Abstract
The cochlear nucleus (CN) commissural connection represents the first opportunity for convergence of binaural information in the auditory brainstem. All major neuron types in the ventral CN (VCN) are innervated by a diverse population of cells in the contralateral VCN. This study examined the effect of contralateral sound stimulation on the spontaneous rates (SRs) of neurons in the VCN. Unit activity was recorded with silicon-substrate multichannel probes which allowed recordings from up to 16 sites simultaneously. On average, 30% of units showed short-latency (often only 2 ms greater than the latencies of ipsilateral sound-evoked responses) inhibition of SR by wideband contralateral noise bursts. Fewer units (4.5%) were excited by contralateral noise at sound levels low enough to exclude excitation by acoustic crossover. Both regular and irregular units in the anterior VCN (AVCN) and posterior VCN (PVCN) were inhibited by contralateral sound. Decrements in SR followed a monotonic function with increases in contralateral sound level, except where responses could be attributed to acoustic crossover. Restricting the contralateral noise bandwidth resulted in a frequency-specific inhibition, dominated by frequencies at and below the ipsilateral BF of the unit, consistent with anatomical findings of the tonotopic organization of the CN commissural pathway. The latencies of these effects are compatible with mono, di and tri-synaptic connections reflecting CN commissural pathway effects.
Similar content being viewed by others
References
Adams JC (1979a) Identification of cochlear nucleus projections by removal of HRP reaction product. Brain Res 177:165–169
Adams JC (1979b) Ascending projections to the inferior colliculus. J Comp Neurol 183:519–538
Alibardi L (1998) Ultrastructural and immunocytochemical characterization of commissural neurons in the ventral cochlear nucleus of the rat. Anat Anz 180:427–438
Alibardi L (2000) Cytology, synaptology and immunocytochemistry of commissural neurons and their putative axonal terminals in the dorsal cochlear nucleus of the. Anat Anz 182:207–220
Altschuler R, Juiz J, Shore S, Bledsoe S, Helfert R, Wenthold R (1993) Inhibitory amino acid synapses and pathways in the ventral cochlear nucleus. In: Merchan M, Juiz J, Godfrey D, Mugnaini E (eds) The mammalian cochlear nuclei: organization and function. Plenum, New York
Babalian AL, Ryugo DK, Vischer MW, Rouiller EM (1999) Inhibitory synaptic interactions between cochlear nuclei: evidence from an in vitro whole brain study. Neuroreport 10:1913–1917
Babalian AL, Jacomme AV, Doucet JR, Ryugo DK, Rouiller EM (2002) Commissural glycinergic inhibition of bushy and stellate cells in the anteroventral cochlear nucleus. Neuroreport 13:555–558
Benson TE, Brown MC (1990) Synapses formed by olivocochlear axon branches in the mouse cochlear nucleus. J Comp Neurol 295:52–70
Brown MC (1989) Morphology and response properties of single olivocochlear fibers in the guinea pig. Hear Res 40:93–109
Brown MC (1993) Fiber pathways and branching patterns of biocytin-labeled olivocochlear neurons in the mouse brainstem. J Comp Neurol 337:600–613
Brown MC, Benson TE (1992) Transneuronal labeling of cochlear nucleus neurons by HRP-labeled auditory nerve fibers and olivocochlear branches in mice. J Comp Neurol 321:645–665
Brown MC, Pierce S, Berglund AM (1991) Cochlear-nucleus branches of thick (medial) olivocochlear fibers in the mouse: a cochleotopic projection. J Comp Neurol 303:300–315
Brown MC, Liberman MC, Benson TE, Ryugo DK (1988a) Brainstem branches from olivocochlear axons in cats and rodents. J Comp Neurol 278:591–603
Brown MC, Berglund AM, Kiang NY, Ryugo DK (1988b) Central trajectories of type II spiral ganglion neurons. J Comp Neurol 278:581–590
Brown M, K DVR, Guinan JJ (2002) Responses of medial olivocochlear neurons: specifying the interneurons of the reflex pathway. In: Rouiller E, Shore S, Clark S (eds) Central auditory processing—integration with other systems. Ascona, Switzerland
Cant NB, Gaston KC (1982) Pathways connecting the right and left cochlear nuclei. J Comp Neurol 212:313–326
Gibson DJ (1982) Interaural crosstalk in the cat. Hear Res 7:325–333
Godfrey D, Kiang N, Norris B (1975) Single unit activity in the posteroventral cochlear nucleus of the cat. J Comp Neurol 162:247–268
Gummer M, Yates GK, Johnstone BM (1988) Modulation transfer function of efferent neurones in the guinea pig cochlea. Hear Res 36:41–51
Hochfeld P (1973) Binaural interactions in the cat's cochlear nucleus. Master's thesis, Dept Elect Eng MIT, Cambridge, MA
Joris PX, Smith PH (1998) Temporal and binaural properties in dorsal cochlear nucleus and its output tract. J Neurosci 18:10157–10170
Kawase T, Liberman MC (1992) Spatial organization of the auditory nerve according to spontaneous discharge rate. J Comp Neurol 319:312–318
Klinke R, Boerger G, Gruber J (1969) Studies on the functional significance of efferent innervation in the auditory system: afferent neuronal activity as influenced by contralaterally-applied sound. Pflugers Arch Ges Physiol 306:165–175
Liberman MC (1991) Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J Comp Neurol 313:240–258
Liberman MC (1993) Central projections of auditory nerve fibers of differing spontaneous rate, II: Posteroventral and dorsal cochlear nuclei. J Comp Neurol 327:17–36
Liberman MC, Brown MC (1986) Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 24:17–36
Lorente de No R (1933) Anatomy of the eighth nerve: III. General plan of structure of the primary cochlear nuclei. Laryngoscope 43:327–350
Mast TE (1973) Dorsal cochlear nucleus of the chinchilla: excitation by contralateral sound. Brain Res 62:61–70
Ostapoff EM, Benson CG, Saint Marie RL (1997) GABA- and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig. J Comp Neurol 381:500–512
Palmer A, Arnott R, Wallace M, Shackleton T (2002) Ventral cochlear nucleus stellate cells: juxtacellular labelling. In: Rouiller E, Shore S, Clark S (eds) Central auditory processing—integration with other systems. Ascona, Switzerland
Pfalz R (1962) Centrifugal inhibition of afferent secondary neurons in the cochlear nucleus by sound. J Acoust Soc Am 34:1472–1477
Pirsig W, Pfalz R (1967) Neurons in the ventral cochlear nucleus, homolaterally stimulated by electrical stimulation on the base of the cochlear coil: centrifugal inhibition by contralateral sound application (guinea pigs). Arch Klin Exp Ohren Nasen Kehlkopfheilkd 189:135–157
Pirsig W, Pfalz R, Sadanaga M (1968) Postsynaptic auditory crossed efferent inhibition in the ventral cochlear nucleus and the blocking of it by strychnine nitrate (guinea pig). Kumamoto Med J 21:75–82
Rhode W, Smith P (1986a) Encoding timing and intensity in the ventral cochlear nucleus of the cat. J Neurophysiol 56:261–286
Rhode WS, Smith PH (1986b) Encoding timing and intensity in the ventral cochlear nucleus of the cat. J Neurophysiol 56:261–286
Robertson D, Winter IM, Mulders W (2002) Action of olivocochlear collaterals in the cochlear nucleus. In: Rouiller E, Shore S, Clark S (eds) Central auditory processing—integration with other systems. Ascona, Switzerland
Saint Marie RL, Benson CG, Ostapoff EM, Morest DK (1991) Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus. Hear Res 51:11–28
Schofield BR (2001) Origins of projections from the inferior colliculus to the cochlear nucleus in guinea pigs. J Comp Neurol 429:206–220
Schofield BR, Cant NB (1992) Organization of the superior olivary complex in the guinea pig: II. Patterns of projection from the periolivary nuclei to the inferior colliculus. J Comp Neurol 317:438–455
Schofield B, Cant N (1996a) Origins and targets of commissural connections between the cochlear nuclei in guinea pigs. J Comp Neurol 375:128–146
Schofield BR, Cant NB (1996b) Origins and targets of commissural connections between the cochlear nuclei in guinea pigs. J Comp Neurol 375:128–146
Shore S (1995) Recovery of forward masked responses in ventral cochlear nucleus neurons. Hear Res 82:31–43
Shore SE, Moore JK (1998) Sources of input to the cochlear granule cell region in the guinea pig. Hear Res 116:33–42
Shore S, Helfert R, Bledsoe SJ, Altschuler R, Godfrey D (1991) Descending projections to the guinea pig cochlear nucleus. Hear Res 52:255–268
Shore S, Godfrey D, Helfert R, Bledsoe S, Altschuler RA (1992) Connections between cochlear nuclei in the guinea pig. Hear Res 62:16–26
Shore SE, Vass Z, Wys NL, Altschuler RA (2000) Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419:271–285
Smith PH, Rhode WS (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282:595–616
Spangler K, Cant N, Henkel C, Farley G, Warr W (1987a) Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J Comp Neurol 259:452–465
Spangler KM, Cant NB, Henkel CK, Farley GR, Warr WB (1987b) Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J Comp Neurol 259:452–465
Warren EH 3rd, Liberman MC (1989a) Effects of contralateral sound on auditory-nerve responses. I. Contributions of cochlear efferents. Hear Res 37:89–104
Warren EH 3rd, Liberman MC (1989b) Effects of contralateral sound on auditory-nerve responses. II. Dependence on stimulus variables. Hear Res 37:105–121
Wenthold RJ, Zempel JM, Parakkal MH, Reeks KA, Altschuler RA (1986) Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Res 380:7–18
Wenthold RJ, Huie D, Altschuler RA, Reeks KA (1987) Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience 22:897–912
Wickesberg RE (1996) Rapid inhibition in the cochlear nuclear complex of the chinchilla. J Acoust Soc Am 100:1691–1702
Wickesberg RE, Oertel D (1990) Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression. J Neurosci 10:1762–1768
Winter IM, Palmer AR (1990) Responses of single units in the anteroventral cochlear nucleus of the guinea pig. Hear Res 44:161–178
Winter IM, Palmer AR (1995) Level dependence of cochlear nucleus onset unit responses and facilitation by second tones or broadband noise. J Neurophysiol 73:141–159
Wu SH, Oertel D (1984) Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus. J Neurosci 4:1577–1588
Ye Y, Machado DG, Kim DO (2000) Projection of the marginal shell of the anteroventral cochlear nucleus to olivocochlear neurons in the cat. J Comp Neurol 420:127–138
Young E (1998a) Cochlear nucleus. In: Shepherd G (ed) The synaptic organization of the brain. In: The synaptic organization of the brain. Oxford University Press, Oxford, pp 121–158
Young E (1998b) Cochlear nucleus. Oxford University Press, Oxford
Young ED, Brownell WE (1976) Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. J Neurophysiol 39:282–300
Acknowledgements
We are grateful to Mazy Bissinger for excellent histological reconstructions, to Chris Ellinger for invaluable electronic assistance and to Ray Meddis for his penetrating insights and positive suggestions. The center for neural communication technology (CNCT) in the Department of Engineering supplied the multichannel electrodes used in this study. This work was supported by NIH grant NIDCD PO1 DC00078.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Shore, S.E., Sumner, C.J., Bledsoe, S.C. et al. Effects of contralateral sound stimulation on unit activity of ventral cochlear nucleus neurons. Exp Brain Res 153, 427–435 (2003). https://doi.org/10.1007/s00221-003-1610-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-003-1610-6