Does the brain connect before the periphery can direct?

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.

Spontaneous activity in the developing auditory system

“…Although some nascent synaptic connections between auditory nuclei are established embryonically (Hoffpauir et al 2009), the auditory brainstem circuit experiences remarkable structural and functional modifications during the first two postnatal weeks, during which auditory neurons obtain their adult morphology (Sanes et al 1992;Sanes and Takacs 1993) and electrical properties (Sanes 1993;Kandler and Friauf 1995a;Youssoufian et al 2005;Lu et al 2007). During this time, synapses undergo morphological changes (Hoffpauir et al 2006;Youssoufian et al 2008;Ford et al 2009), they are strengthened or eliminated (Sanes 1993;Kotak and Sanes 1995;Taschenberger and von Gersdorff 2000;Brenowitz and Trussell 2001;Iwasaki and Takahashi 2001;Kim and Kandler 2003;Awatramani et al 2005;Youssoufian et al 2005;Hoffpauir et al 2006;Lu et al 2007), and undergo spatial refinement to achieve precise tonotopic connections (Sanes et al 1992;Sanes and Takacs 1993;Gabriele et al 2000a;Leake et al 2002;Kim and Kandler 2003).…”

“…This activity is unlikely to be restricted to the cochlea, as the central projections of SGNs grow into the hindbrain quite early (Appler and Goodrich 2011) and reach the cochlear nucleus by E15.5 (Koundakjian et al 2007). Within the brainstem, functional synapses between auditory relay neurons are also present at birth (Friauf and Kandler 1990;Kandler and Friauf 1995b;Hoffpauir et al 2006Hoffpauir et al , 2009Rodriguez-Contreras et al 2008). Together, these anatomical and functional studies indicate that the transduction pathway from IHCs to developing circuits of the brain is established well before hearing onset, providing a substrate that spontaneous activity can act upon to influence its developmental trajectory.…”

“…Most studies have been performed in either chicken (in ovo) or neonatal altricial animals, such as rodents and cats, which are born deaf and remain unresponsive to airborne sound until approximately the end of the 2nd postnatal week. In rodents, the inability to sense ambient sound is not due to the inability of hair cells to transform mechanical stimulation into electrical signals (Lelli et al 2009) or the lack of functional connections between central cochlear neurons (Hoffpauir et al 2009). Rather, deafness results from the combination of physical occlusion of the external ear canal, poor ossicular transduction in the middle ear, underdeveloped mechanics in the organ of Corti, immature ionic composition in the endolymph, and absence of the endocochlear potential (Bosher and Warren 1971;Anniko and Wroblewski 1986;Woolf and Ryan 1988;Rybak et al 1992;Geal-Dor et al 1993;Abe et al 2007).…”

Development of on-off spiking in superior paraolivary nucleus neurons of the mouse

“…Although auditory brain stem development has been studied in detail (for reviews, see, e.g., Hoffpauir et al 2009 andKandler et al 2009), the SPON has received relatively little attention. To our knowledge, this is the first study that focuses on the intrinsic properties of SPON neurons.…”

Comparative Analysis of Gene Regulatory Network Components in the Auditory Hindbrain of Mice and Chicken

“…at postnatal day (P4) and at P25 in the mouse and at embryonic day 13 (E13) and at P14-17 in the chicken. During this period, which succeeds cell birth, migration and the establishment of major connections [Kandler and Friauf, 1993], auditory neurons undergo refinement of their projections [Kim and Kandler, 2003] and synaptic configuration [Hoffpauir et al, 2009;Nothwang et al, 2015], and establish their pharmacological and biophysical properties [Hoffpauir et al, 2009] and their final neurotransmitter phenotype [Friauf et al, 1999;Blaesse et al, 2005].…”