Dorsal Cochlear Nucleus September 14, 2005
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1 HST.722 Brain Mechanisms of Speech and Hearing Fall 2005 Dorsal Cochlear Nucleus September 14, 2005 Ken Hancock Dorsal Cochlear Nucleus (DCN) Overview of the cochlear nucleus and its subdivisions Anatomy of the DCN Physiology of the DCN Functional considerations 1
2 The cochlear nucleus DCN VCN AN AN fibers terminate in a tonotopic or cochleotopic pattern DCN 36.0 khz AVCN 10.2 khz PVCN 0.17 khz 2.7 khz 2
3 Major subdivisions of the cochlear nucleus Spherical bushy Octopus Globular bushy Multipolar Summary of pathways originating in the cochlear nucleus Inferior colliculus Lateral lemniscus SBC GBC MA OA Superior olive 3
4 Projections suggest DCN is a different animal than VCN (All roads lead to the inferior colliculus) VCN projects directly to structures dealing with binaural hearing and olivocochlear feedback DCN??? Dorsal Cochlear Nucleus Overview of the cochlear nucleus and its subdivisions DCN projections do not reveal its function Anatomy of the DCN Physiology of the DCN Functional considerations 4
5 DCN Tzounopoulos 2004 cartwheel granule Kanold Young 2001 golgi stellate Somatosensory Auditory Vestibular? vertical? I.C. fusiform auditory nerve giant T D PVCN Dorsal Cochlear Nucleus Overview of the cochlear nucleus and its subdivisions DCN projections do not reveal its function Anatomy of the DCN more complex than other CN subdivisions nonauditory inputs similar organization to cerebellar cortex Physiology of the DCN Functional considerations Eric Young 5
6 Response Map classification scheme ~ Auditory Nerve increasing inhibition Young 1984 DCN: Vertical cells are type II and type III units type II BF type III BF tone noise Narrow V-shaped region of excitation No spontaneous activity Tone response >> noise response V-shaped region of excitation Inhibitory sidebands Evidence: Antidromic stimulation (Young 1980) 6
7 Antidromic stimulation record from neuron shock its axon recording electrode DCN recording electrode fusiform stimulating electrode vertical DAS giant VCN stimulating electrode DCN: Principal cells are type III and type IV units type III type IV spont Evidence: Antidromic stimulation (Young 1980) Intracellular recording and labeling (Rhode et al. 1983, Ding et al. 1996) Island of excitation & Sea of inhibition BF rate-level curve inhibited at high levels Noise rate-level curve ~ monotonic 7
8 Neural circuitry underlying DCN physiology: type II units inhibit type IV units type II BF Young & Brownell 1976 BF tone noise type IV reciprocal responses spont vertical fusiform giant Classic experiment: type II units inhibit type IV units multiunit recording Voigt & Young (1980, 1990) Cross-correlogram type IV firing rate given type II fires at t=0 inhibitory trough type II unit type IV unit Voigt & Young 1980,1990 8
9 DCN physiology so far IV + ~ principal cells auditory nerve ~ vertical cells + II type II units inhibit type IV units BUT this analysis based on pure-tone responses what happens with more general stimuli??? Inhibition from type II units doesn t account for everything Type IV unit response map spectrum level Notch noise stimuli Upper Inhibitory Sideband (DCN responses to broadband stimuli cannot be predicted from responses to tones: nonlinear) Type II units do not respond to notch noise whither the inhibition? Response map has two inhibitory regions? 9
10 DCN notch noise sensitivity due to wideband inhibition Broadband noise Notch noise WBI level level AN input to type IV unit AN input to WBI frequency strong AN input dominates type IV response is excitatory type IV loses greater portion of its excitatory input WBI input dominates type IV response is inhibitory frequency Nelken & Young 1994 PVCN: is the D-stellate cell the wideband inhibitor? broadly-tuned, onset-chopper units are found in the PVCN (Winter & Palmer 1995) typically respond better to broadband noise than to tones such responses arise from radiate or stellate neurons (Smith & Rhode 1989) stellate cells send axons dorsally into the DCN, thus called Dstellate cells (Oertel et al. 1990) D-stellate cells are inhibitory (Doucet & Ryugo 1997) DCN PVCN 10
11 Summary: Circuitry of DCN deep layer Spirou and Young 1991 type II type II W.B.I. W.B.I. reciprocal response properties Summary of DCN anatomy and physiology granule Nonauditory Somatosensory Auditory Vestibular vertical cell type II unit narrowband inhibition fusiform D D-stellate cell onset-chopper wideband inhibition 11
12 Dorsal Cochlear Nucleus Overview of the cochlear nucleus and its subdivisions DCN projections do not reveal its function Anatomy of the DCN more complex than other CN subdivisions nonauditory inputs similar organization to cerebellar cortex Physiology of the DCN diverse response properties complex interconnections highly nonlinear Functional considerations Filtering by the pinna provides cues to sound source location Head Related Transfer Function (HRTF) Outer ear gain Geisler 1998 first notch frequency changes with elevation 12
13 Type IV units are sensitive to HRTF first notch vary notch freq type IV units are inhibited by notches centered on BF null in DCN population response may code for sound source location Physiology Reiss & Young 2005 Behavior May 2000 Young et al Dorsal Cochlear Nucleus Overview of the cochlear nucleus and its subdivisions DCN projections do not reveal its function Anatomy of the DCN more complex than other CN subdivisions receives nonauditory inputs has similar organization to cerebellar cortex Physiology of the DCN diverse response properties complex interconnections highly nonlinear Functional considerations coding sound source location based on pinna cues 13
14 DCN is a cerebellum-like structure Generic cerebellum-like structure descending auditory somatosensory plastic synapses Bell 2001 cochlea Synaptic plasticity: Long-Term Potentiation (LTP) Classical LTP demonstration at the hippocampal CA3-CA1 synapse LTP evoked by tetanic stimulation (mechanism involves NMDA receptors) Tzounopoulos
15 Electric fish provide clues to cerebellum-like function black ghost knifefish (Apteronotus albifrons) electric organ electric organ discharge (EOD) electric fields detected by electric lateral line afferent activity transmitted to electric lateral line lobe (ELL), analogous to DCN Electric fields provide information about nearby objects Water flea (prey) Larger animal (predators, other knifefish) Zakon 2003 BUT the fish generates its own electric fields: tail movements ventilation cerebellum-like ELL helps solve this problem Bell
16 What do cerebellum-like structures do??? Subtract the expected input pattern from the actual input pattern to reveal unexpected or novel features of a stimulus. DCN: pinna movement is expected to shift the first notch, independent of what the sound source is doing Dorsal Cochlear Nucleus Overview of the cochlear nucleus and its subdivisions DCN projections do not reveal its function Anatomy of the DCN more complex than other CN subdivisions nonauditory inputs similar organization to cerebellar cortex Physiology of the DCN diverse response properties complex interconnections highly nonlinear Functional considerations: the DCN may code sound source location based on pinna cues extract novel components of response 16
17 DCN may play a role in tinnitus percept of noise, ringing, buzzing, etc. affects up to 80% of the population 1 in 200 are debilitated So why DCN? Because tinnitus involves plasticity may involve somatosensory effects Levine 1999 Dorsal Cochlear Nucleus Overview of the cochlear nucleus and its subdivisions DCN projections do not reveal its function Anatomy of the DCN more complex than other CN subdivisions nonauditory inputs similar organization to cerebellar cortex Physiology of the DCN diverse response properties complex interconnections highly nonlinear Functional considerations: the DCN may code sound source location based on pinna cues extract novel components of response contribute to tinnitus 17
18 References 1. Bell CC (2001) Memory-based expectations in electrosensory systems. Curr Opin Neurobiol 11: Ding J, Benson TE, Voigt HF (1999) Acoustic and current-pulse responses of identified neurons in the dorsal cochlear nucleus of unanesthetized, decerebrate gerbils. J Neurophysiol 82: Doucet JR, Ryugo DK (1997) Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats. J Comp Neurol 385: Kanold PO, Young ED (2001) Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 21: Levine RA (1999) Somatic (craniocervical) tinnitus and the dorsal cochlear nucleus hypothesis. Am J Otolaryngol 20: May BJ (2000) Role of the dorsal cochlear nucleus in the sound localization behavior of cats. Hear Res 148: Nelken I, Young ED (1994) Two separate inhibitory mechanisms shape the responses of dorsal cochlear nucleus type IV units to narrowband and wideband stimuli. J Neurophysiol 71: Oertel D, Wu SH, Garb MW, Dizack C (1990) Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. J Comp Neurology 295: Reiss LA, Young ED (2005) Spectral edge sensitivity in neural circuits of the dorsal cochlear nucleus. J Neurosci 25: Rhode WS, Oertel D, Smith PH (1983) Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus. J Comp Neurol 213: Smith PH, Rhode WS (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282: Spirou GA, Young ED (1991) Organization of dorsal cochlear nucleus type IV unit response maps and their relationship to activation by band-limited noise. J Neurophysiol 66: Tzounopoulos T, Kim Y, Oertel D, Trussell LO (2004) Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7: Voigt HF, Young ED (1980) Evidence of inhibitory interactions between neurons in the dorsal cochlear nucleus. J Neurophysiol 44: Voigt HF, Young ED (1990) Neural cross-correlation analysis of inhibitory interactions in dorsal cochlear nucleus. J Neurophysiol 64: Weedman DL, Ryugo DK (1996) Projections from auditory cortex to the cochlear nucleus in rats: synapses on granule cell dendrites. J Comp Neurol 371: Winter IM, Palmer AR (1995) Level dependence of cochlear nucleus onset unit responses and facilitation by second tones or broadband noise. J Neurophysiol 73: Wright DD, Ryugo DK (1996) Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. J Comp Neurol 365: Young ED (1980) Identification of response properties of ascending axons from dorsal cochlear nucleus. Brain Research 200: Young ED (1984) Response characteristics of neurons of the cochlear nuclei. In: Hearing Science (Berlin CI, ed), pp San Diego: College-Hill. 21. Young ED, Spirou GA, Rice JJ, Voigt HF (1992) Neural organization and responses to complex stimuli in the dorsal cochlear nucleus. Philos Trans R Soc Lond B Biol Sci 336: Young ED, Davis KA (2001) Circuitry and Function of the Dorsal Cochlear Nucleus. In: Integrative Functions in the Mammalian Auditory Pathway (Oertel D, Popper AN, Fay RR, eds). New York: Springer-Verlag. 23. Zakon HH (2003) Insight into the mechanisms of neuronal processing from electric fish. Curr Opin Neurobiol 13: Zhang S, Oertel D (1994) Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. J Neurophysiol 71:
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