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Forever Young: Neoteny, Neurogenesis and a Critique of Critical Periods in Olfaction David M. Coppola & Leonard E. White

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Forever Young: Neoteny, Neurogenesis and a Critique of Critical Periods in Olfaction David M. Coppola & Leonard E. White Forever young: Neoteny, neurogenesis and a critique of critical periods in olfaction David M. Coppola & Leonard E. White Journal of Bioenergetics and Biomembranes ISSN 0145-479X J Bioenerg Biomembr DOI 10.1007/s10863-018-9778-4 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science+Business Media, LLC, part of Springer Nature. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self- archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Journal of Bioenergetics and Biomembranes https://doi.org/10.1007/s10863-018-9778-4 MINI-REVIEW Forever young: Neoteny, neurogenesis and a critique of critical periods in olfaction David M. Coppola1 & Leonard E. White2 Received: 2 September 2018 /Accepted: 1 November 2018 # Springer Science+Business Media, LLC, part of Springer Nature 2018 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. Keywords Imprinting . Olfactory-sensory-neurons . Granule cells . Rostral-migratory-stream Introduction established, among other findings, that macaques deprived of normal maternal bonding grow up to be seemingly neurotic That the experiences of youth are particularly impactful on the individuals who are bad parents themselves (Seay et al. 1964). rest of life is an ancient idea, captured in the Romantic Poet Penfield, drawing on his vast experience treating trauma- or Wordsworth’s idiom BThe child is father of the man,^ and disease-induced aphasia as well as the zeitgeist of linguistics, championed by such diverse personages as Sigmund Freud concluded B…a child’s brain has a specialized capacity for and the Beach Boys. Three landmark lines of investigation— learning language—a capacity that decreases with the passage studies of imprinting by Konrad Lorenz (1958), affectional re- of years^ (Penfield and Roberts 1959). sponses by Henry Harlow and colleagues (Harlow and Together, these thought paths established a unique form of Zimmermann 1959;Seayetal.1964), and aphasia by Penfield learning characterized by: (1) no requirement for reinforce- and colleagues (Penfield and Roberts 1959) are generally ment; (2) strong or complete resistance to reversibility; and credited with bringing this phenomenon into the realm of (3) circumscription to a specific developmental period of po- science. tentially short duration (even a few hours) with sharp temporal In filial imprinting, made famous in Lorenz’ studies of the boundaries early in life (Lorenz 1958). Developmental phe- Greylag goose, a newborn develops a Bfollowing response^ to nomena that share these features bear the moniker, critical any large object including—provocatively—the Nobel laure- period. And, it is hard to think of a concept that has been more ate himself. Harlow’s studies of affectional responses influential in neuroscience, medicine, education or society. Indeed, this is too expansive a topic for a short review. Rather, after a brief introduction describing classical examples * David M. Coppola of the physiological underpinnings of critical period in other [email protected] sensory systems, attempts to find critical period phenomena in olfaction will be highlighted. Finally, we will provide a cri- 1 Department of Biology, Randolph Macon College, tique of the concept as applied to olfaction. In an effort to Ashland, VA 23005, USA remain agnostic about candidate olfactory phenomena we will 2 Department of Neurology, Duke Institute for Brain Sciences, Duke use the term, sensitive window, in place of critical period ar- University School of Medicine, Durham, NC 27708, USA guing in our discussion that this is more than a semantic Author's personal copy J Bioenerg Biomembr distinction. For a more nuanced categorization of windows of open channel pores by magnesium ions makes NMDA recep- plasticity in sensory systems, see Krawl (2013). tors de facto Bcoincident detectors^.Thisuniquemolecular feature of the NMDA receptor ensures that synaptic plasticity at glutamatergic synapses is modulated by the coordinated Classical sensory critical periods activation of pre- and post-synaptic elements (Hebbian plasticity; for a recent review, see Zenke and Gerstner 2017). Visual system Thus, presynaptic release of glutamate must be coincident with postsynaptic depolarization mediated by AMPA recep- Insight into the physiological basis of critical period awaited tors if magnesium ions are to be expelled from the channel the now celebrated studies of Hubel and Wiesel on ocular pores (Chater and Goda 2014). When this happens, inward dominance plasticity in the visual cortex of kittens and ma- current is carried by calcium (and sodium) and calcium- caques (reviewed in Hubel and Wiesel 1998;Hubeland dependent second messenger systems mediate a host of post- Wiesel 2005). In this classic model, which remains the gold synaptic effects, depending on the rate and magnitude of cal- standard for studies of critical period plasticity nearly six de- cium influx (Kandel et al. 2014). Consequently, the dynamics cades after its introduction, monocular deprivation (MD) for of postsynaptic calcium influx is a key factor mediating even short periods leads to rapid changes in the physiological experience-dependent competition among monocular afferent responses of visual cortical neurons provided it occurs during inputs in ocular dominance plasticity in the visual cortex. an early sensitive window in postnatal development. However, the impacts of postsynaptic calcium dynamics are Following the onset of MD the open eye increases its ability themselves subject to a host of modulators and intermediaries, to drive cortical circuits while the closed eye progressively including BDNF, PKA and CaMKII, which have been impli- loses this ability. Subsequent to the functional changes cated in the downstream processes that ultimately lead to syn- brought on by MD is rewiring of thalamic afferents and hor- aptic pruning, synaptic formation and neurite outgrowth or re- izontal connections in the visual cortex (Antonini and Stryker traction instantiating structural changes in cortical circuits. Such 1993; Trachtenberg and Stryker 2001). Experience-dependent processes account for the anatomical plasticity that favors competition between thalamic afferents is a necessary condi- thalamocortical afferents driven by the open eye at the expense tion for this process to occur, as shown by the fact that when of those monocular afferents that are driven by the closed eye binocular deprivation is enforced by suturing both eyelids (Antonini and Stryker 1993). Furthermore, BDNF may promote neither eye loses its ability to drive cortex (reviewed in GABA circuit development setting the stage for plasticity by Hubel and Wiesel 1998). Moreover, if the eyes are experimen- shifting the balance of excitation and inhibition and modulating tally (or naturally) misaligned, for example by transecting the flow of experience-evoked activity in cortical circuits extraocular muscles, biased responses to one eye or the other (Huang and Reichart 2001). This balance is germane for the are retained and sharpened while binocular responses are lost, opening and maintenance of the critical period for ocular dom- since the sensory activity of the two eyes is decorrelated inance plasticity. However, the closing of the ocular dominance (reviewed in Hubel and Wiesel 1998). Notably, this process plasticity window is now thought to involve the maturation of underlying ocular dominance plasticity is use-dependent, not extracellular matrix, which evidently restrains neurite growth merely age-dependent, a conclusion supported by experi- and remodeling (Pizzorusso et al. 2002). An important implica- ments demonstrating that raising animals in complete dark- tion of this work is that it would take major dissolution of the ness delays the window of plasticity even into adulthood in extracellular matrix surrounding mature neural circuits to reopen certain model systems (Mower 1991; Morales et al. 2002;but the sensitive period, as may be desirable in treating neurological see
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