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Chapter 23 Activity on Brainstem Circuits 31 This article was originally published in the Comprehensive Developmental Neuroscience: Neural Circuit Development and Function in the Brain published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial Polley D.B., Seidl A.H., Wang Y. and Sanchez J.T. (2013) Functional Circuit Development in the Auditory System. In: RUBENSTEIN J. L. R. and RAKIC P. (ed.) Comprehensive Developmental Neuroscience: Neural Circuit Development and Function in the Brain, volume 3, pp. 21-39 Amsterdam: Elsevier. © 2013 Elsevier Inc. All rights reserved. Author's personal copy CHAPTER 2 Functional Circuit Development in the Auditory System 1 2 2 2 D.B. Polley , A.H. Seidl , Y. Wang , J.T. Sanchez 1Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary & Dept. of Otology and Laryngology, 2 Harvard Medical School, Boston, MA, USA; Virginia Merrill Bloedel Hearing Research Center & Dept. of Otolaryngology, Head and Neck Surgery, University of Washington, Seattle, WA, USA OUTLINE 2.1 Introduction to Auditory System 2.3.4 Afferent Regulation of Cochlear Nucleus Development 22 Development 29 2.1.1 A Neurobiological Approach to Studying 2.3.5 Afferent Regulation of 3rd-Order Brainstem Auditory System Development 22 Nuclei 30 2.1.2 Basic Concepts of Cochlear Transduction 22 2.3.6 Influence of the Source and Pattern of Afferent 2.1.3 Scope of this Chapter 23 Activity on Brainstem Circuits 31 2.2 Development of Peripheral Circuits 23 2.3.7 Conclusions 31 2.2.1 Developing Networks Within the Cochlea 23 2.4 Development of Auditory Midbrain and 2.2.2 Development of the Place Code 24 Forebrain Circuits 32 2.2.3 Development of Afferent and 2.4.1 Development of Thalamocortical Subplate Efferent Circuits 25 Circuitry 32 Phase 1: Well Before Hearing Onset 25 2.4.2 Postnatal Development of Local Phase 2: Shortly Before Hearing Onset 26 Cortical Circuits 33 Phase 3: Shortly After Hearing Onset 26 2.4.3 Afferent Regulation of Higher Auditory Circuit 2.2.4 Conclusions 27 Development 34 2.3 Development of Brainstem Circuits 27 2.4.4 Developmental Regulation over Reinstating 2.3.1 Functional Circuit Assembly in the Hearing in the Deaf 35 Brainstem 27 2.4.5 Experience-Dependent Influences on 2.3.2 Development of Fine-Scale Connectivity Functional Circuit Development 36 in the MSO 28 2.4.6 Conclusions and Directions for 2.3.3 Development of Fine-Scale Connectivity Future Research 37 in the LSO 29 References 38 Neural Circuit Development and Function in the Brain: Comprehensive Developmental 21 # 2013 Elsevier Inc. All rights reserved. Neuroscience, Volume 3 http://dx.doi.org/10.1016/B978-0-12-397267-5.00136-9 Comprehensive Developmental Neuroscience: Neural Circuit Development and Function in the Brain, (2013), vol. 3, pp. 21-39 Author's personal copy 22 2. FUNCTIONAL CIRCUIT DEVELOPMENT IN THE AUDITORY SYSTEM 2.1 INTRODUCTION TO AUDITORY neuron survival and regulate the growth and topo- SYSTEM DEVELOPMENT graphic specificity of axons and dendrites within audi- tory brain areas. In some brain areas, instructive electrical signals generated through the “closed-loop” 2.1.1 A Neurobiological Approach to Studying Auditory System Development spontaneous activity is sufficient to promote normal neural circuit development, whereas higher levels of The auditory system undergoes a series of profound the auditory pathway require structured activity pat- changes from the time neural circuits begin forming in terns arising from acoustic signals to guide their final the fetal brain to the day, years later, when a child stages of assembly. The influence of each activity- first comprehends a complete sentence. The processes dependent and activity-independent factor waxes and unfolding during this period are a fascinating mixture wanes within defined windows of development, and of intrinsic molecular orchestration and activity- piecing together the chronology and mechanisms behind dependent refinement. In humans, auditory perceptual each epoch of auditory system development represents development is a protracted process that begins late in one of the fundamental challenges for researchers in this the second trimester when the fetus first shows discrim- field. The chapter describes the current state of knowl- inative changes in heart rate to variations in specific edge concerning the interplay of these factors in the es- sound features. Progressive improvements in the ability tablishment of functional circuits from the cochlea to the to resolve variations in frequency, temporal patterns and cerebral cortex. spatial positions of sounds are observed throughout in- fancy and early childhood, and these changes often par- allel an increasing capacity to discriminate phonological 2.1.2 Basic Concepts of Cochlear Transduction units of a child’s native language (Werker, 2005). While a greater understanding of the processes at work in hu- The encoding of auditory information begins with a man auditory development is of paramount importance, highly specialized receptor organ known as the cochlea these efforts are often complicated by an inability to iso- in mammals and the basilar papilla in birds. In mam- late the contributions of sensory system development mals, pressure waves are delivered into the fluid filled from other cognitive and physical factors. cochlea via the middle ear bones, setting the cochlear The use of model systems such as birds and rodents partition into motion. The cochlear partition consists of has provided researchers with direct access to central the basilar membrane (BM), the organ of Corti, and the and peripheral auditory circuits, and has elucidated tectorial membrane (Figure 2.1(a)). As a result of this mo- many of the basic mechanisms that underlie their tion and the mechanical properties of these structures, a changes during ontogeny. Songbirds and chickens have relatively crude spectral analysis is performed by a vi- long been popular model systems due to the greater ease bratory pattern that occurs along the partition, a passive of studying and manipulating the embryo in the egg (in process referred to as the traveling wave (Von Be´ke´sy, ovo) rather than in utero. As a result, we can now draw 1960). This traveling wave results in a vibratory pattern information from an extensive corpus of work detailing such that high frequency sounds produce maximum dis- the organization of brainstem and forebrain pathways, placement near the beginning (base) of the partition, and the similarities by which songbirds acquire their while low frequency sounds vibrate maximally near song and humans acquire speech, particularly in their the end (apex) of the partition. dependence on auditory feedback during sensitive pe- The sensory receptors in mammals responsible for riods of development. Interestingly, birds begin hearing transducing these hydro-mechanical vibrations are lo- approximately eight days before hatching, around em- cated in the organ of Corti and are known as inner bryonic (E) day 11, while altricial mammals such as mice, and outer hair cells (IHC and OHC, respectively). Both rats and gerbils do not respond to airborne sound until types of receptors are polarized epithelial cells that con- the second postnatal (P) week of life. The relatively late tain mechano-sensitive organelles located on their api- onset of hearing in rodents has aided research into the cal surface. These actin-filled hair-like processes are cellular and molecular changes that underlie abrupt termed stereocilia and contain mechanotransducer changes in circuit development in the days before and channels near the tips of the ciliary bundles. The bun- after the onset of hearing. dles are deflected as a result of partition movement, Recent studies suggest that molecular cues, whose ex- opening the channels and depolarizing the hair cell þ pression is genetically controlled, play an essential role due to an influx of potassium (K ). This unconventional in the formation of topographically ordered connections form of depolarization activates voltage gated calcium þ in the auditory system. It is also evident that factors (Ca2 ) channels, which triggers the release of the excit- linked to the flux of ions across the cell membrane dur- atory neurotransmitter glutamate. Glutamate binds to ing and following the action potential also support postsynaptic receptors located on first-order spiral I. CIRCUIT DEVELOPMENT Comprehensive Developmental Neuroscience: Neural Circuit Development and Function in the Brain, (2013), vol. 3, pp. 21-39 Author's personal copy 2.2 DEVELOPMENT OF PERIPHERAL CIRCUITS 23 Sound frequency Tectorial membrane High OHC OHC OHC Low IHC Basilar membrane (a) (b) FIGURE 2.1 Connections within the adult auditory system. Schematics illustrate the position of cell bodies and their interconnections in mammalian Organ of Corti (a) and initial components of the auditory pathway (b). (a) Two classes of mechanical
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