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MIT HST 722J - Somatosensory influence on the cochlear nucleus and beyond

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Somatosensory influence on the cochlear nucleus and beyondIntroductionAnatomy of somatosensory connections with the cochlear nucleusTrigeminal ganglion to cochlear nucleus pathwaySpinal trigeminal nucleus to Cochlear nucleus pathwaysProjections from other non-auditory structures to the cochlear nucleusResponses of cochlear nucleus neurons to stimulation of somatosensory pathwaysResponses of CN neurons to somatosensory stimulation in the absence of soundResponses of CN neurons to combined somatosensory and acoustic stimulation: multisensory integrationSignificance of bimodal integration in the CNMaintaining bimodal integration along the auditory pathwayDCN and Sp5 project to the external cortex of IC (ICX)ICX integrates information from DCN and Sp5AcknowledgementsReferencesResearch paperSomatosensory influence on the cochlear nucleus and beyondSusan E. Shore*, Jianxun ZhouUniversity of Michigan, Otolaryngology, 1301 E Ann St, Ann Arbor, MI 48109, United StatesReceived 31 October 2005; received in revised form 5 January 2006; accepted 5 January 2006Available online 2 March 2006AbstractInteractions between somatosensory and auditory systems occur at peripheral levels in the central nervous system. The cochlearnucleus (CN) receives innervation from trigeminal sensory structures: the ophthalmic division of the trigeminal ganglion and the caudaland interpolar regions of the spinal trigeminal nucleus (Sp5I and Sp5C). These projections terminate primarily in the granule cell domain,but also in magnocellular regions of the ventral and dorsal CN. Additionally, new evidence is presented demonstrating that cells in thelateral paragiganticular regions of the reticular formation (RF) also project to the CN. Not unlike the responses obtained from electri-cally stimulating the trigeminal system, stimulating RF regions can also result in excitation/inhibition of dorsal CN neurons. The originsand central connections of these projection neurons are associated with systems controlling vocalization and respiration. Electrical stim-ulation of trigeminal and RF projection neurons can suppress acoustically driven activity of not only CN neurons, but also neurons inthe inferior colliculus. Together with the anatomical observations, these physiological observations suggest that one function of somato-sensory input to the auditory system is to suppress responses to ‘‘expected’’ body-generated sounds such as vocalization or respiration.This would serve to enhance responses to ‘‘unexpected’’ externally-generated sounds, such as the vocalizations of other animals. 2006 Elsevier B.V. All rights reserved.Keywords: Auditory; Cochlear nucleus; Pathways; Trigeminal; Reticular formation; Somatosensory; Non-auditory projections1. IntroductionIt is well established that somatosensory and auditorysignals are integrated by auditory neurons in the inferiorcolliculus (IC), superior colliculus (SC) and auditory cor-tex (Aitkin et al., 1978, 1981; Eliades and Wang, 2003,2005). However, more recent neuroanatomical and physi-ological data indicate that somatosensory and auditoryinformation converge at more peripheral sites: for exam-ple, the trigeminal ganglion (TG), dorsal column nucleiand interpolar and caudal spinal trigeminal nuclei sendfibers directly to the dorsal cochlear nucleus (DCN) andthe granule cell regions of the ventral cochlear nucleus(VCN) (Weinberg and Rustioni, 1987; Wright and Ryugo,1996; Zhou and Shor e, 2004; Haenggeli et al., 2005; Itohet al., 1987). The trigeminal sensory complex that receivessensory information from the head, face and vocal tract/intra oral structures is one major component of this inte-gration. The excitatory and inhibitory responses evoked incochlear nucleus (CN) neurons by stimulating the originsof trigeminal projections (Shore et al., 2003; Zhou andShore, 2004; Shore, 2005) suggest that these projectionsmay be involved in mechanisms related to suppressionof self-generated sounds such as respiration, chewing orself-vocalizations.0378-5955/$ - see front matter  2006 Elsevier B.V. All rights reserved.doi:10.1016/j.heares.2006.01.006Abbreviations: AVCN, anteroventral cochlear nucleus; BBN, broad-band noise; BDA, biotinylated dextran-amine; BF, best frequency; Ca,cartwheel cells; CN, cochlear nucleus; Cu, cuneate nucleus; DAS, dorsalacoustic striae; DCN, dorsal cochlear nucleus; Fu, fusiform cell; GCD,granule cell domain; Gi, giant cell; gr, granule cell; Gr, gracile nucleus;IAS, intermediate acoustic striae; IC, inferior colliculus; ICX, externalcortex of inferior colliculus; ICXV, ventrolateral border region of IC; IO,inferior olive; LPGi, lateral paragigantocellular reticular nucleus; PVCN,posteroventral cochlear nucleus; RF, reticular formation; RVL, rostralventrolateral reticular formation; SC, superior colliculus; SG, subnucleusgelatinosus; sp5, spinal trigeminal tract; Sp5, spinal trigeminal nucleus;Sp5C, pars caudalis of spinal trigeminal nucleus; Sp5I, pars interpolaris ofspinal trigeminal nucleus; Sp5O, pars oralis of spinal trigeminal nucleus;TG, trigeminal ganglion; VCN, ventral cochlear nucleus*Corresponding author. Tel.: +1 734 647 2116; fax: +1 734 764 0014.E-mail address: [email protected] (S.E. Shore).www.elsevier.com/locate/hearesHearing Research 216–217 (2006) 90–99HearingResearch2. Anatomy of soma tosensory connections with the cochlearnucleus2.1. Trigeminal ganglion to cochlear nucleus pathwaySensory information from the head and face is conveyedto the central trigeminal sensory nuclear complex via theophthalmic, maxillar, and mandibul ar branches of the tri-geminal nerve. The ophthalmic nerve innervates the fore-head, upper eyelid, or extraocular muscles; the maxillarynerve supplies the upper lip, the lower eyelid and the upperjaw and roof of the mouth; and the mandibular nerveinnervates the lower lip, the mucous membranes of thelower jaw, the floor of the mouth, and anterio r two thirdsof the tongue (Aigner et al., 1997).Trigeminal ganglion cells that project to the CN arelocated in the medial portion of the ganglion and at the ori-gin of the ophthalmic nerve, as well as in the mandibulardivision of the ganglion. Some projection cells are locatedin the maxillary division (Shore et al., 2000). The locationsof these projection neurons overlap with the regions thatinnervate both the cochlea and the middle ear: The oph-thalmic division innervates the cochlea, and the mandibu-lar region innervates the middle ear (Vass et al.,


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