1932

Abstract

In mammals, odor information detected by olfactory sensory neurons is converted to a topographic map of activated glomeruli in the olfactory bulb. Mitral cells and tufted cells transmit signals sequentially to the olfactory cortex for behavioral outputs. To elicit innate behavioral responses, odor signals are directly transmitted by distinct subsets of mitral cells from particular functional domains in the olfactory bulb to specific amygdala nuclei. As for the learned decisions, input signals are conveyed by tufted cells as well as by mitral cells to the olfactory cortex. Behavioral scene cells link the odor information to the valence cells in the amygdala to elicit memory-based behavioral responses. Olfactory decision and perception take place in relation to the respiratory cycle. How is the sensory quality imposed on the olfactory inputs for behavioral outputs? How are the two types of odor signals, innate and learned, processed during respiration? Here, we review recent progress on the study of neural circuits involved in decision making in the mouse olfactory system.

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2021-02-10
2024-05-06
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Literature Cited

  1. 1. 
    Mori K, Sakano H. 2011. How is the olfactory map formed and interpreted in the mammalian brain. Annu. Rev. Neurosci. 34:467–99
    [Google Scholar]
  2. 2. 
    Sakano H. 2020. Developmental regulation of olfactory circuit formation in mice. Dev. Growth Differ. 62:199–213
    [Google Scholar]
  3. 3. 
    Kepecs A, Uchida N, Mainen ZF 2006. The sniff as a unit of olfactory processing. Chem. Senses 31:167–79
    [Google Scholar]
  4. 4. 
    Mainland J, Sobel N. 2006. The sniff is part of the olfactory percept. Chem. Senses 31:181–96
    [Google Scholar]
  5. 5. 
    Mori K, Manabe H. 2014. Unique characteristics of the olfactory system. The Olfactory System K Mori 1–18 Tokyo: Springer
    [Google Scholar]
  6. 6. 
    Shusterman R, Smear MC, Koulakov AA, Rinberg D 2011. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14:1039–44
    [Google Scholar]
  7. 7. 
    Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T et al. 2007. Innate versus learned odour processing in the mouse olfactory bulb. Nature 450:503–8
    [Google Scholar]
  8. 8. 
    Igarashi KM, Ieki N, An M, Yamaguchi Y, Nagayama S et al. 2012. Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 32:7970–85
    [Google Scholar]
  9. 9. 
    Kikuta S, Fletcher ML, Homma R, Yamasoba T, Nagayama S 2013. Odorant response properties of individual neurons in an olfactory glomerular module. Neuron 77:1122–35
    [Google Scholar]
  10. 10. 
    Nagayama S, Igarashi KM, Manabe H, Mori K 2014. Parallel tufted cell and mitral cell pathways to the olfactory cortex. The Olfactory System K Mori 133–60 Tokyo: Springer
    [Google Scholar]
  11. 11. 
    Fukunaga I, Berning M, Kollo M, Schmaltz A, Schaefer AT 2012. Two distinct channels of olfactory bulb output. Neuron 75:320–29
    [Google Scholar]
  12. 12. 
    Hinds JW. 1968. Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J. Comp. Neurol. 134:287–304
    [Google Scholar]
  13. 13. 
    Bayer SA. 1983. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50:329–40
    [Google Scholar]
  14. 14. 
    Hirata T, Shioi G, Abe T, Kiyonari H, Kato S et al. 2019. A novel birthdate-labeling method reveals segregated parallel projections of mitral and external tufted cells in the main olfactory system. eNeuro 6:6 https://doi.org/10.1523/ENEURO.0234-19.2019
    [Crossref] [Google Scholar]
  15. 15. 
    Ikemoto S. 2007. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex. Brain Res. Rev. 56:27–78
    [Google Scholar]
  16. 16. 
    Murata K, Kanno M, Ieki N, Mori K, Yamaguchi M 2015. Mapping of learned odor-induced motivated behaviors in the mouse olfactory tubercle. J. Neurosci. 35:10581–99
    [Google Scholar]
  17. 17. 
    Shoenfeld TA, Macrides F. 1984. Topographic organization of connections between the main olfactory bulb and pars externa of the anterior olfactory nucleus in the hamster. J. Comp. Neurol. 227:121–35
    [Google Scholar]
  18. 18. 
    Yan Z, Tan J, Qin C, Lu Y, Ding C, Luo M 2008. Precise circuitry links bilaterally symmetric olfactory maps. Neuron 58:613–24
    [Google Scholar]
  19. 19. 
    Kikuta S, Sato K, Kashiwadani H, Tsunoda K, Yamasoba T, Mori K 2010. Neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources. PNAS 107:12363–68
    [Google Scholar]
  20. 20. 
    Mori K, Manabe H, Narikiyo K, Onisawa N 2013. Olfactory consciousness and gamma oscillation coupling across the olfactory bulb, olfactory cortex, and orbitofrontal cortex. Front. Psychol. 4:743
    [Google Scholar]
  21. 21. 
    McDonald AJ. 1998. Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 55:257–332
    [Google Scholar]
  22. 22. 
    Price JL. 2003. Comparative aspects of amygdala connectivity. Ann. N. Y. Acad. Sci. 985:50–58
    [Google Scholar]
  23. 23. 
    Matsumoto H, Kashiwadani H, Nagao H, Aiba A, Mori K 2009. Odor-induced persistent discharge of mitral cells in the mouse olfactory bulb. J. Neurophysiol. 101:1890–900
    [Google Scholar]
  24. 24. 
    Patterson MA, Lagier S, Carleton A 2013. Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage. PNAS 110:E3340–49
    [Google Scholar]
  25. 25. 
    Janak PH, Tye KM. 2015. From circuits to behavior in the amygdala. Nature 517:284–92
    [Google Scholar]
  26. 26. 
    Phelps EA, LeDoux JE. 2005. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–87
    [Google Scholar]
  27. 27. 
    O'Neill PK, Gore F, Salzman CD 2018. Basolateral amygdala circuitry in positive and negative valence. Curr. Opin. Neurobiol. 49:175–83
    [Google Scholar]
  28. 28. 
    Alheid GF, de Olmos JS, Beltramino CS 1995. Amygdala and extended amygdala. The Rat Nervous System G Paxinos 443–93 San Diego: Academic. , 2nd. ed.
    [Google Scholar]
  29. 29. 
    Kevetter GA, Winans SS. 1981. Connections of the corticomedial amygdala in the golden hamster. II. Efferents of the “olfactory amygdala. .” J. Comp. Neurol. 197:99–111
    [Google Scholar]
  30. 30. 
    Santiago AC, Shammah-Lagnado SJ. 2004. Efferent connections of the nucleus of the lateral olfactory tract in the rat. J. Comp. Neurol. 471:314–32
    [Google Scholar]
  31. 31. 
    Yoshida I, Mori K. 2007. Odorant category profile selectivity of olfactory cortex neurons. J. Neurosci. 27:9105–14
    [Google Scholar]
  32. 32. 
    Shiotani K, Tanisumi Y, Murata K, Hirokawa J, Sakurai Y, Manabe H 2020. Tuning of olfactory cortex ventral tenia tecta neurons to distinct task elements of goal-directed behavior. eLife 9:e57268
    [Google Scholar]
  33. 33. 
    Root CM, Denny CA, Hen R, Axel R 2014. The participation of cortical amygdala in innate, odour-driven behaviour. Nature 515:269–73
    [Google Scholar]
  34. 34. 
    Johnson DM, Illig KR, Behan M, Haberly LB 2000. New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that “primary” olfactory cortex functions like “association” cortex in other sensory systems. J. Neurosci. 20:6974–82
    [Google Scholar]
  35. 35. 
    Neville KR, Haberly LB. 2004. Olfactory cortex. The Synaptic Organization of the Brain GM Shepherd 415–54 New York: Oxford Univ. Press
    [Google Scholar]
  36. 36. 
    Franks KM, Russo MJ, Sosulski DL, Mulligan AA, Siegelbaum SA, Axel R 2011. Recurrent circuitry dynamically shapes the activation of piriform cortex. Neuron 72:49–56
    [Google Scholar]
  37. 37. 
    Bekkers JM, Suzuki N. 2013. Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci 36:429–38
    [Google Scholar]
  38. 38. 
    Sakmann B. 2017. From single cells and single columns to cortical networks: dendritic excitability, coincidence detection and synaptic transmission in brain slices and brains. Exp. Physiol. 102.5:489–521
    [Google Scholar]
  39. 39. 
    Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M et al. 2003. Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302:2088–94
    [Google Scholar]
  40. 40. 
    Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A et al. 1996. Visualizing an olfactory sensory map. Cell 87:675–86
    [Google Scholar]
  41. 41. 
    Malnic B, Hirono J, Sato T, Buck LB 1999. Combinatorial receptor codes for odors. Cell 96:713–23
    [Google Scholar]
  42. 42. 
    Mori K, Nagao H, Yoshihara Y 1999. The olfactory bulb: coding and processing of odor molecule information. Science 286:711–15
    [Google Scholar]
  43. 43. 
    Sakano H. 2010. Neural map formation in the mouse olfactory system. Neuron 67:530–42
    [Google Scholar]
  44. 44. 
    Chesler AT, Zou DJ, Le Pichon CE, Peterlin ZA, Matthews GA et al. 2007. A G protein/cAMP signal cascade is required for axonal convergence into olfactory glomeruli. PNAS 104:1039–44
    [Google Scholar]
  45. 45. 
    Dal Col JA, Matsuo T, Storm DR, Rodriguez I 2007. Adenylyl cyclase-dependent axonal targeting in the olfactory system. Development 134:2481–89
    [Google Scholar]
  46. 46. 
    Imai T, Suzuki M, Sakano H 2006. Odorant receptor-derived cAMP signals direct axonal targeting. Science 314:657–61
    [Google Scholar]
  47. 47. 
    Imai T, Yamazaki T, Kobayakawa R, Kobayakawa K, Abe T et al. 2009. Pre-target axon sorting establishes the neural map topography. Science 325:585–90
    [Google Scholar]
  48. 48. 
    Kobilka BK, Deupi X. 2007. Conformational complexity of G-protein coupled receptors. Trends Pharmacol. Sci. 28:397–406
    [Google Scholar]
  49. 49. 
    Rasmussen SG, Choi HJ, Fung JJ, Pardon E, Casarosa P et al. 2011. Structure of a nanobody-stabilized active state of the β2 adrenoceptor. Nature 469:175–80
    [Google Scholar]
  50. 50. 
    Rasmussen SG, DeVree BT, Zou Y, Kruse AC, Chung KY et al. 2011. Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477:549–55
    [Google Scholar]
  51. 51. 
    Nakashima A, Takeuchi H, Imai T, Saito H, Kiyonari H et al. 2013. Agonist-independent GPCR activity regulates axon targeting of olfactory sensory neurons. Cell 154:1314–25
    [Google Scholar]
  52. 52. 
    Yu CR, Power J, Barnea G, O'Donnell S, Brown HE et al. 2004. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553–66
    [Google Scholar]
  53. 53. 
    Astic L, Saucier D, Holley A 1987. Topographical relationships between olfactory receptor cells and glomerular foci in the rat olfactory bulb. Brain Res 424:144–52
    [Google Scholar]
  54. 54. 
    Miyamichi K, Serizawa S, Kimura HM, Sakano H 2005. Continuous and overlapping expression domains of odorant receptor genes in the olfactory epithelium determine the dorsal/ventral positioning of glomeruli in the olfactory bulb. J. Neurosci. 25:3586–92
    [Google Scholar]
  55. 55. 
    Cloutier JF, Giger RJ, Koentges G, Dulac C, Kolodkin AL, Ginty DD 2002. Neuropilin-2 mediates axonal fasciculation, zonal segregation, but not axonal convergence, of primary accessory olfactory neurons. Neuron 33:877–92
    [Google Scholar]
  56. 56. 
    Walz A, Rodriguez I, Mombaerts P 2002. Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice. J. Neurosci. 22:4025–35
    [Google Scholar]
  57. 57. 
    Nguyen-Ba-Charvet KT, Di Meglio T, Fouquet C, Chedotal A 2008. Robos and slits control the pathfinding and targeting of mouse olfactory sensory axons. J. Neurosci. 28:4244–49
    [Google Scholar]
  58. 58. 
    Aoki M, Takeuchi H, Nakashima A, Nishizumi H, Sakano H 2013. Possible roles of robo1+ ensheathing cells in guiding dorsal-zone olfactory sensory neurons in mouse. Dev. Neurobiol. 73:828–40
    [Google Scholar]
  59. 59. 
    Cho JH, Lepine M, Andrews W, Parnavelas J, Cloutier JF 2007. Requirement for Slit-1 and Robo-2 in zonal segregation of olfactory sensory neuron axons in the main olfactory bulb. J. Neurosci. 27:9094–104
    [Google Scholar]
  60. 60. 
    Norlin EM, Alenius M, Gussing F, Hägglund M, Vedin V, Bohm S 2001. Evidence for gradients of gene expression correlating with zonal topography of the olfactory sensory map. Mol. Cell. Neurosci. 18:283–95
    [Google Scholar]
  61. 61. 
    Takeuchi H, Inokuchi K, Aoki M, Suto F, Tsuboi A et al. 2010. Sequential arrival and graded secretion of Sema3F by olfactory neuron axons specify map topography at the bulb. Cell 141:1056–67
    [Google Scholar]
  62. 62. 
    Zhao H, Reed RR. 2001. X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104:651–60
    [Google Scholar]
  63. 63. 
    Serizawa S, Miyamichi K, Takeuchi H, Yamagishi Y, Suzuki M, Sakano H 2006. A neuronal identity code for the odorant receptor-specific and activity-dependent axon sorting. Cell 127:1057–69
    [Google Scholar]
  64. 64. 
    Kaneko-Gotoh T, Yoshihara S, Miyazaki H, Yoshihara Y 2008. BIG-2 mediates olfactory axon convergence to target glomeruli. Neuron 57:834–46
    [Google Scholar]
  65. 65. 
    Reisert J. 2010. Origin of basal activity in mammalian olfactory receptor neurons. J. Gen. Physiol. 136:529–40
    [Google Scholar]
  66. 66. 
    Lorenzon P, Redolfi N, Podolsky MJ, Zamparo I, Franchi SA et al. 2015. Circuit formation and function in the olfactory bulb of mice with reduced spontaneous afferent activity. J. Neurosci. 35:146–60
    [Google Scholar]
  67. 67. 
    Nakashima A, Ihara N, Shigeta M, Kiyonari H, Ikegaya Y, Takeuchi H 2019. Structured spike series specify gene expression patterns for olfactory circuit formation. Science 365:eaaw5030
    [Google Scholar]
  68. 68. 
    Inoue N, Nishizumi H, Naritsuka H, Kiyonari H, Sakano H 2018. Sema7A/PlxnC1 signaling triggers activity-dependent olfactory synapse formation. Nat. Commun. 9:1842
    [Google Scholar]
  69. 69. 
    Inoue N, Sakano H. 2018. Sema7A signaling is essential for activity-dependent synapse formation in the mouse olfactory bulb. J. Neurol. Neuromed. 3:33–38
    [Google Scholar]
  70. 70. 
    Jiang Y, Gong NN, Hu XS, Ni MJ, Pasi R, Matsunami H 2015. Molecular profiling of activated olfactory neurons identifies odorant receptors for odors in vivo. Nat. Neurosci 18:1446–54
    [Google Scholar]
  71. 71. 
    von der Weid B, Rossier D, Lindup M, Tuberosa J, Widmer A et al. 2015. Large-scale transcriptional profiling of chemosensory neurons identifies receptor-ligand pairs in vivo. Nat. Neurosci. 18:1455–63
    [Google Scholar]
  72. 72. 
    Xu L, Li W, Voleti V, Zou DJ, Hillman EMC, Firestein S 2020. Widespread receptor-driven modulation in peripheral olfactory coding. Science 368:eaaz5390
    [Google Scholar]
  73. 73. 
    Matsumoto H, Kobayakawa K, Kobayakawa R, Tashiro T, Mori K et al. 2010. Spatial arrangement of glomerular molecular-feature clusters in the odorant-receptor class domains of the mouse olfactory bulb. J. Neurophysiol. 103:3490–500
    [Google Scholar]
  74. 74. 
    Saito H, Nishizumi H, Suzuki S, Matsumoto H, Ieki N et al. 2017. Immobility responses are induced by photoactivation of single glomerular species responsive to fox odour TMT. Nat. Commun. 8:16011
    [Google Scholar]
  75. 75. 
    Smear M, Resulaj A, Zhang J, Bozza T, Rinberg D 2013. Multiple perceptible signals from a single olfactory glomerulus. Nat. Neurosci. 16:1687–91
    [Google Scholar]
  76. 76. 
    Keller A, Zhuang H, Chi Q, Vosshall LB, Matsunami H 2007. Genetic variation in a human odorant receptor alters odor perception. Nature 499:486–72
    [Google Scholar]
  77. 77. 
    Lin DY, Zhang SZ, Block E, Katz LC 2005. Encoding social signals in the mouse main olfactory bulb. Nature 434:470–77
    [Google Scholar]
  78. 78. 
    Yoshikawa K, Nakagawa H, Mori N, Watanabe H, Touhara K 2013. An unsaturated aliphatic alcohol as a natural ligand for a mouse odorant receptor. Nat. Chem. Biol. 9:160–62
    [Google Scholar]
  79. 79. 
    Duan X, Block E, Li Z, Connelly T, Zhang J et al. 2012. Crucial role of copper in detection of metal-coordinating odorants. PNAS 109:3492–97
    [Google Scholar]
  80. 80. 
    Horio N, Murata K, Yoshikawa K, Yoshihara Y, Touhara K 2019. Contribution of individual olfactory receptors to odor-induced attractive or aversive behavior in mice. Nat. Commun. 14:209
    [Google Scholar]
  81. 81. 
    Day HE, Masini CV, Campeau S 2004. The pattern of brain c-fos mRNA induced by a component of fox odor; 2,5-dihydro-2,4,5-trimethylthiazoline (TMT), in rats, suggests both systemic and processive stress characteristics. Brain Res 1025:139–51
    [Google Scholar]
  82. 82. 
    Miyamichi K, Amat F, Moussavi F, Wang C, Wickersham I et al. 2011. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472:191–96
    [Google Scholar]
  83. 83. 
    Lehman MN, Winans SS, Powers JN 1980. Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. Science 210:557–60
    [Google Scholar]
  84. 84. 
    Inokuchi K, Imamura F, Takeuchi H, Kim R, Okuno H et al. 2017. Nrp2 is sufficient to instruct circuit formation of mitral-cells to mediate odour-induced attractive social responses. Nat. Commun. 8:15977
    [Google Scholar]
  85. 85. 
    Imamura F, Ayoub AE, Rakic P, Greer CA 2011. Timing of neurogenesis is a determinant of olfactory circuitry. Nat. Neurosci. 14:331–37
    [Google Scholar]
  86. 86. 
    Nishizumi H, Miyashita A, Inoue N, Inokuchi K, Aoki M, Sakano H 2019. Primary dendrites of mitral cells synapse unto neighboring glomeruli independent of their odorant receptor identity. Commun. Biol. 2:14
    [Google Scholar]
  87. 87. 
    Nishizumi H, Kumasaka K, Inoue N, Nakashima A, Sakano H 2007. Deletion of the core-H region in mice abolishes the expression of three proximal odorant receptor genes in cis. . PNAS 104:20067–72
    [Google Scholar]
  88. 88. 
    Kondoh K, Lu Z, Ye X, Olson DP, Lowell DD, Buck LB 2016. A specific area of olfactory cortex involved in stress hormone responses to predator odors. Nature 532:103–6
    [Google Scholar]
  89. 89. 
    Hensch TK. 2005. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6:877–88
    [Google Scholar]
  90. 90. 
    Espinosa JS, Stryker MP. 2012. Development and plasticity of the primary visual cortex. Neuron 75:230–49
    [Google Scholar]
  91. 91. 
    Wiesel TN, Hubel DH. 1963. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26:1003–17
    [Google Scholar]
  92. 92. 
    Horn G. 2004. Pathways of the past: the imprint of memory. Nat. Rev. Neurosci. 5:108–20
    [Google Scholar]
  93. 93. 
    Nevitt GA, Dittman AH, Quinn TP, Moody WJ Jr 1994. Evidence for a peripheral olfactory memory in imprinted salmon. PNAS 91:4288–49
    [Google Scholar]
  94. 94. 
    Leung CT, Coulombe PA, Reed RR 2007. Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat. Neurosci. 10:720–26
    [Google Scholar]
  95. 95. 
    Ma L, Wu Y, Qiu Q, Scheerer H, Moran A, Yu CR 2014. A developmental switch of axon targeting in the continuously regenerating mouse olfactory system. Science 344:194–97
    [Google Scholar]
  96. 96. 
    Tsai L, Barnea G. 2014. A critical period defined by axon-targeting mechanisms in the murine olfactory bulb. Science 344:197–200
    [Google Scholar]
  97. 97. 
    Geramita M, Urban NN. 2016. Postnatal odor exposure increases the strength of interglomerular lateral inhibition onto olfactory bulb tufted cells. J. Neurosci. 36:12321–27
    [Google Scholar]
  98. 98. 
    Liu A, Savya S, Urban NN 2016. Early odorant exposure increases the number of mitral and tufted cells associated with a single glomerulus. J. Neurosci. 36:11646–53
    [Google Scholar]
  99. 99. 
    Liu A, Urban NN. 2017. Prenatal and early postnatal odorant exposure heightens odor-evoked mitral cell responses in the mouse olfactory bulb. eNeuro 4: https://doi.org/10.1523/ENEURO.0129-17.2017
    [Crossref] [Google Scholar]
  100. 100. 
    Logan DW, Brunet LJ, Webb WR, Cutforth T, Ngai J, Stowers L 2012. Learned recognition of maternal signature odors mediates the first suckling episode in mice. Curr. Biol. 22:1998–2007
    [Google Scholar]
  101. 101. 
    Mennella JA, Jagnow CP, Beauchamp GK 2001. Prenatal and postnatal flavor learning by human infants. Pediatrics 107:6e88
    [Google Scholar]
  102. 102. 
    Sullivan RM, Landers M, Yeaman B, Wilson DA 2000. Good memories of bad events in infancy. Nature 407:38–39
    [Google Scholar]
  103. 103. 
    Anderson KE. 2000. Neurotransmitters: central and peripheral mechanisms. Int. J. Impot. Res. 4:S26–33
    [Google Scholar]
  104. 104. 
    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 76:377–86
    [Google Scholar]
  105. 105. 
    Bosch OJ, Young LJ. 2018. Oxytocin and social relationships: From attachment to bond disruption. Curr. Top. Behav. Neurosci. 35:97–117
    [Google Scholar]
  106. 106. 
    Muscatelli F, Desarménien MG, Matarazzo V, Grinevich V 2018. Oxytocin signaling in the early life of mammals: link to neurodevelopmental disorders associated with ASD. Curr. Top. Behav. Neurosci. 35:239–68
    [Google Scholar]
  107. 107. 
    Sannino S, Chini B, Grinevich V 2017. Lifespan oxytocin signaling: maturation, flexibility, and stability in newborn, adolescent, and aged brain. Dev. Neurobiol. 77:158–68
    [Google Scholar]
  108. 108. 
    Nishimori K, Young LJ, Guo Q, Wang Z, Insel TR, Matzuk MM 1996. Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. PNAS 93:11699–704
    [Google Scholar]
  109. 109. 
    Takayanagi T, Yoshida M, Bielsky IF, Ross HE, Kawamata M et al. 2005. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. PNAS 102:16096–101
    [Google Scholar]
  110. 110. 
    Jefferis GS, Marin EC, Stocker RF, Luo L 2001. Target neuron specifications in the olfactory map of Drosophila. . Nature 414:204–8
    [Google Scholar]
  111. 111. 
    Hong W, Luo L. 2014. Genetic control of wiring specificity in the fly olfactory system. Genetics 196:17–29
    [Google Scholar]
  112. 112. 
    Liberles SD. 2015. Trace amine-associated receptors: ligands, neural circuits, and behaviors. Curr. Opin. Neurobiol. 34:1–7
    [Google Scholar]
  113. 113. 
    Dewan A, Pacifico R, Zhan R, Rinberg D, Bozza T 2013. Non-redundant coding of aversive odours in the main olfactory pathway. Nature 497:486–89
    [Google Scholar]
  114. 114. 
    Pashkovski SL, Iuriilli G, Brann D, Chicharro D, Drummey K et al. 2020. Structure and flexibility in cortical representations of odour space. Nature 583:253–58
    [Google Scholar]
  115. 115. 
    Chong E, Moroni M, Wilson C, Shoham S, Panzeri S, Rinberg D 2020. Manipulating synthetic optogenetic odors reveals the coding logic of olfactory perception. Science 368:1329–37
    [Google Scholar]
  116. 116. 
    Josselyn S, Tonegawa S. 2020. Memory engrams: recalling the past and imaging the future. Science 367:eaaw4325
    [Google Scholar]
  117. 117. 
    Redondo RL, Kim J, Arons AL, Ramirez S, Liu X, Tonegawa S 2014. Bidirectional switch of the valence associated with a hippocampal contextual memory engram. Nature 513:426–30
    [Google Scholar]
  118. 118. 
    Gore F, Schwartz EC, Brangers BC, Aladi S, Stujenske JM et al. 2015. Neural representations of unconditioned stimuli in basolateral amygdala mediate innate and learned responses. Cell 162:13445
    [Google Scholar]
  119. 119. 
    Iurilli G, Datta SR. 2017. Population coding in an innately relevant olfactory area. Neuron 93:1180–97
    [Google Scholar]
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