Skip to main content

Advertisement

SpringerLink
Log in

Can homeostatic plasticity in deafferented primary auditory cortex lead to travelling waves of excitation?

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Travelling waves of activity in neural circuits have been proposed as a mechanism underlying a variety of neurological disorders, including epileptic seizures, migraine auras and brain injury. The highly influential Wilson-Cowan cortical model describes the dynamics of a network of excitatory and inhibitory neurons. The Wilson-Cowan equations predict travelling waves of activity in rate-based models that have sufficiently reduced levels of lateral inhibition. Travelling waves of excitation may play a role in functional changes in the auditory cortex after hearing loss. We propose that down-regulation of lateral inhibition may be induced in deafferented cortex via homeostatic plasticity mechanisms. We use the Wilson-Cowan equations to construct a spiking model of the primary auditory cortex that includes a novel, mathematically formalized description of homeostatic plasticity. In our model, the homeostatic mechanisms respond to hearing loss by reducing inhibition and increasing excitation, producing conditions under which travelling waves of excitation can emerge. However, our model predicts that the presence of spontaneous activity prevents the development of long-range travelling waves of excitation. Rather, our simulations show short-duration excitatory waves that cancel each other out. We also describe changes in spontaneous firing, synchrony and tuning after simulated hearing loss. With the exception of shifts in characteristic frequency, changes after hearing loss were qualitatively the same as empirical findings. Finally, we discuss possible applications to tinnitus, the perception of sound without an external stimulus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Notes

  1. The peak values and variances of the Gaussian functions defined in this subsection are chosen so that a tonal stimulus would only excite a small portion of the pyramidal neurons. See the model response to a 723-Hz pure tone in Fig. 8 for an example.

References

  • Basta, D., & Ernest, A. (2004). Noise-induced changes of neuronal spontaneous activity in mice inferior colliculus brain slices. Neuroscience Letters, 368, 297–302.

    Article  PubMed  CAS  Google Scholar 

  • Bhattacharyya, T., & Dayal, V. (1989). Influence of age on hair cell loss in the rabbit cochlea. Hearing Research, 40, 179–183.

    Article  PubMed  CAS  Google Scholar 

  • Brozoski, T., Bauer, C., & Caspary, D. (2002). Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. Journal of Neuroscience, 22, 2383–2390.

    PubMed  CAS  Google Scholar 

  • Bruce, I., Bajaj, H., & Ko, J. (2003). Lateral-inhibitory-network models of tinnuts. In Proceedings of the 5th IFAC symposium on modeling and control in biomedical systems (pp. 359–363). Dordrecht: Elsevier.

    Google Scholar 

  • Burrone, J., & Murthy, V. (2003). Synaptic gain control and homeostasis. Current Opinion in Neurobiology, 13, 560–567.

    Article  PubMed  CAS  Google Scholar 

  • Calford, M. (2002). Dynamic representational plasticity in sensory cortex. Neuroscience, 111, 709-738.

    Article  PubMed  CAS  Google Scholar 

  • Calford, M., Rajan, R., & Irvine, D. R. F. (1993). Rapid changes in the frequency tuning of neurons in cat aduitory cortex resulting from pure-tone-induced temporary threshold shift. Neuroscience, 55(4), 953-964.

    Article  PubMed  CAS  Google Scholar 

  • Charles, A. & Brennan, K. (2009). Cortical spreading depression-new insights and persistent questions. Cephalagia, 29(10), 1115–1124.

    Article  CAS  Google Scholar 

  • Chen, Q., & Jen, P. (2000). Bicuculline application affects discharge patterns, rate-intensity functions, and frequency tuning characteristics of bat auditory cortical neurons. Hearing Research, 150, 161–174.

    Article  PubMed  CAS  Google Scholar 

  • Cheung, S., Bedenbaugh, P., Nagarajan, S., & Schreiner, C. (2001). Functional organization of squirrel monkey primary auditory cortex: Responses to pure tones. Journal of Neurophysiology, 85, 1732–1749.

    PubMed  CAS  Google Scholar 

  • Dayan, P., & Abbott, L. F. (2005). Theoretical neuroscience: Computational and mathematical modeling of neural systems. The MIT Press.

  • Desai, N., Cudmore, R., Nelson, S., & Turrigiano, G. (2002). Critical periods for experience-dependent synaptic scaling in visual cortex. Nature Neuroscience, 5, 783–789.

    PubMed  CAS  Google Scholar 

  • Dietrich, V., Nieschalk, M., Stoll, W., Rajan, R., & Pantev, C. (2001). Cortical reorganization in patients with high frequency cochlear hearing loss. Hearing Research, 158, 95–101.

    Article  PubMed  CAS  Google Scholar 

  • Dominguez, M., Becker, S., Bruce, I., & Read, H. (2006). A spiking neuron model of cortical correlates of sensorineural hearing loss: Spontaneous firing, synchrony and tinnitus. Neural computation, 18(12), 2942–2958.

    Article  PubMed  Google Scholar 

  • Douglas, R., & Martin, K. (1998). Neocortex. In G. M. Shepherd (Ed.), The synaptic organization of the brain (pp. 459–509). New York: Oxford University Press.

    Google Scholar 

  • Eggermont, J. (2000). Sound induced correlation of neural activity between and within three auditory cortical areas. Journal of Neurophysiology, 83, 2708–2722.

    PubMed  CAS  Google Scholar 

  • Eggermont, J. (2003). Central Tinnitus. Auris Nass Larynx, 30, 7–12.

    Article  Google Scholar 

  • Eggermont, J. (2005). Tinnitus: Neurobiological substrates. Drug Discovery Today 19, 1283–1290.

    Article  Google Scholar 

  • Eggermont, J., & Roberts L. E. (2004). The neuroscience of Tinnitus. Trends in Neurosciences, 27, 676–682.

    Article  PubMed  CAS  Google Scholar 

  • Foeller, E., Vater, M., & Kossl, M. (2001). Laminar analysis of inhibition in the gerbil primary auditory cortex. Journal of the Association for Research in Otolaryngology, 2(3), 279–296.

    PubMed  CAS  Google Scholar 

  • Fröhlich, F., Bazhenow, M., & Sejnowski, T. (2008). Pathological effect of homeostatic synaptic scaling on network dynamics in diseases of the cortex. Journal of Neuroscience, 28(7), 1709–1720.

    Article  PubMed  Google Scholar 

  • Gerken, G. (1996). Central tinnitus and lateral inhibition: An auditory brainstem model. Hearing Research, 97, 75–83.

    PubMed  CAS  Google Scholar 

  • Gestner, W., & Kistler, W. (2002). Spiking neuron models: Single neurons, populations, plasticity. Cambridge University Press.

  • Greenwood, D. (1990). A cochlear frequency-position function for several species-29 years later. Journal of the Acoustical Society of America, 87, 2592–2605.

    Article  PubMed  CAS  Google Scholar 

  • Houweling, A., Bazhenov, M., Timofeev, I., Steriade, M., & Sejnowski, T. (2005). Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. Cerebral Cortex, 15, 834–845.

    Article  PubMed  Google Scholar 

  • Hwa, T., & Kardar, M. (1992). Avalanches, hydrodynamics, and discharge events in models of sandpiles. Physical Review A, 45, 7002–7023.

    Article  PubMed  Google Scholar 

  • Jones, E. (1995). Overview: Basic elements of the cortical network. In M. J. Gutnick & I. Moody (Ed.), The Cortical Neuron (pp. 111–122). New York: Oxford University Press.

    Google Scholar 

  • Kaltenbach, J. (2000). Neurophysiologic mechanisms of Tinnitus. Journal of the American Academy of Audiology, 11, 125–137.

    PubMed  CAS  Google Scholar 

  • Kaltenbach, J., Zacharek, M., Zhang, J., & Frederick, S. (2004). Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure. Neuroscience Letters, 355, 121–125.

    Article  PubMed  CAS  Google Scholar 

  • Kilman, V., van Rossum, M., & Turrigiano, G. (2002). Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABA(A) receptors clustered at neocortical synapses. Journal of Neuroscience, 22, 1328–1337.

    PubMed  CAS  Google Scholar 

  • Komiya, H., & Eggermont, J. (2000). Spontaneous firing activity of cortical neurons in adult cats with reorganized tonotopic map following pure-tone trauma. Acta Otorhinolaryngologica, 120, 750–756.

    Article  CAS  Google Scholar 

  • Konig, O., Schaette, R., Kempter, R., & Gross, M. (2006). Course of hearing loss and occurrence of tinnitus. Hearing Research, 221, 59–64.

    Article  PubMed  Google Scholar 

  • Kotak, V., Fujisawa, S., Lee, F., Aoki, C., & Sanes D. (2005). Hearing loss raises excitability in the auditory cortex. Journal of Neuroscience, 25, 3908–3918.

    Article  PubMed  CAS  Google Scholar 

  • Liberman, M. (1987). Chronic ultrastructural changes in acoustic trauma: Serial-section reconstruction of stereocilia and cuticular plates. Hearing Research, 26, 65–88.

    Article  PubMed  CAS  Google Scholar 

  • Leslie, K., Nelson, S., & Turrigiano, G. (2001). Postsynaptic depolarization scales quantal amplitude in cortical pyramidal neurons. Journal of Neuroscience, 21, 1–6.

    Google Scholar 

  • Lu, Y., & Jen, P. (2001). GABAergic and glycinergic neural inhibition in excitatory frequency tuning of bat inferior collicular neurons. Experimental Brain Research, 141, 331–339.

    Article  CAS  Google Scholar 

  • Markram, H., Lubke, J., Frotscher, M., & Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213–215.

    Article  PubMed  CAS  Google Scholar 

  • Merzenich, M., Knight, P., & Roth, G. (1975). Representation of cochlea within primary auditory cortex in the cat. Journal of Neuroscience, 38, 231–249.

    CAS  Google Scholar 

  • Miller, L., Escabi, M., Read, H., & Schreiner, C. (2001). Functional convergence of response properties in the auditory thalamocortical system. Neuron, 32, 151–160.

    Article  PubMed  CAS  Google Scholar 

  • Milner, P. M. (1958). Note on a possible correspondence between the scotomas of migraine and spreading depression of Leao. Electroencephalography and Clinical Neurophysiology, 10, 705.

    Article  PubMed  CAS  Google Scholar 

  • Muhlnickel, W., Elbert, T., Taub, E., & Flor, H. (1998). Reorganization of auditory cortex in tinnitus. Proceedings of the National Academy of Sciences, 95, 10340–10343.

    Article  CAS  Google Scholar 

  • Muly, S., Gross, J., & Potashner, S. (2004). Noise trauma alters D-[3H]aspartate release and AMPA binding in chinchilla cochlear nucleus. Journal of Neuroscience Research, 75, 585–596.

    Article  PubMed  CAS  Google Scholar 

  • Noreña, A. & Eggermont, J. (2003). Changes in spontaneous neural activity immediately after an acoustic trauma: Implications for neural correlates of tinnitus. Hearing Research, 183, 137–153.

    Article  PubMed  Google Scholar 

  • Noreña, A., Tomita M., & Eggermont, J. (2003). Neural changes in cat auditory cortex after a transient pure-tone trauma. Journal of Neurophysiology, 90, 2387–2401.

    Article  PubMed  Google Scholar 

  • Ottaviani, F., Di Girolamo, S., Briglia, G., De Rossi, G., Di Giuda, D., & Di Nardo, W. (1997). Tonotopic organization of human auditory cortex analyzed by SPET. Audiology, 36, 241–248.

    Article  PubMed  CAS  Google Scholar 

  • Parra, L. C. & Pearlmutter, B. A. (2007). Illusory percepts from auditory adaptation. Journal of the Acoustical Society of America, 121, 1632–1641.

    Article  PubMed  Google Scholar 

  • Phillips, D., & Irvine, D. (1981). Responses of single neurons in physiologically defined primary auditory cortex AI of the cat: Frequency tuning and responses to intensity. Journal of Neurophysiology, 45, 48–58.

    PubMed  CAS  Google Scholar 

  • Popelar, J., Erre, J., Aran, J., & Cazals, Y. (1994). Plastic changes in ipsicontralateral differences of auditory cortex and inferior colliculus evoked potentials after injury to one ear in the adult guinea pig. Hearing Research, 72, 125–134.

    Article  PubMed  CAS  Google Scholar 

  • Rajan, R. (1998). Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nature Neuroscience, 1, 138–143.

    Article  PubMed  CAS  Google Scholar 

  • Rajan, R. (2001). Plasticity of excitation and inhibition in the receptive field of primary auditory cortical neurons after limited receptor organ damage. Cerebral Cortex, 11, 171–182.

    Article  PubMed  CAS  Google Scholar 

  • Rajan, R., Irvine, R., Wise, L., & Heil, P. (1993). Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex. Journal of Comparative Neurology, 338, 17–49.

    Article  PubMed  CAS  Google Scholar 

  • Read, H., Winer, J., & Schreiner, C. (2002). Functional architecture of the auditory cortex. Current Opinion in Neurobiology, 12, 433–440.

    Article  PubMed  CAS  Google Scholar 

  • Riegle, K., & Meyer, R. (2007). Rapid homeostatic plasticity in the intact adult visual system. Journal of Neuroscience, 27, 10556–10567.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, D., & Irvine, D. R. F. (1989). Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. Journal of Comparative Neurology, 282, 456–471.

    Article  PubMed  CAS  Google Scholar 

  • van Rossum, M., Bi, G., & Turrigiano, G. (2000). Stable Hebbian learning from spike-timing dependent plasticity. Journal of Neuroscience, 20, 8812–8821.

    PubMed  Google Scholar 

  • Rutherford, L., Dewan, A., Lauer, H., & Turrigiano G. (1997). Brain-deprived neutrotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. Journal of Neuroscience, 17, 4527–4535.

    PubMed  CAS  Google Scholar 

  • Rutherford, L., Nelson, S., & Turrigiano, G. (1998). Opposite effects of BDNF on the quantal amplitude of pyramidal and interneuron excitatory synapses. Neuron, 21, 521–530.

    Article  PubMed  CAS  Google Scholar 

  • Salvi, R., Henderson, D., Hamernik, R., & Parkins, C. (1980). VIII nerve response to click stimuli in normal and pathological cochleas. Hearing Research, 2, 335–342.

    Article  PubMed  CAS  Google Scholar 

  • Salvi, R., Wang, J., & Ding, D. (2000). Auditory plasticity and hyperactivity following cochlear damage. Hearing Research, 147, 261–274.

    Article  PubMed  CAS  Google Scholar 

  • Schaette, R., & Kempter, R. (2006). Development of tinnitus-related neuronal hyperactivity through homeostatic plasticity after hearing loss: a computational model. European Journal of Neuroscience, 23, 3124–3138.

    Article  PubMed  Google Scholar 

  • Schreiner, C., Read, H., & Sutter, M. (2000). Modular organization of frequency integration in primary auditory cortex. Annual Review of Neuroscience, 23, 501–529.

    Article  PubMed  CAS  Google Scholar 

  • Seki, S., & Eggermont, J. (2002). Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss. Hearing Research, 173, 172–186.

    Article  PubMed  Google Scholar 

  • Seki, S., & Eggermont, J. (2003). Changes in spontaneous activity firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hearing Research, 180, 28–38.

    Article  PubMed  Google Scholar 

  • Suneja, S., Benson, C., & Potashner, S. (1998a). Glycine receptors in adult guinea pig brain stem auditory nuclei: Regulation after unilateral cochlear ablation. Experimental Neurology, 154, 473–488.

    Article  PubMed  CAS  Google Scholar 

  • Suneja, S., Potashner, S., & Benson, C. (1998b). Plastic changes in glycine and GABA release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Experimental Neurology, 151, 273–288.

    Article  PubMed  CAS  Google Scholar 

  • Takano, T., Tian, G. F., Peng, W., Lou, N., Lovatt, D., Hansen, A. J., et al. (2007). Cortical spreading depression causes and coincides with tissue hypoxia. Nature Neuroscience, 10(6), 754–762.

    Article  PubMed  CAS  Google Scholar 

  • Turner, J., Hughes, L., & Caspary, D. (2005). Divergent response properties of layer-V neurons in rat primary auditory cortex. Hearing Research, 202, 129–140.

    Article  PubMed  Google Scholar 

  • Turrigiano, G., Leslie, K., Desai, N., Rutherford, L., & Nelson, S. (1998). Activity dependent scaling of quantal amplitude in neocortical pyamidal neurons. Nature, 391, 892–895.

    Article  PubMed  CAS  Google Scholar 

  • Vale, C., & Sanes, D. (2002). The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus. European Journal of Neuroscience, 16, 2394–2404.

    Article  PubMed  Google Scholar 

  • Wang, J., Salvi, R., & Powers, N. (1996). Plasticity of response properties of inferior colliculus neurons following acute cochlear damage. Journal of Neurophysiology, 75, 171–183.

    PubMed  CAS  Google Scholar 

  • Wang, J., Ding, D., & Salvi, R. (2002). Functional reorganization in chinchilla inferior colliculus associated with chronic and cochlear damage. Hearing Research, 168, 238–249.

    Article  PubMed  Google Scholar 

  • Wehr and Zador (2003). Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature, 426, 442–446.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, H. (1999). Spikes, decisions and actions: dyanmic foundations of neuroscience. Oxford University Press.

  • Wilson, H., & Cowan, J. (1972). Excitatory and inhibitory interactions in localized populations of model neurons. Biophysical Journal, 12, 1–24.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, H., & Cowan, J. (1973). A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Kybernetics, 13, 55–80.

    Article  CAS  Google Scholar 

  • Wilson, H., Blake, R., & Lee, S. (2001). Dynamics of travelling waves in visual perception. Nature, 412, 907–910.

    Article  PubMed  CAS  Google Scholar 

  • Zilany, M., & Bruce, I. (2006). Modeling auditory-nerve responses for high sound pressure levels in the normal and impaired auditory periphery. Journal of the Acoustical Society of America, 120, 1446–1466.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to express their gratitude to the reviewers for important feedback and advice, and to Dr. Jos J. Eggermont for his critical comments on earlier versions of this manuscript.

Author information

Authors and Affiliations

  1. McMaster Integrative Neuroscience Discovery & Study, McMaster University, 1280 Main Street West, Hamilton, ON, Canada, L8S 4K1

    Michael Chrostowski

  2. Department of Electrical and Computer Engineering, McMaster University, 1280 Main Street West, Hamilton, ON, Canada, L8S 4K1

    Le Yang & Ian C. Bruce

  3. Center for Vision Research, York University, 4700 Keele Street, Toronto, ON, Canada, M3J 1P3

    Hugh R. Wilson

  4. Department of Psychology, Neuroscience and Behaviour, McMaster University, 1280 Main Street West, Hamilton, ON, Canada, L8S 4K1

    Suzanna Becker

Authors
  1. Michael Chrostowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Le Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hugh R. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ian C. Bruce
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Suzanna Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Chrostowski.

Additional information

Action Editor: S. A. Shamma

This research was supported by a New Emerging Teams Grant from the Canadian Institutes of Health Research to S.B. and I.B. and Discovery grants from the Natural Sciences and Engineering Research Council of Canada to S.B and I.B.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chrostowski, M., Yang, L., Wilson, H.R. et al. Can homeostatic plasticity in deafferented primary auditory cortex lead to travelling waves of excitation?. J Comput Neurosci 30, 279–299 (2011). https://doi.org/10.1007/s10827-010-0256-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-010-0256-1

Keywords

Search

Navigation