Elsevier

Brain Research

Volume 1277, 24 June 2009, Pages 115-129
Brain Research

Review
Does the brain connect before the periphery can direct?: A comparison of three sensory systems in mice

https://doi.org/10.1016/j.brainres.2009.02.050Get rights and content

Abstract

The development of peripheral to central neural connections within the auditory, visual, and olfactory systems of mice is reviewed to address whether peripheral signaling may play an instructive role during initial synapse formation. For each sensory system, developmental times of histogenesis and the earliest ages of innervation and function are considered for peripheral and selected central relays. For the auditory and visual system, anatomical and functional reports indicate that central connections may form prior to synapse formation in the periphery. However, evidence from the olfactory system suggests that the peripheral olfactory sensory neurons form synaptic connections before more central olfactory connections are established. We find that significant gaps in knowledge exist for embryonic development of these systems in mice and that genetic tools have not yet been systematically directed to address these issues.

Introduction

Neural circuits begin to form during early brain development at embryonic ages. Whether each synaptic relay of the circuit forms autonomously or is directed in some fashion by a previous relay is a key issue and is typically addressed by investigating whether neural activity plays a role in neural development. Here we evaluate the more general question of whether neural signaling, including both electrical and synaptic activity but also non-synaptic biochemical interactions between neurons and along neural pathways, drives circuit formation. This issue is more easily approached in sensory systems because the primary direction of information transfer is specified, in that neural activity originates in the peripheral sensory organ and propagates along neural circuits in the CNS. One means to answer the question of whether sensory systems connect from periphery to cortex, or specifically, does one synaptic relay drive patterning and neural connectivity at subsequent relays, is to examine whether central contacts between neurons form and are functional prior to ability of the sensory periphery to transmit information to more central structures. In this context we evaluate when cellular processes first reach the vicinity of cells with which they will later form classical synaptic contacts. We explored this issue by comparing three relay stations of the ascending neural circuit in sensory systems: (1) receptor cells and associated neurons including ganglion cells, (2) first order CNS target neurons of the sensory ganglion neurons, and (3) second order CNS target neurons of the first order CNS neurons. We present and consider the state of knowledge for three well-studied sensory systems, the auditory, visual and olfactory systems. Given an increasing emphasis on the mouse model for studies of nervous system development, we focus our presentation on data from that species. For each sensory system, we present the birthdates of the circuit-forming cells and information about the structural and functional development of these selected neural connections. We evaluate when the anatomical substrate for each functional connection is established by reporting the earliest evidence from light and/or electron microscopy (EM) studies. We then present the earliest evidence for functional synaptic connections based on electrophysiological recordings, induced expression of immediate early genes, or behavioral readouts of appropriate sensory stimulation.

Although the auditory, visual and olfactory systems are similar in basic organization, they differ in detail. The olfactory system is simplest in peripheral organization, in that the olfactory sensory neuron (OSN) forms the olfactory nerve (without an intervening synapse) and so projects directly into the CNS. The auditory system incorporates a synaptic connection between the receptor cell, or hair cell, and peripheral ganglion cell whose axons form the auditory nerve projection into the CNS. The visual system is most complex in its peripheral organization, whereby the retina is a multi-layered neural network that is part of the CNS, with multiple synaptic connections preceding input to ganglion cells whose axons form the optic nerve projection to the thalamus and other central targets. For the visual and olfactory pathways presented here, the first order target neurons of their respective ganglion neurons project directly to sensory cortex. In contrast, the auditory system has at least four processing stations interposed between the first order CNS target of the auditory nerve and auditory cortex. The systems differ also in the onset of sensitivity to external environmental stimuli. The olfactory system is exposed to airborne odorants at birth, but the auditory and visual systems are not engaged fully until airborne sound is capable of eliciting action potentials in the auditory nerve at postnatal day (P)9 (Mikaelian and Ruben, 1965) and the eyes open at P13–14 (Poole, 1987).

The purpose of this article is to describe and compare the initial formation of synaptic contacts among these three sensory systems. Refinement of central connections that is dependent on neural activity is beyond the scope of this presentation, and we refer the reader to the following references that describe refinement in the auditory (Huang et al., 2007, Kandler, 2004, Rubel et al., 1998), visual (Hooks and Chen, 2007, Huberman et al., 2008, Torborg and Feller, 2005), and olfactory systems (Schwob et al., 1984, Schwob and Price, 1984, Zou et al., 2004). Although this review is focused upon comparisons among sensory systems in the mouse, references to other rodent species are made where data from mouse are incomplete. We found that many questions regarding the timing and nature of neural circuit formation in these systems remain open, so a key purpose of this presentation is to highlight topics that merit further study.

Section snippets

Auditory system

The three circuit connections that we consider for the auditory system are: (1) the connection between the inner hair cell and primary afferent spiral ganglion neuron, (2) the connection between the spiral ganglion neuron and a subdivision of its target cell group in the CNS, the ventral subdivision of the cochlear nucleus (VCN), and (3) the connection between the VCN and the next processing station in the auditory pathway, the superior olivary complex (SOC) located in the core of the brainstem

Visual system

Of the three sensory organs discussed here, the neuronal architecture within the eye is the most complex in terms of cell types, circuitry and processing. Therefore, for the purpose of this review, we focus on the following retinal circuits that together comprise the initial connections in the visual system: (1a) photoreceptor connections onto bipolar cells, (1b) bipolar cell connections onto retinal ganglion cells (RGCs), and (1c) amacrine cell synapses onto RGCs. For the sake of simplicity,

Olfactory system

Olfaction initiates in the nasal epithelium where combinations of olfactory sensory neurons (OSNs) reside, each encoding a single receptor subtype that selectively binds to a particular odorant molecule (Bozza et al., 2002, Buck and Axel, 1991, Chess et al., 1994). The mouse genome encodes approximately 1200 different OSN receptor types for OSNs. Although OSN cell types are relatively scattered across 4 epithelial zones, OSN axons are targeted by individual receptor type to particular mitral

Unresolved issues in sensory system development

The title of this article posed the question: does the brain connect before the periphery can direct?

Multiple observations might suggest it does. Soon after final mitosis, many neurons extend an axon toward their target even as their cell body migrates toward its final position in the brain (Yee et al., 1999). Axon guidance cues then position the axon growth cone into an approximate location to innervate its target (Tessier-Lavigne and Goodman, 1996). The role of neurotransmitter release in

Acknowledgments

Portions of this work were supported by National Institutes of Health (NIH) grants F32 DC008730 to BH, RO1 DC007695 to GS, RO1 EY012152 to PM and a NIH/NCRR COBRE grant P20 RR15574 to the Sensory Neuroscience Research Center.

References (133)

  • GodementP. et al.

    Thalamic afferents to the visual cortex in congenitally anophthalmic mice

    Neurosci. Lett.

    (1979)
  • HoltC.E. et al.

    Cellular determination in the Xenopus retina is independent of lineage and birth date

    Neuron

    (1988)
  • HooksB.M. et al.

    Critical periods in the visual system: changing views for a model of experience-dependent plasticity

    Neuron

    (2007)
  • IlligK.R.

    Developmental changes in odor-evoked activity in rat piriform cortex

    Neuroscience

    (2007)
  • Kaiserman-AbramofI.R. et al.

    The thalamic projection to cortical area 17 in a congenitally anophthalmic mouse strain

    Neuroscience

    (1980)
  • KandlerK.

    Activity-dependent organization of inhibitory circuits: lessons from the auditory system

    Curr. Opin. Neurobiol.

    (2004)
  • LattemannM. et al.

    Semaphorin-1a controls receptor neuron-specific axonal convergence in the primary olfactory center of Drosophila

    Neuron

    (2007)
  • LinD.M. et al.

    Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity

    Neuron

    (2000)
  • MairR.G. et al.

    Response properties of mitral cells in the olfactory bulb of the neonatal rat

    Neuroscience

    (1982)
  • MombaertsP. et al.

    Visualizing an olfactory sensory map

    Cell

    (1996)
  • MooneyR. et al.

    Thalamic relay of spontaneous retinal activity prior to vision

    Neuron

    (1996)
  • MoshiriA. et al.

    Near complete loss of retinal ganglion cells in the math5/brn3b double knockout elicits severe reductions of other cell types during retinal development

    Dev. Biol.

    (2008)
  • Nemzou NR.M. et al.

    Synaptic organization in cochlear inner hair cells deficient for the CaV1.3 ([alpha]1D) subunit of L-type Ca2+ channels

    Neuroscience

    (2006)
  • PierceE.T.

    Time of origin of neurons in the brain stem of the mouse

    Prog. Brain Res.

    (1973)
  • PuyalJ. et al.

    Distribution of [alpha]-amino-3-hydroxy-5-methyl-4 isoazolepropionic acid and N-methyl-aspartate receptor subunits in the vestibular and spiral ganglia of the mouse during early development

    Dev. Brain Res.

    (2002)
  • ResslerK.J. et al.

    A zonal organization of odorant receptor gene expression in the olfactory epithelium

    Cell

    (1993)
  • RouxI. et al.

    Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse

    Cell

    (2006)
  • AngevineJ.B.

    Time of neuron origin in the diencephalon of the mouse. An autoradiographic study

    J. Comp. Neurol.

    (1970)
  • BansalA. et al.

    Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina

    J. Neurosci.

    (2000)
  • BensonT.E. et al.

    Effects of sensory deprivation on the developing mouse olfactory system: a light and electron microscopic, morphometric analysis

    J. Neurosci.

    (1984)
  • BerminghamN.A. et al.

    Math1: an essential gene for the generation of inner ear hair cells

    Science

    (1999)
  • BeurgM. et al.

    Calcium- and otoferlin-dependent exocytosis by immature outer hair cells

    J. Neurosci.

    (2008)
  • BijuK.C. et al.

    Deletion of voltage-gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

    J. Comp. Neurol.

    (2008)
  • BlanchartA. et al.

    Time frame of mitral cell development in the mice olfactory bulb

    J. Comp. Neurol.

    (2006)
  • BlanchartA. et al.

    Synaptogenesis in the mouse olfactory bulb during glomerulus development

    Eur. J. Neurosci.

    (2008)
  • BlanksJ.C. et al.

    Synaptogenesis in the photoreceptor terminal of the mouse retina

    J. Comp. Neurol.

    (1974)
  • BozzaT. et al.

    Odorant receptor expression defines functional units in the mouse olfactory system

    J. Neurosci.

    (2002)
  • BrandtA. et al.

    CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells

    J. Neurosci.

    (2003)
  • BrunjesP.C.

    Unilateral naris closure and olfactory system development

    Brain Res. Brain Res. Rev.

    (1994)
  • CantN.B.

    Structural development of the mammalian auditory pathways

  • CepkoC.L. et al.

    Cell fate determination in the vertebrate retina

    Proc. Natl. Acad. Sci. U. S. A.

    (1996)
  • ChenP. et al.

    p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti

    Development

    (1999)
  • ChenP. et al.

    The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination

    Development

    (2002)
  • Del RioJ.A. et al.

    Developmental history of the subplate and developing white matter in the murine neocortex. neuronal organization and relationship with the main afferent systems at embryonic and perinatal stages

    Cereb. Cortex

    (2000)
  • EneF.A. et al.

    Glutamatergic calcium responses in the developing lateral superior olive: receptor types and their specific activation by synaptic activity patterns

    J. Neurophysiol.

    (2003)
  • Erazo-FischerE. et al.

    The role of physiological afferent nerve activity during in vivo maturation of the calyx of Held synapse

    J. Neurosci.

    (2007)
  • FellerM.B. et al.

    Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves

    Science

    (1996)
  • FisherL.J.

    Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina

    J. Comp. Neurol.

    (1979)
  • Galli-RestaL. et al.

    Afferent spontaneous electrical activity promotes the survival of target cells in the developing retinotectal system of the rat

    J. Neurosci.

    (1993)
  • GardetteR. et al.

    Prenatal development of mouse central nervous structures: time of neuron origin and gradients of neuronal production. A radioautographic study

    J. Hirnforsch.

    (1982)
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