Abstract
Sensory environments are known to shape nervous system organization. Here we show that passive long-term exposure to a spectrally enhanced acoustic environment (EAE) causes reorganization of the tonotopic map in juvenile cat auditory cortex without inducing any hearing loss. The EAE consisted of tone pips of 32 different frequencies (5–20 kHz), presented in random order at an average rate of 96 Hz. The EAE caused a strong reduction of the representation of EAE frequencies and an over-representation of frequencies neighboring those of the EAE. This is in sharp contrast with earlier developmental studies showing an enlargement of the cortical representation of EAEs consisting of a narrow frequency band. We observed fewer than normal appropriately tuned short-latency responses to EAE frequencies, together with more common long-latency responses tuned to EAE-neighboring frequencies.
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03 August 2006
added eacute
References
Buonomano, D.V. & Merzenich, M.M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149–186 (1998).
Doupe, A.J. & Kuhl, P.K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999).
Kanwal, J.S. Processing species-specific calls by combination-sensitive neurons in an echolocating bat. in The Design of Animal Communication (eds. Hauser, M. & Konishi, M.) 133–157 (MIT Press, Cambridge, Massachusetts, 1999).
Feng, A.S. & Ratnam, R. Neural basis of hearing in real-world situations. Annu. Rev. Psychol. 51, 699–725 (2000).
Krishnan, A., Xu, Y., Gandour, J. & Cariani, P. Encoding of pitch in the human brainstem is sensitive to language experience. Brain Res. Cogn. Brain Res. 25, 161–168 (2005).
Kilgard, M.P. & Merzenich, M.M. Plasticity of temporal information processing in the primary auditory cortex. Nat. Neurosci. 1, 727–731 (1998).
Kilgard, M.P., Pandya, P.K., Engineer, N.D. & Moucha, R. Cortical network reorganization guided by sensory input features. Biol. Cybern. 87, 333–343 (2002).
Zhang, L.I., Bao, S. & Merzenich, M.M. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat. Neurosci. 4, 1123–1130 (2001).
Weinberger, N.M. Dynamic regulation of receptive fields and maps in the adult sensory cortex. Annu. Rev. Neurosci. 18, 129–158 (1995).
Edeline, J.M. Learning-induced physiological plasticity in the thalamo-cortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms. Prog. Neurobiol. 57, 165–224 (1999).
Weinberger, N.M., Javid, R. & Lepan, B. Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. Proc. Natl. Acad. Sci. USA 90, 2394–2398 (1993).
Bakin, J.S. & Weinberger, N.M. Induction of physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. USA 93, 11219–11224 (1996).
Bao, S., Chan, V.T. & Merzenich, M.M. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412, 79–83 (2001).
Sanes, D.H. & Constantine-Paton, M. The sharpening of frequency tuning curves requires patterned activity during development in the mouse, Mus musculus. J. Neurosci. 5, 1152–1166 (1985).
Zhang, L.I., Bao, S. & Merzenich, M.M. Disruption of primary auditory cortex by synchronous auditory inputs during a critical period. Proc. Natl. Acad. Sci. USA 99, 2309–2314 (2002).
Bao, S., Chang, E.F., Davis, J.D., Gobeske, K.T. & Merzenich, M.M. Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex. J. Neurosci. 23, 10765–10775 (2003).
Robertson, D. & Irvine, D.R. Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J. Comp. Neurol. 282, 456–471 (1989).
Rajan, R., Irvine, D.R., Wise, L.Z. & Heil, P. Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex. J. Comp. Neurol. 338, 17–49 (1993).
Noreña, A.J. & Eggermont, J.J. Enriched acoustic environment after noise trauma reduces hearing loss and prevents cortical map reorganization. J. Neurosci. 25, 699–705 (2005).
Kamke, M.R., Brown, M. & Irvine, D.R. Basal forebrain cholinergic input is not essential for lesion-induced plasticity in mature auditory cortex. Neuron 48, 675–686 (2005).
Liberman, M.C. Auditory-nerve response from cats raised in a low-noise chamber. J. Acoust. Soc. Am. 63, 442–455 (1978).
Noreña, A. & Eggermont, J.J. Comparison between local field potentials and unit cluster activity in primary auditory cortex and anterior auditory field in the cat. Hear. Res. 166, 202–213 (2002).
Stanton, S.G. & Harrison, R.V. Abnormal cochleotopic organization in the auditory cortex of cats reared in a frequency augmented environment. Aud. Neurosci. 2, 97–107 (1996).
Eggermont, J.J. & Komiya, H. Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood. Hear. Res. 142, 89–101 (2000).
Brosch, M. & Schreiner, C.E. Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 77, 923–943 (1997).
Kadia, S.C. & Wang, X. Spectral integration in A1 of awake primates: neurons with single- and multipeaked tuning characteristics. J. Neurophysiol. 89, 1603–1622 (2003).
Wehr, M. & Zador, A.M. Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47, 437–445 (2005).
Eggermont, J.J. The magnitude and phase of temporal modulation transfer functions in cat auditory cortex. J. Neurosci. 19, 2780–2788 (1999).
Noreña, A.J., Tomita, M. & Eggermont, J.J. Neural changes in cat auditory cortex after a transient pure-tone trauma. J. Neurophysiol. 90, 2387–2401 (2003).
Abbott, L.F. & Nelson, S.B. Synaptic plasticity: taming the beast. Nat. Neurosci. suppl. Suppl, 1178–1183 (2000).
Feldman, D.E. Inhibition and plasticity. Nat. Neurosci. 3, 303–304 (2000).
Shamma, S.A. & Symmes, D. Patterns of inhibition in auditory cortical cells in awake squirrel monkeys. Hear. Res. 19, 1–13 (1985).
Volkov, I.O. & Galazjuk, A.V. Formation of spike response to sound tones in cat auditory cortex neurons: interaction of excitatory and inhibitory effects. Neuroscience 43, 307–321 (1991).
Nakahara, H., Zhang, L.I. & Merzenich, M.M. Specialization of primary auditory cortex processing by sound exposure in the “critical period”. Proc. Natl. Acad. Sci. USA 101, 7170–7174 (2004).
Romand, R. Modification of tonotopic representation in the auditory system during development. Prog. Neurobiol. 51, 1–17 (1997).
Eggermont, J.J. Differential maturation rates for response parameters in cat primary auditory cortex. Aud. Neurosci. 2, 309–327 (1996).
Bonham, B.H., Cheung, S.W., Godey, B. & Schreiner, C.E. Spatial organization of frequency response areas and rate/level functions in the developing AI. J. Neurophysiol. 91, 841–854 (2004).
Cragg, B.G. The development of synapses in the visual system of the cat. J. Comp. Neurol. 160, 147–166 (1975).
Tsumoto, T. & Suda, K. Laminar differences in development of afferent innervation to striate cortex neurones in kittens. Exp. Brain Res. 45, 433–446 (1982).
Winfield, D.A. The postnatal development of synapses in the different laminae of the visual cortex in the normal kitten and in kittens with eyelid suture. Brain Res. 285, 155–169 (1983).
Mitzdorf, U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65, 37–100 (1985).
Nowak, L.G. & Bullier, J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp. Brain Res. 118, 477–488 (1988).
Darian-Smith, C. & Gilbert, C.D. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J. Neurosci. 15, 1631–1647 (1995).
Fox, K. Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111, 799–814 (2002).
Blake, D.T. & Merzenich, M.M. Changes of AI receptive fields with sound density. J. Neurophysiol. 88, 3409–3420 (2002).
Ngan, E.M. & May, B.J. Relationship between the auditory brainstem response and auditory nerve thresholds in cats with hearing loss. Hear. Res. 156, 44–52 (2001).
Eggermont, J.J. Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation, and age. J. Neurophysiol. 68, 1216–1228 (1992).
Tomita, M. & Eggermont, J.J. Cross-correlation and joint spectro-temporal receptive field properties in auditory cortex. J. Neurophysiol. 93, 378–392 (2005).
Eggermont, J.J. & Smith, G.M. Separating local from global effects in neural pair correlograms. Neuroreport 6, 2121–2124 (1995).
Eggermont, J.J. & Smith, G.M. Neural connectivity only accounts for a small part of neural correlation in auditory cortex. Exp. Brain Res. 110, 379–391 (1996).
Acknowledgements
This work was supported by the Alberta Heritage Foundation for Medical Research, the National Sciences and Engineering Research Council, a Canadian Institutes of Health–New Emerging Team grant, and the Campbell McLaurin Chair for Hearing Deficiencies.
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Noreña, A., Gourévitch, B., Aizawa, N. et al. Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex. Nat Neurosci 9, 932–939 (2006). https://doi.org/10.1038/nn1720
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DOI: https://doi.org/10.1038/nn1720
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