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Listening to another sense: somatosensory integration in the auditory system

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Abstract

Conventionally, sensory systems are viewed as separate entities, each with its own physiological process serving a different purpose. However, many functions require integrative inputs from multiple sensory systems and sensory intersection and convergence occur throughout the central nervous system. The neural processes for hearing perception undergo significant modulation by the two other major sensory systems, vision and somatosensation. This synthesis occurs at every level of the ascending auditory pathway: the cochlear nucleus, inferior colliculus, medial geniculate body and the auditory cortex. In this review, we explore the process of multisensory integration from (1) anatomical (inputs and connections), (2) physiological (cellular responses), (3) functional and (4) pathological aspects. We focus on the convergence between auditory and somatosensory inputs in each ascending auditory station. This review highlights the intricacy of sensory processing and offers a multisensory perspective regarding the understanding of sensory disorders.

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References

  • Adams JC (1980) Crossed and descending projections to the inferior colliculus. Neurosci Lett 19:1–5

    CAS  PubMed  Google Scholar 

  • Aitkin LM (1973) Medial geniculate body of the cat: responses to tonal stimuli of neurons in medial division. J Neurophysiol 36:275–283

    CAS  PubMed  Google Scholar 

  • Aitkin LM, Webster WR (1972) Medial geniculate body of the cat: organization and responses to tonal stimuli of neurons in ventral division. J Neurophysiol 35:365–380

    CAS  PubMed  Google Scholar 

  • Aitkin LM, Dickhaus H, Schult W, Zimmermann M (1978) External nucleus of inferior colliculus: auditory and spinal somatosensory afferents and their interactions. J Neurophysiol 41:837–847

    CAS  PubMed  Google Scholar 

  • Aitkin LM, Kenyon CE, Philpott P (1981) The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus. J Comp Neurol 196:25–40

    CAS  PubMed  Google Scholar 

  • Allman BL, Meredith MA (2007) Multisensory processing in “unimodal” neurons: cross-modal subthreshold auditory effects in cat extrastriate visual cortex. J Neurophysiol 98:545–549

    PubMed  Google Scholar 

  • Allman BL, Keniston LP, Meredith MA (2009) Adult deafness induces somatosensory conversion of ferret auditory cortex. Proc Natl Acad Sci U S A 106:5925–5930

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anderson LA, Malmierca MS, Wallace MN, Palmer AR (2006) Evidence for a direct, short latency projection from the dorsal cochlear nucleus to the auditory thalamus in the guinea pig. Eur J Neurosci 24:491–498

    CAS  PubMed  Google Scholar 

  • Bajo VM, Leach ND, Cordery PM, Nodal FR, King AJ (2014) The cholinergic basal forebrain in the ferret and its inputs to the auditory cortex. Eur J Neurosci (in press)

  • Banks MI, Uhlrich DJ, Smith PH, Krause BM, Manning KA (2011) Descending projections from extrastriate visual cortex modulate responses of cells in primary auditory cortex. Cereb Cortex 21:2620–2638

    PubMed Central  PubMed  Google Scholar 

  • Barker M, Solinski HJ, Hashimoto H, Tagoe T, Pilati N, Hamann M (2012) Acoustic overexposure increases the expression of VGLUT-2 mediated projections from the lateral vestibular nucleus to the dorsal cochlear nucleus. PLoS ONE 7:e35955

    CAS  PubMed Central  PubMed  Google Scholar 

  • Basura GJ, Koehler SD, Shore SE (2012) Multi-sensory integration in brainstem and auditory cortex. Brain Res 1485:95–107

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bavelier D, Neville HJ (2002) Cross-modal plasticity: where and how? Nat Rev Neurosci 3:443–452

    CAS  PubMed  Google Scholar 

  • Bayazitov IT, Westmoreland JJ, Zakharenko SS (2013) Forward suppression in the auditory cortex is caused by the Ca(v)3.1 calcium channel-mediated switch from bursting to tonic firing at thalamocortical projections. J Neurosci 33:18940–18950

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bell CC (2001) Memory-based expectations in electrosensory systems. Curr Opin Neurobiol 11:481–487

    CAS  PubMed  Google Scholar 

  • Bell C, Bodznick D, Montgomery J, Bastian J (1997) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav Evol 50(Suppl 1):17–31

    PubMed  Google Scholar 

  • Bell CC, Han VZ, Sugawara Y, Grant K (1999) Synaptic plasticity in the mormyrid electrosensory lobe. J Exp Biol 202:1339–1347

    CAS  PubMed  Google Scholar 

  • Bell CC, Han V, Sawtell NB (2008) Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31:1–24

    CAS  PubMed  Google Scholar 

  • Binns KE, Grant S, Withington DJ, Keating MJ (1992) A topographic representation of auditory space in the external nucleus of the inferior colliculus of the guinea-pig. Brain Res 589:231–242

    CAS  PubMed  Google Scholar 

  • Bizley JK, King AJ (2009) Visual influences on ferret auditory cortex. Hear Res 258:55–63

    PubMed Central  PubMed  Google Scholar 

  • Blakemore SJ, Wolpert DM, Frith CD (1998) Central cancellation of self-produced tickle sensation. Nat Neurosci 1:635–640

    CAS  PubMed  Google Scholar 

  • Blundon JA, Bayazitov IT, Zakharenko SS (2011) Presynaptic gating of postsynaptically expressed plasticity at mature thalamocortical synapses. J Neurosci 31:16012–16025

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bukowska D (2002) Morphological evidence for secondary vestibular afferent connections to the dorsal cochlear nucleus in the rabbit. Cells Tissues Organs 170:61–68

    CAS  PubMed  Google Scholar 

  • Burian M, Gstoettner W (1988) Projection of primary vestibular afferent fibres to the cochlear nucleus in the guinea pig. Neurosci Lett 84:13–17

    CAS  PubMed  Google Scholar 

  • Calford MB, Aitkin LM (1983) Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3:2365–2380

    CAS  PubMed  Google Scholar 

  • Campolattaro MM, Halverson HE, Freeman JH (2007) Medial auditory thalamic stimulation as a conditioned stimulus for eyeblink conditioning in rats. Learn Mem 14:152–159

    PubMed Central  PubMed  Google Scholar 

  • Cant NB (2013) Patterns of convergence in the central nucleus of the inferior colliculus of the Mongolian gerbil: organization of inputs from the superior olivary complex in the low frequency representation. Front Neural Circ 7:29

    Google Scholar 

  • Cant NB, Benson CG (2006) Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): differences in distribution of projections from the cochlear nuclei and the superior olivary complex. J Comp Neurol 495:511–528

    PubMed Central  PubMed  Google Scholar 

  • Cappe C, Barone P (2005) Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey. Eur J Neurosci 22:2886–2902

    PubMed  Google Scholar 

  • Chun S, Bayazitov IT, Blundon JA, Zakharenko SS (2013) Thalamocortical long-term potentiation becomes gated after the early critical period in the auditory cortex. J Neurosci 33:7345–7357

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cohen L, Rothschild G, Mizrahi A (2011) Multisensory integration of natural odors and sounds in the auditory cortex. Neuron 72:357–369

    CAS  PubMed  Google Scholar 

  • Coleman JR, Clerici WJ (1987) Sources of projections to subdivisions of the inferior colliculus in the rat. J Comp Neurol 262:215–226

    CAS  PubMed  Google Scholar 

  • Cooper AM, Cowey A (1990) Development and retraction of a crossed retinal projection to the inferior colliculus in neonatal pigmented rats. Neuroscience 35:335–344

    CAS  PubMed  Google Scholar 

  • Cooper MH, Young PA (1976) Cortical projections to the inferior colliculus of the cat. Exp Neurol 51:488–502

    CAS  PubMed  Google Scholar 

  • Cruikshank SJ, Edeline JM, Weinberger NM (1992) Stimulation at a site of auditory-somatosensory convergence in the medial geniculate nucleus is an effective unconditioned stimulus for fear conditioning. Behav Neurosci 106:471–483

    CAS  PubMed  Google Scholar 

  • Dahmen JC, Hartley DE, King AJ (2008) Stimulus-timing-dependent plasticity of cortical frequency representation. J Neurosci 28:13629–13639

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353–375

    CAS  PubMed  Google Scholar 

  • de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA (2006a) Cortical connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J Comp Neurol 496:27–71

    PubMed  Google Scholar 

  • de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA (2006b) Thalamic connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J Comp Neurol 496:72–96

    PubMed Central  PubMed  Google Scholar 

  • Dehmel S, Pradhan S, Koehler S, Bledsoe S, Shore S (2012) Noise overexposure alters long-term somatosensory-auditory processing in the dorsal cochlear nucleus–possible basis for tinnitus-related hyperactivity? J Neurosci 32:1660–1671

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dehner LR, Keniston LP, Clemo HR, Meredith MA (2004) Cross-modal circuitry between auditory and somatosensory areas of the cat anterior ectosylvian sulcal cortex: a ‘new’ inhibitory form of multisensory convergence. Cereb Cortex 14:387–403

    PubMed  Google Scholar 

  • Donishi T, Kimura A, Imbe H, Yokoi I, Kaneoke Y (2011) Sub-threshold cross-modal sensory interaction in the thalamus: lemniscal auditory response in the medial geniculate nucleus is modulated by somatosensory stimulation. Neuroscience 174:200–215

    CAS  PubMed  Google Scholar 

  • Druga R, Syka J (1984) Projections from auditory structures to the superior colliculus in the rat. Neurosci Lett 45:247–252

    CAS  PubMed  Google Scholar 

  • Edeline JM, Manunta Y, Hennevin E (2011) Induction of selective plasticity in the frequency tuning of auditory cortex and auditory thalamus neurons by locus coeruleus stimulation. Hear Res 274:75–84

    PubMed  Google Scholar 

  • Foxe JJ, Wylie GR, Martinez A, Schroeder CE, Javitt DC, Guilfoyle D, Ritter W, Murray MM (2002) Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. J Neurophysiol 88:540–543

    PubMed  Google Scholar 

  • Freeman JH, Halverson HE, Hubbard EM (2007) Inferior colliculus lesions impair eyeblink conditioning in rats. Learn Mem 14:842–846

    PubMed Central  PubMed  Google Scholar 

  • Fu KM, Johnston TA, Shah AS, Arnold L, Smiley J, Hackett TA, Garraghty PE, Schroeder CE (2003) Auditory cortical neurons respond to somatosensory stimulation. J Neurosci 23:7510–7515

    CAS  PubMed  Google Scholar 

  • Gerren RA, Weinberger NM (1983) Long term potentiation in the magnocellular medial geniculate nucleus of the anesthetized cat. Brain Res 265:138–142

    CAS  PubMed  Google Scholar 

  • Gobbele R, Schurmann M, Forss N, Juottonen K, Buchner H, Hari R (2003) Activation of the human posterior parietal and temporoparietal cortices during audiotactile interaction. NeuroImage 20:503–511

    CAS  PubMed  Google Scholar 

  • Golding NL, Oertel D (1996) Context-dependent synaptic action of glycinergic and GABAergic inputs in the dorsal cochlear nucleus. J Neurosci 16:2208–2219

    CAS  PubMed  Google Scholar 

  • Golding NL, Oertel D (1997) Physiological identification of the targets of cartwheel cells in the dorsal cochlear nucleus. J Neurophysiol 78:248–260

    CAS  PubMed  Google Scholar 

  • Gomez-Nieto R, Rubio ME (2011) Ultrastructure, synaptic organization, and molecular components of bushy cell networks in the anteroventral cochlear nucleus of the rhesus monkey. Neuroscience 179:188–207

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gruters KG, Groh JM (2012) Sounds and beyond: multisensory and other non-auditory signals in the inferior colliculus. Front Neural Circ 6:96

    Google Scholar 

  • Hackett TA, Smiley JF, Ulbert I, Karmos G, Lakatos P, de la Mothe LA, Schroeder CE (2007) Sources of somatosensory input to the caudal belt areas of auditory cortex. Perception 36:1419–1430

    PubMed  Google Scholar 

  • Haenggeli CA, Pongstaporn T, Doucet JR, Ryugo DK (2005) Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat. J Comp Neurol 484:191–205

    PubMed  Google Scholar 

  • Heldt SA, Falls WA (2003) Destruction of the inferior colliculus disrupts the production and inhibition of fear conditioned to an acoustic stimulus. Behav Brain Res 144:175–185

    PubMed  Google Scholar 

  • Hotting K, Roder B (2004) Hearing cheats touch, but less in congenitally blind than in sighted individuals. Psychol Sci 15:60–64

    PubMed  Google Scholar 

  • Huang J, Gamble D, Sarnlertsophon K, Wang X, Hsiao S (2012) Feeling music: integration of auditory and tactile inputs in musical meter perception. PLoS ONE 7:e48496

    CAS  PubMed Central  PubMed  Google Scholar 

  • Itoh K, Kamiya H, Mitani A, Yasui Y, Takada M, Mizuno N (1987) Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat. Brain Res 400:145–150

    CAS  PubMed  Google Scholar 

  • Jain R, Shore S (2006) External inferior colliculus integrates trigeminal and acoustic information: unit responses to trigeminal nucleus and acoustic stimulation in the guinea pig. Neurosci Lett 395:71–75

    CAS  PubMed  Google Scholar 

  • Ji W, Suga N (2013) Histaminergic modulation of nonspecific plasticity of the auditory system and differential gating. J Neurophysiol 109:792–802

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jones EG, Burton H (1974) Cytoarchitecture and somatic sensory connectivity of thalamic nuclei other than the ventrobasal complex in the cat. J Comp Neurol 154:395–432

    CAS  PubMed  Google Scholar 

  • Jones EG, Rockel AJ (1971) The synaptic organization in the medial geniculate body of afferent fibres ascending from the inferior colliculus. Z Zellforsch Mikrosk Anat 113:44–66

    CAS  PubMed  Google Scholar 

  • Jousmaki V, Hari R (1998) Parchment-skin illusion: sound-biased touch. Curr Biol: CB 8:R190

    CAS  PubMed  Google Scholar 

  • Kalappa BI, Brozoski TJ, Turner JG, Caspary DM (2014) Single-unit hyperactivity and bursting in the auditory thalamus of awake rats directly correlates with behavioral evidence of tinnitus. J Physiol (in press)

  • Kaltenbach JA (2007) The dorsal cochlear nucleus as a contributor to tinnitus: mechanisms underlying the induction of hyperactivity. Prog Brain Res 166:89–106

    CAS  PubMed  Google Scholar 

  • Kaltenbach JA, Godfrey DA (2008) Dorsal cochlear nucleus hyperactivity and tinnitus: are they related? Am J Audiol 17:S148–S161

    PubMed  Google Scholar 

  • Kanold PO, Manis PB (1999) Transient potassium currents regulate the discharge patterns of dorsal cochlear nucleus pyramidal cells. J Neurosci 19:2195–2208

    CAS  PubMed  Google Scholar 

  • Kayser C, Petkov CI, Augath M, Logothetis NK (2005) Integration of touch and sound in auditory cortex. Neuron 48:373–384

    CAS  PubMed  Google Scholar 

  • Kayser C, Montemurro MA, Logothetis NK, Panzeri S (2009) Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 61:597–608

    CAS  PubMed  Google Scholar 

  • Khorevin VI (1978) Responses of units in the magnocellular part of the medial geniculate body to acoustic and somatosensory stimulation. Neurophysiology 10:89–94

    Google Scholar 

  • Khorevin VI (1980a) Effect of electrodermal stimulation on single unit responses to acoustic stimulation in the parvocellular part of the medial geniculate body. Neurophysiology 12:129–134

    Google Scholar 

  • Khorevin VI (1980b) Interaction between responses evoked by acoustic and somatosensory stimuli in neurons of the magnocellular part of the medial geniculate body. Neurophysiology 12:241–245

    Google Scholar 

  • Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714–1718

    CAS  PubMed  Google Scholar 

  • King AJ (2009) Visual influences on auditory spatial learning. Philos Trans R Soc Lond B 364:331–339

    Google Scholar 

  • Kirzinger A, Jurgens U (1991) Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey. Exp Brain Res 84:545–560

    CAS  PubMed  Google Scholar 

  • Koehler SD, Shore SE (2013) Stimulus timing-dependent plasticity in dorsal cochlear nucleus is altered in tinnitus. J Neurosci 33:19647–19656

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koehler SD, Pradhan S, Manis PB, Shore SE (2011) Somatosensory inputs modify auditory spike timing in dorsal cochlear nucleus principal cells. Eur J Neurosci 33:409–420

    PubMed Central  PubMed  Google Scholar 

  • Kotchabhakdi N, Rinvik E, Walberg F, Yingchareon K (1980) The vestibulothalamic projections in the cat studied by retrograde axonal transport of horseradish peroxidase. Exp Brain Res 40:405–418

    CAS  PubMed  Google Scholar 

  • Kuchenbuch A, Paraskevopoulos E, Herholz SC, Pantev C (2014) Audio-tactile integration and the influence of musical training. PLoS ONE 9:e85743

    PubMed Central  PubMed  Google Scholar 

  • Kujala T, Alho K, Naatanen R (2000) Cross-modal reorganization of human cortical functions. Trends Neurosci 23:115–120

    CAS  PubMed  Google Scholar 

  • Lakatos P, Chen CM, O’Connell MN, Mills A, Schroeder CE (2007) Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53:279–292

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lambertz N, Gizewski ER, de Greiff A, Forsting M (2005) Cross-modal plasticity in deaf subjects dependent on the extent of hearing loss. Brain Res Cogn Brain Res 25:884–890

    PubMed  Google Scholar 

  • Landry SP, Guillemot JP, Champoux F (2013) Temporary deafness can impair multisensory integration: a study of cochlear-implant users. Psychol Sci 24:1260–1268

    PubMed  Google Scholar 

  • Leach ND, Nodal FR, Cordery PM, King AJ, Bajo VM (2013) Cortical cholinergic input is required for normal auditory perception and experience-dependent plasticity in adult ferrets. J Neurosci 33:6659–6671

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ledoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ (1987) Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264:123–146

    CAS  PubMed  Google Scholar 

  • LeDoux JE, Farb C, Ruggiero DA (1990) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10:1043–1054

    CAS  PubMed  Google Scholar 

  • Levine RA (1999) Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. Am J Otolaryngol 20:351–362

    CAS  PubMed  Google Scholar 

  • Levine RA, Abel M, Cheng H (2003) CNS somatosensory-auditory interactions elicit or modulate tinnitus. Exp Brain Res 153:643–648

    CAS  PubMed  Google Scholar 

  • Levine RA, Nam EC, Oron Y, Melcher JR (2007) Evidence for a tinnitus subgroup responsive to somatosensory based treatment modalities. Prog Brain Res 166:195–207

    CAS  PubMed  Google Scholar 

  • Li H, Mizuno N (1997) Single neurons in the spinal trigeminal and dorsal column nuclei project to both the cochlear nucleus and the inferior colliculus by way of axon collaterals: a fluorescent retrograde double-labeling study in the rat. Neurosci Res 29:135–142

    CAS  PubMed  Google Scholar 

  • Linke R, De Lima AD, Schwegler H, Pape HC (1999) Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: possible substrates of a subcortical visual pathway to the amygdala. J Comp Neurol 403:158–170

    CAS  PubMed  Google Scholar 

  • Loftus WC, Malmierca MS, Bishop DC, Oliver DL (2008) The cytoarchitecture of the inferior colliculus revisited: a common organization of the lateral cortex in rat and cat. Neuroscience 154:196–205

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lomber SG, Meredith MA, Kral A (2010) Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nat Neurosci 13:1421–1427

    CAS  PubMed  Google Scholar 

  • Love JA, Scott JW (1969) Some response characteristics of cells of the magnocellular division of the medial geniculate body of the cat. Can J Physiol Pharmacol 47:881–888

    CAS  PubMed  Google Scholar 

  • Lund RD, Webster KE (1967a) Thalamic afferents from the dorsal column nuclei. An experimental anatomical study in the rat. J Comp Neurol 130:301–312

    CAS  PubMed  Google Scholar 

  • Lund RD, Webster KE (1967b) Thalamic afferents from the spinal cord and trigeminal nuclei. An experimental anatomical study in the rat. J Comp Neurol 130:313–328

    CAS  PubMed  Google Scholar 

  • Luo F, Yan J (2013) Sound-specific plasticity in the primary auditory cortex as induced by the cholinergic pedunculopontine tegmental nucleus. Eur J Neurosci 37:393–399

    PubMed  Google Scholar 

  • Lutkenhoner B, Lammertmann C, Simoes C, Hari R (2002) Magnetoencephalographic correlates of audiotactile interaction. NeuroImage 15:509–522

    CAS  PubMed  Google Scholar 

  • Ma X, Suga N (2009) Specific and nonspecific plasticity of the primary auditory cortex elicited by thalamic auditory neurons. J Neurosci 29:4888–4896

    CAS  PubMed Central  PubMed  Google Scholar 

  • Malmierca MS, Merchan MA, Henkel CK, Oliver DL (2002) Direct projections from cochlear nuclear complex to auditory thalamus in the rat. J Neurosci 22:10891–10897

    CAS  PubMed  Google Scholar 

  • Manis PB (1990) Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro. J Neurosci 10:2338–2351

    CAS  PubMed  Google Scholar 

  • Manns JR, Zilli EA, Ong KC, Hasselmo ME, Eichenbaum H (2007) Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol Learn Mem 87:9–20

    PubMed  Google Scholar 

  • Manunta Y, Edeline JM (1999) Effects of noradrenaline on frequency tuning of auditory cortex neurons during wakefulness and slow-wave sleep. Eur JNeurosci 11:2134–2150

    CAS  Google Scholar 

  • Manunta Y, Edeline JM (2004) Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. J Neurophysiol 92:1445–1463

    CAS  PubMed  Google Scholar 

  • Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931

    CAS  PubMed  Google Scholar 

  • Merabet LB, Pascual-Leone A (2010) Neural reorganization following sensory loss: the opportunity of change. Nat Rev Neurosci 11:44–52

    CAS  PubMed Central  PubMed  Google Scholar 

  • Meredith MA (2002) On the neuronal basis for multisensory convergence: a brief overview. Brain Res Cogn Brain Res 14:31–40

    PubMed  Google Scholar 

  • Meredith MA, Allman BL (2009) Subthreshold multisensory processing in cat auditory cortex. Neuroreport 20:126–131

    PubMed Central  PubMed  Google Scholar 

  • Meredith MA, Allman BL (2012) Early hearing-impairment results in crossmodal reorganization of ferret core auditory cortex. Neural Plast 2012:601591

    PubMed Central  PubMed  Google Scholar 

  • Meredith MA, Stein BE (1986) Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. J Neurophysiol 56:640–662

    CAS  PubMed  Google Scholar 

  • Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214:170–197

    CAS  PubMed  Google Scholar 

  • Middlebrooks JC, Knudsen EI (1984) A neural code for auditory space in the cat’s superior colliculus. J Neurosci 4:2621–2634

    CAS  PubMed  Google Scholar 

  • Montemurro MA, Rasch MJ, Murayama Y, Logothetis NK, Panzeri S (2008) Phase-of-firing coding of natural visual stimuli in primary visual cortex. Curr Biol 18:375–380

    CAS  PubMed  Google Scholar 

  • Morest DK (1975) Synaptic relationships of Golgi type II cells in the medial geniculate body of the cat. J Comp Neurol 162:157–193

    CAS  PubMed  Google Scholar 

  • Morest DK, Oliver DL (1984) The neuronal architecture of the inferior colliculus in the cat: defining the functional anatomy of the auditory midbrain. J Comp Neurol 222:209–236

    CAS  PubMed  Google Scholar 

  • Nava E, Bottari D, Villwock A, Fengler I, Buchner A, Lenarz T, Roder B (2014) Audio-tactile integration in congenitally and late deaf cochlear implant users. PLoS ONE 9:e99606

    PubMed Central  PubMed  Google Scholar 

  • Nelken I, Young ED (1997) Linear and nonlinear spectral integration in type IV neurons of the dorsal cochlear nucleus.I Regions of linear interaction. J Neurophysiol 78:790–799

    CAS  PubMed  Google Scholar 

  • Neti C, Young ED, Schneider MH (1992) Neural network models of sound localization based on directional filtering by the pinna. J Acoust Soc Am 92:3140–3156

    CAS  PubMed  Google Scholar 

  • Nishimura H, Hashikawa K, Doi K, Iwaki T, Watanabe Y, Kusuoka H, Nishimura T, Kubo T (1999) Sign language ‘heard’ in the auditory cortex. Nature 397:116

    CAS  PubMed  Google Scholar 

  • Oliver DL (2005) Neuronal organization in the inferior colliculus. In: Winer J, Schreiner C (eds) The inferior colliculus. Springer, New York, pp 69–114

    Google Scholar 

  • Palmer AR, King AJ (1982) The representation of auditory space in the mammalian superior colliculus. Nature 299:248–249

    CAS  PubMed  Google Scholar 

  • Pieper F, Jurgens U (2003) Neuronal activity in the inferior colliculus and bordering structures during vocalization in the squirrel monkey. Brain Res 979:153–164

    CAS  PubMed  Google Scholar 

  • Polley DB, Thompson JH, Guo W (2013) Brief hearing loss disrupts binaural integration during two early critical periods of auditory cortex development. Nat Commun 4:2547

    PubMed Central  PubMed  Google Scholar 

  • Powell EW, Hatton JB (1969) Projections of the inferior colliculus in cat. J Comp Neurol 136:183–192

    CAS  PubMed  Google Scholar 

  • Roberts PD, Portfors CV (2008) Design principles of sensory processing in cerebellum-like structures. Early stage processing of electrosensory and auditory objects. Biol Cybern 98:491–507

    PubMed  Google Scholar 

  • Rogan MT, LeDoux JE (1995) LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit. Neuron 15:127–136

    CAS  PubMed  Google Scholar 

  • Rutishauser U, Ross IB, Mamelak AN, Schuman EM (2010) Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464:903–907

    CAS  PubMed  Google Scholar 

  • Ryugo DK, Weinberger NM (1978) Differential plasticity of morphologically distinct neuron populations in the medical geniculate body of the cat during classical conditioning. Behav Biol 22:275–301

    CAS  PubMed  Google Scholar 

  • Sanchez TG, Rocha CB (2011) Diagnosis and management of somatosensory tinnitus: review article. Clinics (Sao Paulo) 66:1089–1094

    Google Scholar 

  • Schofield B (2011) Central descending auditory pathways. In: Ryugo DK, Fay RR (eds) Auditory and vestibular efferents, vol 38. Springer handbook of auditory research. Springer, New York, pp 261–290

    Google Scholar 

  • Schofield BR, Coomes DL (2006) Pathways from auditory cortex to the cochlear nucleus in guinea pigs. Hear Res 216–217:81–89

    PubMed  Google Scholar 

  • Schofield BR, Motts SD, Mellott JG, Foster NL (2014) Projections from the dorsal and ventral cochlear nuclei to the medial geniculate body. Front Neuroanat 8:10

    PubMed Central  PubMed  Google Scholar 

  • Schroeder CE, Lindsley RW, Specht C, Marcovici A, Smiley JF, Javitt DC (2001) Somatosensory input to auditory association cortex in the macaque monkey. J Neurophysiol 85:1322–1327

    CAS  PubMed  Google Scholar 

  • Schurmann M, Caetano G, Hlushchuk Y, Jousmaki V, Hari R (2006) Touch activates human auditory cortex. NeuroImage 30:1325–1331

    PubMed  Google Scholar 

  • Shore SE (2011) Plasticity of somatosensory inputs to the cochlear nucleus–implications for tinnitus. Hear Res 281:38–46

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shore SE, Zhou J (2006) Somatosensory influence on the cochlear nucleus and beyond. Hear Res 216–217:90–99

    PubMed  Google Scholar 

  • Shore SE, Vass Z, Wys NL, Altschuler RA (2000) Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419:271–285

    CAS  PubMed  Google Scholar 

  • Shore SE, El Kashlan H, Lu J (2003) Effects of trigeminal ganglion stimulation on unit activity of ventral cochlear nucleus neurons. Neuroscience 119:1085–1101

    CAS  PubMed  Google Scholar 

  • Shore SE, Koehler S, Oldakowski M, Hughes LF, Syed S (2008) Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise-induced hearing loss. Eur J Neurosci 27:155–168

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smiley JF, Falchier A (2009) Multisensory connections of monkey auditory cerebral cortex. Hear Res 258:37–46

    PubMed Central  PubMed  Google Scholar 

  • Stein BE, Meredith MA (1990) Multisensory integration.Neural and behavioral solutions for dealing with stimuli from different sensory modalities. Ann N Y Acad Sci 608:51–65, discussion 65–70

    CAS  PubMed  Google Scholar 

  • Stein BE, Wallace MW, Stanford TR, Jiang W (2002) Cortex governs multisensory integration in the midbrain. Neuroscientist 8:306–314

    PubMed  Google Scholar 

  • Sugihara T, Diltz MD, Averbeck BB, Romanski LM (2006) Integration of auditory and visual communication information in the primate ventrolateral prefrontal cortex. J Neurosci 26:11138–11147

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tammer R, Ehrenreich L, Jurgens U (2004) Telemetrically recorded neuronal activity in the inferior colliculus and bordering tegmentum during vocal communication in squirrel monkeys (Saimiri sciureus). Behav Brain Res 151:331–336

    PubMed  Google Scholar 

  • Thornton SK, Withington DJ (1996) The role of the external nucleus of the inferior colliculus in the construction of the superior collicular auditory space map in the guinea-pig. Neurosci Res 25:239–246

    CAS  PubMed  Google Scholar 

  • Tokunaga A, Sugita S, Otani K (1984) Auditory and non-auditory subcortical afferents to the inferior colliculus in the rat. J Hirnforsch 25:461–472

    CAS  PubMed  Google Scholar 

  • Tzounopoulos T, Kim Y, Oertel D, Trussell LO (2004) Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7:719–725

    CAS  PubMed  Google Scholar 

  • Tzounopoulos T, Rubio ME, Keen JE, Trussell LO (2007) Coactivation of pre- and postsynaptic signaling mechanisms determines cell-specific spike-timing-dependent plasticity. Neuron 54:291–301

    CAS  PubMed Central  PubMed  Google Scholar 

  • Van Buskirk RL (1983) Subcortical auditory and somatosensory afferents to hamster superior colliculus. Brain Res Bull 10:583–587

    PubMed  Google Scholar 

  • van Elk M, Lenggenhager B, Heydrich L, Blanke O (2014a) Suppression of the auditory N1-component for heartbeat-related sounds reflects interoceptive predictive coding. Biol Psychol 99:172–182

    PubMed  Google Scholar 

  • van Elk M, Salomon R, Kannape O, Blanke O (2014b) Suppression of the N1 auditory evoked potential for sounds generated by the upper and lower limbs. Biol Psychol 102:108–117

    PubMed  Google Scholar 

  • van Wingerden M, Vinck M, Lankelma J, Pennartz CM (2010) Theta-band phase locking of orbitofrontal neurons during reward expectancy. J Neurosci 30:7078–7087

    PubMed  Google Scholar 

  • Vogler DP, Robertson D, Mulders WH (2014) Hyperactivity following unilateral hearing loss in characterized cells in the inferior colliculus. Neuroscience 265C:28–36

    Google Scholar 

  • von Holst E (1954) Relations between the central Nervous System and the peripheral organs. Br J Anim Behav 2:89–94

    Google Scholar 

  • Wallace MT, Stein BE (2007) Early experience determines how the senses will interact. J Neurophysiol 97:921–926

    PubMed  Google Scholar 

  • Weinberger NM (2011) The medial geniculate, not the amygdala, as the root of auditory fear conditioning. Hear Res 274:61–74

    PubMed Central  PubMed  Google Scholar 

  • Wepsic JG (1966) Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. Exp Neurol 15:299–318

    CAS  PubMed  Google Scholar 

  • Whitton JP, Polley DB (2011) Evaluating the perceptual and pathophysiological consequences of auditory deprivation in early postnatal life: a comparison of basic and clinical studies. J Assoc Res Otolaryngol 12:535–547

    PubMed Central  PubMed  Google Scholar 

  • Winer JA, Larue DT (1987) Patterns of reciprocity in auditory thalamocortical and corticothalamic connections: study with horseradish peroxidase and autoradiographic methods in the rat medial geniculate body. J Comp Neurol 257:282–315

    CAS  PubMed  Google Scholar 

  • Winer JA, Morest DK, Diamond IT (1988) A cytoarchitectonic atlas of the medial geniculate body of the opossum, Didelphys virginiana, with a comment on the posterior intralaminar nuclei of the thalamus. J Comp Neurol 274:422–448

    CAS  PubMed  Google Scholar 

  • Winer JA, Saint Marie RL, Larue DT, Oliver DL (1996) GABAergic feedforward projections from the inferior colliculus to the medial geniculate body. Proc Natl Acad Sci U S A 93:8005–8010

    CAS  PubMed Central  PubMed  Google Scholar 

  • Winer JA, Chernock ML, Larue DT, Cheung SW (2002) Descending projections to the inferior colliculus from the posterior thalamus and the auditory cortex in rat, cat, and monkey. Hear Res 168:181–195

    PubMed  Google Scholar 

  • Yu L, Rowland BA, Stein BE (2010) Initiating the development of multisensory integration by manipulating sensory experience. J Neurosci 30:4904–4913

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zeng C, Nannapaneni N, Zhou J, Hughes LF, Shore S (2009) Cochlear damage changes the distribution of vesicular glutamate transporters associated with auditory and nonauditory inputs to the cochlear nucleus. J Neurosci 29:4210–4217

    CAS  PubMed  Google Scholar 

  • Zeng C, Shroff H, Shore SE (2011) Cuneate and spinal trigeminal nucleus projections to the cochlear nucleus are differentially associated with vesicular glutamate transporter-2. Neuroscience 176:142–151

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zeng C, Yang Z, Shreve L, Bledsoe S, Shore S (2012) Somatosensory projections to cochlear nucleus are upregulated after unilateral deafness. J Neurosci 32:15791–15801

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhan X, Pongstaporn T, Ryugo DK (2006) Projections of the second cervical dorsal root ganglion to the cochlear nucleus in rats. J Comp Neurol 496:335–348

    PubMed Central  PubMed  Google Scholar 

  • Zhang W, Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885–900

    CAS  PubMed  Google Scholar 

  • Zhou J, Shore S (2004) Projections from the trigeminal nuclear complex to the cochlear nuclei: a retrograde and anterograde tracing study in the guinea pig. J Neurosci Res 78:901–907

    CAS  PubMed  Google Scholar 

  • Zhou J, Shore S (2006) Convergence of spinal trigeminal and cochlear nucleus projections in the inferior colliculus of the guinea pig. J Comp Neurol 495:100–112

    PubMed  Google Scholar 

  • Zhou J, Nannapaneni N, Shore S (2007) Vessicular glutamate transporters 1 and 2 are differentially associated with auditory nerve and spinal trigeminal inputs to the cochlear nucleus. J Comp Neurol 500:777–787

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Otolaryngology, Kresge Hearing Research Institute, University of Michigan, Ann Arbor, MI, 48109, USA

    Calvin Wu, Roxana A. Stefanescu, David T. Martel & Susan E. Shore

  2. Department of Molecular and integrative Physiology, Ann Arbor, MI, USA

    Susan E. Shore

  3. Department of Biomedical Engineering, Ann Arbor, MI, USA

    David T. Martel & Susan E. Shore

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  1. Calvin Wu
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  2. Roxana A. Stefanescu
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  3. David T. Martel
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  4. Susan E. Shore
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Correspondence to Susan E. Shore.

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Wu, C., Stefanescu, R.A., Martel, D.T. et al. Listening to another sense: somatosensory integration in the auditory system. Cell Tissue Res 361, 233–250 (2015). https://doi.org/10.1007/s00441-014-2074-7

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