRefPubMedGoogle Scholar
  58. Keverne EB (2004) Importance of olfactory and vomeronasal systems for male sexual function. Physiol Behav 83:177–187PubMedCrossRefGoogle Scholar
  59. Keverne E, Levy F, Guevara-Guzman R, Kendrick K (1993) Influence of birth and maternal experience on olfactory bulb neurotransmitter release. Neuroscience 56:557–565PubMedCrossRefGoogle Scholar
  60. 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 10:292–305PubMedCrossRefGoogle Scholar
  61. 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 73:553–566PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kogan JH, Frankland PW, Silva AJ (2000) Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10:47–56PubMedCrossRefGoogle Scholar
  63. Kristal MB, Graber GC (1976) Placentophagia in nonpregnant rats: influence of estrous cycle stage and birthplace. Physiol Behav 17:599–605PubMedCrossRefGoogle Scholar
  64. 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 152:585–593PubMedCrossRefGoogle Scholar
  65. 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 510:309–350PubMedCrossRefGoogle Scholar
  66. Leinders-Zufall T, Lane AP, Puche AC, Ma W, Novotny MV, Shipley MT, Zufall F (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405:792–796PubMedCrossRefGoogle Scholar
  67. 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 306:1033–1037PubMedCrossRefGoogle Scholar
  68. Levy F, Keller M (2009) Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res 200:336–345PubMedCrossRefGoogle Scholar
  69. 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 31:687–692PubMedCrossRefGoogle Scholar
  70. Lévy 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 106:427–432PubMedCrossRefGoogle Scholar
  71. 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 669:197–206PubMedCrossRefGoogle Scholar
  72. 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 57:97–104PubMedCrossRefGoogle Scholar
  73. Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735–769PubMedCrossRefGoogle Scholar
  74. Lukas M, Neumann ID (2013) Oxytocin and vasopressin in rodent behaviors related to social dysfunctions in autism spectrum disorders. Behav Brain Res 251:85–94PubMedPubMedCentralCrossRefGoogle Scholar
  75. 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 36:2159–2168PubMedPubMedCentralCrossRefGoogle Scholar
  76. 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 38:916–926PubMedCrossRefGoogle Scholar
  77. Luo M, Fee MS, Katz LC (2003) Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299:1196–1201PubMedCrossRefGoogle Scholar
  78. Luskin MB, Price JL (1983) The laminar distribution of intracortical fibers originating in the olfactory cortex of the rat. J Comp Neurol 216:292–302PubMedCrossRefGoogle Scholar
  79. 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 16:2317–2323PubMedCrossRefGoogle Scholar
  80. Mandairon N, Poncelet J, Bensafi M, Didier A (2009) Humans and mice express similar olfactory preferences. PLoS One 4:e4209PubMedPubMedCentralCrossRefGoogle Scholar
  81. 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 98:319–324PubMedCrossRefGoogle Scholar
  82. Markopoulos F, Rokni D, Gire DH, Murthy VN (2012) Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76:1175–1188PubMedPubMedCentralCrossRefGoogle Scholar
  83. Marlin BJ, Mitre M, D’Amour JA, Chao MV, Froemke RC (2015) Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520:499–504PubMedPubMedCentralCrossRefGoogle Scholar
  84. 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 148:5095–5104PubMedCrossRefGoogle Scholar
  85. 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 36:2517–2535PubMedPubMedCentralCrossRefGoogle Scholar
  86. Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer, New YorkGoogle Scholar
  87. Numan M, Numan MJ, English JB (1993) Excitotoxic amino acid injections into the medial amygdala facilitate maternal behavior in virgin female rats. Horm Behav 27:56–81PubMedCrossRefGoogle Scholar
  88. 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 90:609–621PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 49:681–687CrossRefPubMedGoogle Scholar
  90. Owen SF, Tuncdemir SN, Bader PL, Tirko NN, Fishell G, Tsien RW (2013) Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature 500:458–462PubMedPubMedCentralCrossRefGoogle Scholar
  91. 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 24:9451–9457PubMedCrossRefGoogle Scholar
  92. 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 120:925–936PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 76:6661–6665PubMedPubMedCentralCrossRefGoogle Scholar
  94. Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ Jr (1985) Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides 6:175–182CrossRefPubMedGoogle Scholar
  95. Rosenblatt JS, Lehrman D (1963) Maternal behavior of the laboratory rat. In: Rheingold HL (ed) Maternal behavior in mammals, Wiley, New York, pp 8–57Google Scholar
  96. 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 177–230Google Scholar
  97. 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 25:1904–1910PubMedPubMedCentralCrossRefGoogle Scholar
  98. Sanchez-Andrade G, Kendrick KM (2009) The main olfactory system and social learning in mammals. Behav Brain Res 200:323–335PubMedPubMedCentralCrossRefGoogle Scholar
  99. Scalia F, Winans SS (1975) The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol 161:31–55PubMedCrossRefGoogle Scholar
  100. Shamay-Tsoory SG, Abu-Akel A (2016) The social salience hypothesis of oxytocin. Biol Psychiatry 79:194–202PubMedPubMedCentralCrossRefGoogle Scholar
  101. Slotnick BM, Carpenter ML, Fusco R (1973) Initiation of maternal behavior in pregnant nulliparous rats. Horm Behav 4:53–59CrossRefGoogle Scholar
  102. 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 26:1961–1970PubMedCrossRefGoogle Scholar
  103. 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 102:16096–16101PubMedPubMedCentralCrossRefGoogle Scholar
  104. Thor DH, Holloway WR (1982) Social memory of the male laboratory rat. J Comp Physiol Psychol 96:1000–1006CrossRefGoogle Scholar
  105. Uchida N, Kepecs A, Mainen ZF (2006) Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat Rev Neurosci 7:485–491PubMedCrossRefGoogle Scholar
  106. Vaccari C, Lolait SJ, Ostrowski NL (1998) Comparative distribution of vasopressin V1b and oxytocin receptor messenger ribonucleic acids in brain. Endocrinology 139:5015–5033PubMedCrossRefGoogle Scholar
  107. 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 333:104–107PubMedPubMedCentralCrossRefGoogle Scholar
  108. Wacker DW, Ludwig M (2012) Vasopressin, oxytocin, and social odor recognition. Horm Behav 61:259–265PubMedCrossRefGoogle Scholar
  109. 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 588:4705–4717PubMedPubMedCentralCrossRefGoogle Scholar
  110. Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc Natl Acad Sci U S A 104:16681–16684PubMedPubMedCentralCrossRefGoogle Scholar
  111. Wamboldt MZ, Insel TR (1987) The ability of oxytocin to induce short latency maternal behavior is dependent on peripheral anosmia. Behav Neurosci 101:439–441CrossRefPubMedGoogle Scholar
  112. Wesson DW (2013) Sniffing behavior communicates social hierarchy. Curr Biol 23:575–580PubMedCrossRefGoogle Scholar
  113. Wesson DW, Keller M, Douhard Q, Baum MJ, Bakker J (2006) Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm Behav 49:580–586PubMedPubMedCentralCrossRefGoogle Scholar
  114. Wiesner BP, Sheard NM (1933) Maternal behaviour in the rat. Oliver and Boyd, EdinburghGoogle Scholar
  115. 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 489:491–500PubMedCrossRefGoogle Scholar
  116. 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 72:1083–1088PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Medical Faculty Mannheim, Central Institute of Mental HealthHeidelberg UniversityHeidelbergGermany

Personalised recommendations