The severity of developmental hearing loss does not determine the magnitude of synapse dysfunction
Resumé
The loss of auditory experience can disrupt synapse function, particularly when it occurs during development. However, the extent of hearing loss can vary from mild to profound, and the duration of hearing loss can vary from days to years. Here, we asked whether the dysfunction of central auditory synapses scales with the severity of hearing loss. The manipulations range from mild sound attenuation to complete deafferentation at the time of hearing onset. Synapse function is measured in central auditory structures from the cochlear nucleus to cortex. The core finding is that even a ~25 dB attenuation in sensation level produces a quantitatively similar change to synaptic currents and membrane properties, as compared to deafferentation. Therefore, profound changes to central processing may occur even when developmental hearing loss is mild, provided it occurs when sound is first transduced.Referencer
Balakrishnan, V., Becker, M., Lohrke, S., Nothwang, H.G., Guresir, E., and Friauf, E. (2003). “Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem,” J. Neurosci., 23, 4134-4145.
Brenowitz, S., and Trussell, L.O. (2001). “Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus,” J. Neurosci., 21, 9487-9498.
Chirila, F.V., Rowland, K.C., Thompson, J.M., and Spirou, G.A. (2007). “Development of gerbil medial superior olive: integration of temporally delayed excitation and inhibition at physiological temperature,” J. Physiol., 584, 167-190.
Chuhma, N., and Ohmori, H. (1998). “Postnatal development of phase-locked high-fidelity synaptic transmission in the medial nucleus of the trapezoid body of the rat,” J. Neurosci., 18, 512-520.
Dorrn, A.L., Yuan, K., Barker, A.J., Schreiner, C.E., and Froemke, R.C. (2010). “Developmental sensory experience balances cortical excitation and inhibition,” Nature, 465, 932-936.
Fitzgerald, K.K., and Sanes, D.H. (2001). “The development of stimulus coding in the auditory system,” in Physiology of the Ear, 2nd Edition. Edited by E. Jahn and J. Santos-Sacchi (Singular Publishing, San Diego), pp. 215-240.
Gao, H., and Lu, Y. (2008). “Early development of intrinsic and synaptic properties of chicken nucleus laminaris neurons,” Neurosci., 153, 131-143.
Johnson, S.L., Eckrich, T., Kuhn, S., Zampini, V., Franz, C., Ranatunga, K.M., Roberts, T.P., Masetto, S., Knipper, M., Kros, C.J., and Marcotti, W. (2011). “Position-dependent patterning of spontaneous action potentials in immature cochlear inner hair cells,” Nature Neurosci., 14, 711-717.
Jones, T.A., Leake, P.A., Snyder, R.L., Stakhovskaya, O., and Bonham, B. (2007). “Spontaneous discharge patterns in cochlear spiral ganglion cells before the onset of hearing in cats,” J. Neurophys., 98, 1898-1908.
Kandler, K., and Friauf, E. (1995). “Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats,” J. Neurosci., 15, 6890-6904.
Kotak, V.C., and Sanes, D.H. (1997). “Deafferentation of glutamatergic afferents weakens synaptic strength in the developing auditory system,” Eur. J. Neurosci. 9, 2340-2347.
Kotak, V.C., Fujisawa, S., Leem F.A., Karthikeyan, O., Aoki, C., and Sanes, D.H. (2005). “Hearing loss raises excitability in the auditory cortex,” J. Neurosci., 25, 3908-3918.
Kotak, V.C., Breithaupt, A.D., and Sanes, D.H. (2007a). “Developmental hearing loss eliminates long-term potentiation in the auditory cortex,” Proc. Natl. Acad. Sci. USA, 104, 3550-3555.
Kotak, V.C., Sadahiro, M., and Fall, C.P. (2007b) “Developmental expression of endogenous oscillations and waves in the auditory cortex involves calcium, gap junctions, and GABA,” Neurosci., 146, 1629-1639.
Kotak, V.C., Takesian, A.E., and Sanes, D.H. (2008). “Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex,” Cerebral Cortex, 18, 2098-2108.
Kotak, V.C., Péndolam L.M., and Rodríguez-Contreras, A. (2012). “Spontaneous activity in the developing gerbil auditory cortex in vivo involves GABAergic transmission,” Neurosci., 226, 130-144.
Kotak, V.C., Takesian, A.E., MacKenzie, P.C., and Sanes, D.H. (2013). “Rescue of inhibitory synapse function following developmental hearing loss,” PLoS One, 8, e53438.
Kuba, H., Oichi, Y., and Ohmori, H. (2010). “Presynaptic activity regulates Na(+) channel distribution at the axon initial segment,” Nature, 465, 1075-1078.
Magnusson, A.K., Kapfer, C., Grothe, B., and Koch, U. (2005). “Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset,” J. Physiol., 568, 497-512.
Mowery, T.M., Kotak, V.K., and Sanes, D.H. (2013), “Critical period for auditory cortex inhibitory maturation closes by postnatal day 19,” Soc. Neurosci. Abs. 43.
Nakamura, Y., and Takahashi, T. (2007). “Developmental changes in potassium currents at the rat calyx of Held presynaptic terminal,” J. Physiol., 581, 1101-1112.
Oswald, A.M., and Reyes, A.D. (2008). “Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex,” J. Neurophysiol., 99, 2998-3008.
Oswald, A.M., and Reyes, A.D. (2011). “Development of inhibitory timescales in auditory cortex,” Cereb. Cortex, 21, 1351-1361.
Pinto, J.G., Hornby, K.R., Jones, D.G., and Murphy, K.M. (2010). “Developmental changes in GABAergic mechanisms in human visual cortex across the lifespan,” Front. Cell. Neurosci., 4, 16.
Rao, D., Basura, G.J., Roche, J., Daniels, S., Mancilla, J.G., and Manis, P.B. (2010). “Hearing loss alters serotonergic modulation of intrinsic excitability in auditory cortex,” J. Neurophys., 104, 2693-2703.
Sanchez, J.T., Wang, Y., Rubel, E.W., and Barria, A. (2010). “Development of glutamatergic synaptic transmission in binaural auditory neurons,” J. Neurophysiol., 104, 1774-1789.
Sanes, D.H. (1993). “The development of synaptic function and integration in the central auditory system,” J. Neurosci., 13, 2627-2637.
Sanes, D.H., and Walsh, E.J. (1997). “Development of Auditory Processing,” in Development of the Auditory System. Edited by E.W Rubel, A.N. Popper, and R.R. Fay (Springer-Verlag, New York), pp. 271-314.
Sanes, D.H., and Bao, S. (2009). “Tuning up the developing auditory CNS,” Curr. Opin. Neurobiol., 19, 188-199.
Sanes, D.H., and Woolley, S.M.N. (2011). “A behavioral framework to guide research on central auditory development and plasticity,” Neuron, 72, 912-929.
Sanes, D.H. (2013). “Synaptic and cellular consequences of hearing loss,” in Springer Handbook of Auditory Research: Deafness. Edited by A. Kral, R.R. Fay, and A.N. Popper (Springer-Verlag: New York).
Sarro, E.C., Kotak, V.C., Sanes, D.H., and Aoki, C. (2008), “Hearing Loss Alters the Subcellular Distribution of Presynaptic GAD and Postsynaptic GABAA Receptors in the Auditory Cortex,” Cereb. Cortex 18, 2855-2867.
Scott, L.L., Mathews, P.J., and Golding, N.L. (2005). “Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive,” J. Neurosci., 25, 7887-7895.
Takesian, A.E., Kotak, V.C., and Sanes, D.H. (2010). “Presynaptic GABA(B) receptors regulate experience-dependent development of inhibitory short-term plasticity,” J. Neurosci., 30, 2716-2727.
Takesian, A.E., Kotak, V.C., and Sanes, D.H. (2012). “Age-dependent effect of hearing loss on cortical inhibitory synapse function,” J. Neurophys., 107, 937-947.
Taschenberger, H., and von Gersdorff, H. (2000). “Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity,” J. Neurosci., 20, 9162-9173.
Tritsch, N.X., Yi, E., Gale, J.E., Glowatzki, E., and Bergles, D.E. (2007). “The origin of spontaneous activity in the developing auditory system,” Nature, 450, 50-55.
Tritsch, N.X., Rodríguez-Contreras, A., Crins, T.T., Wang, H.C., Borst, J.G., and Bergles, D.E. (2010). “Calcium action potentials in hair cells pattern auditory neuron activity before hearing onset,” Nature Neurosci., 13, 1050-1052.
Vale, C., and Sanes, D.H. (2000). “Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain,” J. Neurosci., 20, 1912-1921.
Vale, C., and Sanes, D.H. (2002). “The effect of bilateral deafness on excitatory synaptic strength in the auditory midbrain,” Eur. J. Neurosci., 16, 2394-2404.
Vale, C., Schoorlemmer, J., and Sanes, D.H. (2003). “Deafness disrupts chloride transport and inhibitory synaptic transmission,” J. Neurosci., 23, 7516-7524.
Xu, H., Kotak, V.C., and Sanes, D.H. (2007). “Conductive hearing loss disrupts synaptic and spike adaptation in developing auditory cortex,” J. Neurosci., 27, 9417-9426.
Xu, H., Kotak, V.C., and Sanes, D.H. (2010). “Normal hearing is required for the emergence of long-lasting inhibitory potentiation in cortex,” J. Neurosci., 30, 331-341.
Brenowitz, S., and Trussell, L.O. (2001). “Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus,” J. Neurosci., 21, 9487-9498.
Chirila, F.V., Rowland, K.C., Thompson, J.M., and Spirou, G.A. (2007). “Development of gerbil medial superior olive: integration of temporally delayed excitation and inhibition at physiological temperature,” J. Physiol., 584, 167-190.
Chuhma, N., and Ohmori, H. (1998). “Postnatal development of phase-locked high-fidelity synaptic transmission in the medial nucleus of the trapezoid body of the rat,” J. Neurosci., 18, 512-520.
Dorrn, A.L., Yuan, K., Barker, A.J., Schreiner, C.E., and Froemke, R.C. (2010). “Developmental sensory experience balances cortical excitation and inhibition,” Nature, 465, 932-936.
Fitzgerald, K.K., and Sanes, D.H. (2001). “The development of stimulus coding in the auditory system,” in Physiology of the Ear, 2nd Edition. Edited by E. Jahn and J. Santos-Sacchi (Singular Publishing, San Diego), pp. 215-240.
Gao, H., and Lu, Y. (2008). “Early development of intrinsic and synaptic properties of chicken nucleus laminaris neurons,” Neurosci., 153, 131-143.
Johnson, S.L., Eckrich, T., Kuhn, S., Zampini, V., Franz, C., Ranatunga, K.M., Roberts, T.P., Masetto, S., Knipper, M., Kros, C.J., and Marcotti, W. (2011). “Position-dependent patterning of spontaneous action potentials in immature cochlear inner hair cells,” Nature Neurosci., 14, 711-717.
Jones, T.A., Leake, P.A., Snyder, R.L., Stakhovskaya, O., and Bonham, B. (2007). “Spontaneous discharge patterns in cochlear spiral ganglion cells before the onset of hearing in cats,” J. Neurophys., 98, 1898-1908.
Kandler, K., and Friauf, E. (1995). “Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats,” J. Neurosci., 15, 6890-6904.
Kotak, V.C., and Sanes, D.H. (1997). “Deafferentation of glutamatergic afferents weakens synaptic strength in the developing auditory system,” Eur. J. Neurosci. 9, 2340-2347.
Kotak, V.C., Fujisawa, S., Leem F.A., Karthikeyan, O., Aoki, C., and Sanes, D.H. (2005). “Hearing loss raises excitability in the auditory cortex,” J. Neurosci., 25, 3908-3918.
Kotak, V.C., Breithaupt, A.D., and Sanes, D.H. (2007a). “Developmental hearing loss eliminates long-term potentiation in the auditory cortex,” Proc. Natl. Acad. Sci. USA, 104, 3550-3555.
Kotak, V.C., Sadahiro, M., and Fall, C.P. (2007b) “Developmental expression of endogenous oscillations and waves in the auditory cortex involves calcium, gap junctions, and GABA,” Neurosci., 146, 1629-1639.
Kotak, V.C., Takesian, A.E., and Sanes, D.H. (2008). “Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex,” Cerebral Cortex, 18, 2098-2108.
Kotak, V.C., Péndolam L.M., and Rodríguez-Contreras, A. (2012). “Spontaneous activity in the developing gerbil auditory cortex in vivo involves GABAergic transmission,” Neurosci., 226, 130-144.
Kotak, V.C., Takesian, A.E., MacKenzie, P.C., and Sanes, D.H. (2013). “Rescue of inhibitory synapse function following developmental hearing loss,” PLoS One, 8, e53438.
Kuba, H., Oichi, Y., and Ohmori, H. (2010). “Presynaptic activity regulates Na(+) channel distribution at the axon initial segment,” Nature, 465, 1075-1078.
Magnusson, A.K., Kapfer, C., Grothe, B., and Koch, U. (2005). “Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset,” J. Physiol., 568, 497-512.
Mowery, T.M., Kotak, V.K., and Sanes, D.H. (2013), “Critical period for auditory cortex inhibitory maturation closes by postnatal day 19,” Soc. Neurosci. Abs. 43.
Nakamura, Y., and Takahashi, T. (2007). “Developmental changes in potassium currents at the rat calyx of Held presynaptic terminal,” J. Physiol., 581, 1101-1112.
Oswald, A.M., and Reyes, A.D. (2008). “Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex,” J. Neurophysiol., 99, 2998-3008.
Oswald, A.M., and Reyes, A.D. (2011). “Development of inhibitory timescales in auditory cortex,” Cereb. Cortex, 21, 1351-1361.
Pinto, J.G., Hornby, K.R., Jones, D.G., and Murphy, K.M. (2010). “Developmental changes in GABAergic mechanisms in human visual cortex across the lifespan,” Front. Cell. Neurosci., 4, 16.
Rao, D., Basura, G.J., Roche, J., Daniels, S., Mancilla, J.G., and Manis, P.B. (2010). “Hearing loss alters serotonergic modulation of intrinsic excitability in auditory cortex,” J. Neurophys., 104, 2693-2703.
Sanchez, J.T., Wang, Y., Rubel, E.W., and Barria, A. (2010). “Development of glutamatergic synaptic transmission in binaural auditory neurons,” J. Neurophysiol., 104, 1774-1789.
Sanes, D.H. (1993). “The development of synaptic function and integration in the central auditory system,” J. Neurosci., 13, 2627-2637.
Sanes, D.H., and Walsh, E.J. (1997). “Development of Auditory Processing,” in Development of the Auditory System. Edited by E.W Rubel, A.N. Popper, and R.R. Fay (Springer-Verlag, New York), pp. 271-314.
Sanes, D.H., and Bao, S. (2009). “Tuning up the developing auditory CNS,” Curr. Opin. Neurobiol., 19, 188-199.
Sanes, D.H., and Woolley, S.M.N. (2011). “A behavioral framework to guide research on central auditory development and plasticity,” Neuron, 72, 912-929.
Sanes, D.H. (2013). “Synaptic and cellular consequences of hearing loss,” in Springer Handbook of Auditory Research: Deafness. Edited by A. Kral, R.R. Fay, and A.N. Popper (Springer-Verlag: New York).
Sarro, E.C., Kotak, V.C., Sanes, D.H., and Aoki, C. (2008), “Hearing Loss Alters the Subcellular Distribution of Presynaptic GAD and Postsynaptic GABAA Receptors in the Auditory Cortex,” Cereb. Cortex 18, 2855-2867.
Scott, L.L., Mathews, P.J., and Golding, N.L. (2005). “Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive,” J. Neurosci., 25, 7887-7895.
Takesian, A.E., Kotak, V.C., and Sanes, D.H. (2010). “Presynaptic GABA(B) receptors regulate experience-dependent development of inhibitory short-term plasticity,” J. Neurosci., 30, 2716-2727.
Takesian, A.E., Kotak, V.C., and Sanes, D.H. (2012). “Age-dependent effect of hearing loss on cortical inhibitory synapse function,” J. Neurophys., 107, 937-947.
Taschenberger, H., and von Gersdorff, H. (2000). “Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity,” J. Neurosci., 20, 9162-9173.
Tritsch, N.X., Yi, E., Gale, J.E., Glowatzki, E., and Bergles, D.E. (2007). “The origin of spontaneous activity in the developing auditory system,” Nature, 450, 50-55.
Tritsch, N.X., Rodríguez-Contreras, A., Crins, T.T., Wang, H.C., Borst, J.G., and Bergles, D.E. (2010). “Calcium action potentials in hair cells pattern auditory neuron activity before hearing onset,” Nature Neurosci., 13, 1050-1052.
Vale, C., and Sanes, D.H. (2000). “Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain,” J. Neurosci., 20, 1912-1921.
Vale, C., and Sanes, D.H. (2002). “The effect of bilateral deafness on excitatory synaptic strength in the auditory midbrain,” Eur. J. Neurosci., 16, 2394-2404.
Vale, C., Schoorlemmer, J., and Sanes, D.H. (2003). “Deafness disrupts chloride transport and inhibitory synaptic transmission,” J. Neurosci., 23, 7516-7524.
Xu, H., Kotak, V.C., and Sanes, D.H. (2007). “Conductive hearing loss disrupts synaptic and spike adaptation in developing auditory cortex,” J. Neurosci., 27, 9417-9426.
Xu, H., Kotak, V.C., and Sanes, D.H. (2010). “Normal hearing is required for the emergence of long-lasting inhibitory potentiation in cortex,” J. Neurosci., 30, 331-341.
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2013-12-15
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Mowery, T. M., Kotak, V. C., & Sanes, D. H. (2013). The severity of developmental hearing loss does not determine the magnitude of synapse dysfunction. Proceedings of the International Symposium on Auditory and Audiological Research, 4, 101–112. Hentet fra https://proceedings.isaar.eu/index.php/isaarproc/article/view/2013-11
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2013/2. Physiological correlates and modeling of auditory plasticity
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