Skip to main content

Advertisement

Log in

Forever young: Neoteny, neurogenesis and a critique of critical periods in olfaction

  • Mini-Review
  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

The critical period concept has been one of the most transcendent in science, education, and society forming the basis of our fixation on ‘quality’ of childhood experiences. The neural basis of this process has been revealed in developmental studies of visual, auditory and somatosensory maps and their enduring modification through manipulations of experience early in life. Olfaction, too, possesses a number of phenomena that share key characteristics with classical critical periods like sensitive temporal windows and experience dependence. In this review, we analyze the candidate critical period-like phenomena in olfaction and find them disanalogous to classical critical periods in other sensory systems in several important ways. This leads us to speculate as to why olfaction may be alone among exteroceptive systems in lacking classical critical periods and how life-long neurogenesis of olfactory sensory neurons and bulbar interneurons—a neotenic vestige-- relates to the structure and function of the mammalian olfactory system.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

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  CAS  PubMed  Google Scholar 

  • Antonini A, Stryker MP (1993) Rapid remodeling of axonal arbors in the visual cortex. Science 260(5115):1819–1821

    Article  CAS  PubMed  Google Scholar 

  • Bergan JF, Ro P, Ro D, Knudsen EI (2005) Hunting increases adaptive auditory map plasticity in adult barn owls. J Neurosci 25:9816–9820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brainard MS, Knudsen EI (1998) Sensitive periods for visual calibration of the auditory space map in the barn owl optic tectum. J Neurosci 18:3929–3942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breton-Provencher V, Lemasson M, Peralta MR 3rd, Saghatelyan A (2009) Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci 29:15245–15257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown CE, Li P, Boyd JD, Delaney KR, Murphy TH (2007) Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J Neurosci 27:4101–4109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bushdid C, Magnasco MO, Vosshall LB, Keller A (2014) Humans can discriminate more than 1 trillion olfactory stimuli. Science 343:1370–1372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cadiou H, Aoudé I, Tazir B, Molinas A, Fenech C, Meunier N, Grosmaitre X (2014) Postnatal odorant exposure induces peripheral olfactory plasticity at the cellular level. J Neurosci 34(14):4857–4870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang EF, Merzenich MM (2003) Environmental noise retards auditory cortical development. Science 300(5618):498–502

    Article  CAS  PubMed  Google Scholar 

  • Chater TE, Goda Y (2014) The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity. Front Cell Neurosci 8:401

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheetham CE, Belluscio L (2014) An olfactory critical period. Science 344:157–158

    Article  CAS  PubMed  Google Scholar 

  • Cheetum CEJ, Park U, Beluscio L (2016) Rapid and continuous activity-dependent plasticity of olfactory sensory input. Nature Com 7:10729

    Article  CAS  Google Scholar 

  • Coppola DM (2012) Studies of olfactory system neural plasticity: the contribution of the unilateral naris occlusion technique. Neural Plasticity 2012:1–14. https://doi.org/10.1155/2012/351752

    Article  Google Scholar 

  • Coppola DM, Ritchie BR, Craven BA (2017) Tests of the sorption and olfactory ‘fovea’ hypotheses in the mouse. J Neurophys 118:2770–2788

    Article  CAS  Google Scholar 

  • Coppola DM, Waggener C (2012) The effects of unilateral naris occlusion on gene expression profiles in mouse olfactory mucosa. J Mol Neurosci 47(3):604–618

    Article  CAS  PubMed  Google Scholar 

  • Coppola DM, Waggener CT, Radwani SM, Brooks DA (2013) An electroolfactogram study of odor response patterns from the mouse olfactory epithelium with reference to receptor zones and odor sorptiveness. J Neurophys 109(8):2179–2191

    Article  CAS  Google Scholar 

  • Dalton P (2004) Olfaction and anosmia in rhinosinusitis. Cur All Asth Rep 4:230–236

    Article  Google Scholar 

  • de Villers-Sidani E, Chang EF, Bao S, Merzenich MM (2007) Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J Neurosci 27(1):180–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24(38):8354–8365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erzurumlu RS, Gaspar P (2012) Development and critical period plasticity of the barrel cortex. Eur J Neurosci 35(10):1540–1553

    Article  PubMed  PubMed Central  Google Scholar 

  • Franks K, Isaacson JS (2005) Synapse-specific downregulation of NMDA receptors by early experience: a critical period for plasticity of sensory input to olfactory cortex. Neuron 47:101–114

    Article  CAS  PubMed  Google Scholar 

  • Furudono Y, Sone Y, Takizawa K, Hirono J, Sato T (2009) Relationship between peripheral receptor code and perceived odor quality. Chem Senses 34(2):151–158

    Article  PubMed  Google Scholar 

  • Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438

    Article  CAS  PubMed  Google Scholar 

  • Graziadei PP, Graziadei GA (1979) Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neurons. J Neurocytol 8:1–18

    Article  CAS  PubMed  Google Scholar 

  • Greifzu F, Pielecka-Fortuna J, Kalogeraki E, Krempler K, Favaro PD, Schluter OM, Lowel S (2014) Environmental enrichment extends ocular dominance plasticity into adulthood and protects from stroke-induced impairments of plasticity. Proc Natl Acad Sci U S A 111:1150–1155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grelat A, Benoit L, Wagner S, Moigneu C, Lledo PM, Alonso M (2018) Adult-born neurons boost odor-reward association. Proc Natl Acad Sci U S A 115(10):2514–2519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haberly LB (1998) Olfactory cortex. In: Shepherd GM (ed) The synaptic Organization of the Brain. Oxford University Press, New York, pp 377–416

    Google Scholar 

  • Harlow HF, Zimmermann RR (1959) Affectional responses in the infant monkey. Science 130(3373):421–432

    Article  CAS  PubMed  Google Scholar 

  • He HY, Hodos W, Quinlan EM (2006) Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. J Neurosci 26:2951–2955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He HY, Ray B, Dennis K, Quinlan EM (2007) Experience-dependent recovery of vision following chronic deprivation amblyopia. Nat Neurosci 10:1134–1136

    Article  CAS  PubMed  Google Scholar 

  • Hensch TK (2004) Critical period regulation. Annu Rev Neurosci 27:549–579

    Article  CAS  PubMed  Google Scholar 

  • Hinds JW, Hinds PL, McNelly NA (1984) An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors. Anat Rec 210:375–383

    Article  CAS  PubMed  Google Scholar 

  • Holl A (2018) Survival of mature mouse olfactory sensory neurons labeled genetically perinatally. Mol Cell Neurosci 88:258–269. https://doi.org/10.1016/j.mcn.2018.02.005

    Article  CAS  PubMed  Google Scholar 

  • Huang EJ, Reichart LF (2001) Neurotrophins: roles in neurodevelopment and function. Annu Rev Neurosci 24:677–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubel DH, Wiesel TN (1998) Early exploration of the visual cortex. Neuron 20(3):401–412

    Article  CAS  PubMed  Google Scholar 

  • Hubel DH, Wiesel TN (2005) Brain and visual perception: the story of a 25-year collaboration. Oxford University Press, Oxford

    Google Scholar 

  • Hubener M, Bonhoeffer T (2014) Neuronal plasticity: beyond the critical period. Cell 159:727–737

    Article  CAS  PubMed  Google Scholar 

  • Kandel ER, Dudai Y, Mayford MR (2014) The molecular and systems biology of memory. Cell 157:163–186

    Article  CAS  PubMed  Google Scholar 

  • Kaschube M, Schnabel M, Löwel S, Coppola DM, White LE, Wolf F (2010) Universality in the evolution of orientation columns in the visual cortex. Science 330(6007):1113–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaslin J, Ganz J, Brand M (2008) Proliferation, neurogenesis and regeneration in the non mammalian vertebrate brain. Phil Trans R Soc B 363:101–122

    Article  PubMed  Google Scholar 

  • Kass MD, Guang SA, Moberly AH, McGann JP (2016) Changes in olfactory sensory neuron physiology and olfactory perceptual learning after odorant exposure in adult mice. Chem Senses 41(2):123–133

    CAS  PubMed  Google Scholar 

  • Kelsch W, Lin C, Mosley CP, Lois C (2009) A critical period for activity-dependent synaptic development during olfactory bulb adult neurogenesis. J Neurosci 29:1852–11858

    Article  CAS  Google Scholar 

  • Kempermann G, Gage FH, Aigner L, Song H, Curtis MA, Thuret S, Kuhn HG, Jessberger S, Frankland PW, Cameron HA, Gould E, Hen R, Abrous DN, Toni N, Schinder AF, Zhao X, Lucassen PL, Frisé J (2018) Human adult neurogenesis: evidence and remaining questions. Cell Stem Cell 23:1–6

    Article  CAS  Google Scholar 

  • Khan M, Vaes E, Mombaerts P (2013) Temporal patterns of odorant receptor gene expression in adult and aged mice. Mol Cell Neurosci 57:120–129

    Article  CAS  PubMed  Google Scholar 

  • Kikuta S, Sakamoto T, Nagayama S, Kanaya K, Kinoshita M, Kondo K, Tsunoda K, Mori K, Yamasoba T (2015) Sensory deprivation disrupts homeostatic regeneration of newly generated olfactory sensory neurons after injury in adult mice. J Neurosci 35:2657–2673

    Article  PubMed  PubMed Central  Google Scholar 

  • Knudsen EI (1998) Capacity for plasticity in the adult owl auditory system expanded by juvenile experience. Science 279:1531–1533

    Article  CAS  PubMed  Google Scholar 

  • Krawl A (2013) Auditory critical period: a review from system’s perspective. Neurosci 247:117–133

    Article  CAS  Google Scholar 

  • Laska M (2017) Human and animal olfactory capabilities compared. In: Buettner A (ed) Handbook of Odor. Springer, New York, pp 675–689

    Google Scholar 

  • Lledo P, Saghatelyan A (2005) Integrating new neurons into the adult olfactory bulb: joining the network, life–death decisions, and the effects of sensory experience. Trends Neurosci 28(5):248–254

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Fitzpatrick D, White LE (2006) The development of direction selectivity in ferret visual cortex requires early visual experience. Nature Neurosci 9:676–681

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Van Hooser SD, Mazurek M, White LE, Fitzpatrick D (2008) Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456:952–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu A, Urban NN (2017) Prenatal and early postnatal odorant exposure heightens odor-evoked mitral cell responses in the mouse olfactory bulb. eNeuro 4:ENEURO.0129–ENEU17.2017. https://doi.org/10.1523/ENEURO.0129-17.2017

    Article  Google Scholar 

  • Lo SQ, Sng JCG, Augstine GJ (2017) Defining a critical period for inhibitory circuits within the somatosensory cortex. Sci Rep 7:7271. https://doi.org/10.1038/s41598-017-07400-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148

    Article  CAS  PubMed  Google Scholar 

  • Lorenz K (1958) The evolution of behavior. Sci Amer 199(6):67–82

  • 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(6180):194–197

    Article  CAS  PubMed  Google Scholar 

  • Marks CA, Cheng K, Cummings DM, Belluscio L (2006) Activity-dependent plasticity in the olfactory intrabulbar map. J Neurosci 26(44):11257–11266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matthies U, Balog J, Lehmann K (2013) Temporally coherent visual stimuli boost ocular dominance plasticity. J Neurosci 33:11774–11778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meister M (2015) On the dimensionality of odor space. eLife 4:e07865

    Article  PubMed  PubMed Central  Google Scholar 

  • Merzenich MM, Nelson RJ, Stryker MP, Cynader MS, Schoppmann A, Zook JM (1984) Somatosensory cortical map changes following digit amputation in adult monkeys. J Comp Neurol 224:591–605

    Article  CAS  PubMed  Google Scholar 

  • Miyazaki K, Ogawa Y (2006) Learning absolute pitch by children: a cross-sectional study. Music Percept 24(1):63–78

    Article  Google Scholar 

  • Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87(4):675–686

    Article  CAS  PubMed  Google Scholar 

  • Morales B, Choi SY, Kirkwood A (2002) Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci 22(18):8084–8090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno MM, Linster C, Escanilla O, Sacquet J, Didier A, Mandairon N (2009) Olfactory perceptual learning requires adult neurogenesis. Proc Natl Acad Sci U S A 106(42):17980–17985

    Article  PubMed  PubMed Central  Google Scholar 

  • Moriceau S, Sullivan RM (2005) Neurobiology of infant attachment. Dev Psychobiol 47(3):230–242

    Article  PubMed  PubMed Central  Google Scholar 

  • Mower GD (1991) The effect of dark rearing on the time course of the critical period in cat visual cortex. Brain Res Dev Brain Res 58(2):151–158

    Article  CAS  PubMed  Google Scholar 

  • Penfield W, Roberts L (1959) Speech and brain mechanisms. Princeton University Press. Princeton, New Jersey, USA. pp. 286

  • Petreanu L, Alvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22(14):6106–6113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinker S (1994) The language instinct. HarperCollins, New York, NY, USA

    Book  Google Scholar 

  • Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298(5596):1248–1251

    Article  CAS  PubMed  Google Scholar 

  • Poo C, Isaacon JS (2007) An early critical period for long-term plasticity and structural modification of sensory synapses in olfactory cortex. J Neurosci 27:7553–7558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sailor KA, Schinder AF, Lledo PM (2017) Adult neurogenesis beyond the niche: its potential for driving brain plasticity. Curr Opin Neurobiol 42:111–117

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto M, Imayoshi I, Ohtsuka T, Yamaguchi M, Mori K, Kageyama R (2011) Continuous neurogenesis in the adult forebrain is required for innate olfactory responses. Proc Natl Acad Sci U S A 108:8479–8484

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478(7369):382–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawtell NB, Frenkel MY, Philpot BD, Nakazawa K, Tonegawa S, Bear MF (2003) NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38:977–985

    Article  CAS  PubMed  Google Scholar 

  • Schoenfeld TA, Marchand JE, Macrides F (1985) Topographic organization of tufted cell axonal projections in the hamster main olfactory bulb: an intrabulbar associational system. J Comp Neurol 235:503–518

    Article  CAS  PubMed  Google Scholar 

  • Seay B, Alexander BK, Harlow HF (1964) Maternal behavior of socially deprived rhesus monkeys. J Abn Soc Psychol 69:345–354

    Article  CAS  Google Scholar 

  • Sorrells SF, Paredes MF, Cebrian-Silla A, Sandoval K, Qi D, Kelley KW, James D, Mayer S, Chang J, Auguste KI, Chang EF, Gutierrez AJ, Kriegstein AR, Mathern GW, Oldham MC, Huang EJ, Garcia-Verdugo JM, Yang Z, Alvarez-Buylla A (2018) Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature 555:377–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeuchi H, Sakano H (2014) Neural map formation in the mouse olfactory system. Cell Mol Life Sci 71(16):3049–3057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trachtenberg JT, Stryker MP (2001) Rapid anatomical plasticity of horizontal connections in the developing visual cortex. J Neurosci 21(10):3476–3482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai L, Barnea G (2014) A critical period defined by axon-targeting mechanisms in the murine olfactory bulb. Science 344(6180):197–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van der Loos H, Woolsey TA (1973) Somatosensory cortex: structural alterations following early injury to sense organs. Science 179:395–398

    Article  PubMed  Google Scholar 

  • Van Hooser SD, Li Y, Christensson M, Smith G, White LE, Fitzpatrick D (2012) Initial neighborhood biases and the quality of motion stimulation jointly influence the rapid emergence of direction preference in visual cortex. J Neurosci 32:7258–7266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watt WC, Sakano H, Lee ZY, Reusch JE, Trinh K, Storm DR (2004) Odorant stimulation enhances survival of olfactory sensory neurons via MAPK and CREB. Neuron 41(6):955–967

    Article  CAS  PubMed  Google Scholar 

  • White LE, Coppola DM, Fitzpatrick D (2001) The contribution of sensory experience to the development of orientation maps in ferret visual cortex. Nature 411:1049–1052

    Article  CAS  PubMed  Google Scholar 

  • White LE, Fitzpatrick D (2007) Vision and cortical map development. Neuron 56(2):327–338

    Article  CAS  PubMed  Google Scholar 

  • Woolsey TA, Wann JR (1976) Areal changes in mouse cortical barrels following vibrissal damage at different postnatal ages. J Comp Neurol 170:53–66

    Article  CAS  PubMed  Google Scholar 

  • Yamaguci M, Mori K (2005) Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. PNAS (USA) 102:9697–9702

    Article  CAS  Google Scholar 

  • Yang T, Maunsell JHR (2004) The effect of perceptual learning on neuronal responses in monkey visual area V4. J Neurosci 24:1617–1626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42(4):553–566

    Article  CAS  PubMed  Google Scholar 

  • Zenke F, Gerstner W (2017) Hebbian plasticity requires compensatory processes on multiple timescales. Phil Trans R Soc B 372:20160259

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang LI, Bao S, Merzenich MM (2002) Disruption of primary auditory cortex by synchronous auditory inputs during a critical period. Proc Natl Acad Sci U S A 99(4):2309–2314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Panizzutti R, de Villers-Sidani E, Madeira C, Merzenich MM (2011) Natural restoration of critical period plasticity in the juvenile and adult primary auditory cortex. J Neurosci 31(15):5625–5634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the National Science Foundation (United States) [grant number IOS-1655113 to D.M.C.]

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David M. Coppola.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Coppola, D.M., White, L.E. Forever young: Neoteny, neurogenesis and a critique of critical periods in olfaction. J Bioenerg Biomembr 51, 53–63 (2019). https://doi.org/10.1007/s10863-018-9778-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10863-018-9778-4

Keywords

Navigation