How dopamine shapes representations in auditory cortex

Authors

  • Sebastian Puschmann Biological Psychology, Department of Psychology, European Medical School, Carl-von-Ossietzky Universität Oldenburg, Oldenburg, Germany. Cluster of Excellence “Hearing4all”, Carl von Ossietzky Universität Oldenburg, Oldenburg, Germany Author
  • Tina Weis Biological Psychology, Department of Psychology, European Medical School, Carl-von-Ossietzky Universität Oldenburg. Cognitive and Developmental Psychology, Technical University Kaiserslautern. Author
  • Christiane M. Thiel Biological Psychology, Department of Psychology, European Medical School, Carl-von-Ossietzky Universität Oldenburg. Research Center Neurosensory Science, Carl-von-Ossietzky Universität Oldenburg. Author

DOI:

https://doi.org/10.15517/ap.v28i117.14137

Keywords:

dopamine, auditory, learning, plasticity, neuroimaging

Abstract

The neural representation of sound in the auditory cortex is not invariably predetermined by its  acoustical properties, but it is constantly reshaped while the listener acquires new experiences. Such plastic changes are a prerequisite for lifelong learning and allow some degree of rehabilitation after brain injuries. Several neurotransmitter systems modulate these plastic changes. In this paper, we focus on how the neurotransmitter dopamine modulates learning-related plasticity in auditory cortex, and how animal and human research can complement each other in providing an experimental approach that has relevance for studying mechanisms of recovery of function.

Downloads

Download data is not yet available.

References

Albert, S. J., & Kesselring, J. (2012). Neurorehabilitation of stroke. J Neurol, 259(5), 817-832. doi: 10.1007/s00415-011-6247-y DOI: https://doi.org/10.1007/s00415-011-6247-y

Bakin, J. S., South, D. A., & Weinberger, N. M. (1996). Induction of receptive field plasticity in the auditory cortex of the guinea pig during instrumental avoidance conditioning. Behav Neurosci, 110(5), 905-913. DOI: https://doi.org/10.1037//0735-7044.110.5.905

Bakin, J. S., & Weinberger, N. M. (1996). Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc Natl Acad Sci USA, 93(20), 11219-11224. DOI: https://doi.org/10.1073/pnas.93.20.11219

Bao, S., Chan, V. T., & Merzenich, M. M. (2001). Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature, 412(6842), 79-83. DOI: https://doi.org/10.1038/35083586

Bao, S., Chang, E. F., Woods, J., & Merzenich, M. M.(2004). Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. NatNeurosci, 7(9), 974-981. DOI: https://doi.org/10.1038/nn1293

Bieszczad, K. M., & Weinberger, N. M. (2010). Remodeling the cortex in memory: Increased use of a learning strategy increases the representational area of relevant acoustic cues. Neurobiol Learn Mem, 94(2), 127-144. doi: 10.1016/j.nlm.2010.04.009 DOI: https://doi.org/10.1016/j.nlm.2010.04.009

Blake, D. T., Heiser, M. A., Caywood, M., & Merzenich, M. M. (2006). Experience-dependent adult cortical plasticity requires cognitive association between sensation and reward. Neuron, 52(2), 371-381. DOI: https://doi.org/10.1016/j.neuron.2006.08.009

Blake, D. T., Strata, F., Churchland, A. K., & Merzenich, M. M. (2002). Neural correlates of instrumental learning in primary auditory cortex. Proc Natl Acad Sci USA, 99(15), 10114-10119. DOI: https://doi.org/10.1073/pnas.092278099

Brechmann, A., & Scheich, H. (2005). Hemispheric shifts of sound representation in auditory cortex with conceptual listening. Cerebral Cortex, 15(5), 578-587. DOI: https://doi.org/10.1093/cercor/bhh159

Condon, C. D., & Weinberger, N. M. (1991). Habituation produces frequency-specific plasticity of receptive fields in the auditory cortex. Behavioral Neuroscience, 105(3), 416-430. DOI: https://doi.org/10.1037/0735-7044.105.3.416

Diamond, D. M., & Weinberger, N. M. (1986). Classical conditioning rapidly induces specific changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields. Brain Research, 372(2), 357-360. DOI: https://doi.org/10.1016/0006-8993(86)91144-3

Edeline, J. M., Pham, P., & Weinberger, N. M. (1993). Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behav.Neurosci, 107(4), 539-551. DOI: https://doi.org/10.1037//0735-7044.107.4.539

Fallon, J. B., Irvine, D. R., & Shepherd, R. K. (2008). Cochlear implants and brain plasticity. Hear Res, 238(1-2), 110-117. doi:10.1016/j.heares.2007.08.004 DOI: https://doi.org/10.1016/j.heares.2007.08.004

Froemke, R. C., Carcea, I., Barker, A. J., Yuan, K., Seybold, B. A., Martins, A. R., ... Schreiner, C. E. (2013). Long-term modification of cortical synapses improves sensory perception. Nat Neurosci, 16(1), 79-88. doi: 10.1038/nn.3274 DOI: https://doi.org/10.1038/nn.3274

Froemke, R. C., & Jones, B. J. (2011). Development of auditory cortical synaptic receptive fields. Neurosci Biobehav Rev, 35(10), 2105-2113. doi: 10.1016/j.neubiorev.2011.02.006 DOI: https://doi.org/10.1016/j.neubiorev.2011.02.006

Galvan, V. V., & Weinberger, N. M. (2002). Long-term consolidation and retention of learning-induced tuning plasticity in the auditory cortex of the guinea pig. Neurobiology Learn Mem, 77(1), 78-108. doi:10.1006/nlme.2001.4044 DOI: https://doi.org/10.1006/nlme.2001.4044

Hui, G. K., Wong, K. L., Chavez, C. M., Leon, M.I., Robin, K. M., & Weinberger, N. M. (2009). Conditioned tone control of brain reward behavior produces highly specific representational gain in the primary auditory cortex. Neurobiol Learn Mem, 92(1), 27-34. doi:10.1016/j.nlm.2009.02.008 DOI: https://doi.org/10.1016/j.nlm.2009.02.008

James, W. (1890). The Principles of Psychology. New York, USA: Cosimo. DOI: https://doi.org/10.1037/10538-000

Jancke, L., Gaab, N., Wustenberg, T., Scheich, H., & Heinze, H. J. (2001). Short-term functional plasticity in the human auditory cortex: an fMRI study. Brain Res.Cogn Brain Res., 12(3), 479-485. DOI: https://doi.org/10.1016/S0926-6410(01)00092-1

Kilgard, M. P., & Merzenich, M. M. (1998). Cortical map reorganization enabled by nucleus basalis activity [see comments]. Science, 279(5357), 1714-1718. DOI: https://doi.org/10.1126/science.279.5357.1714

Kilgard, M. P., Vazquez, J. L., Engineer, N. D., & Pandya, P. K. (2007). Experience dependent plasticity alters cortical synchronization. Hear Res, 229(1-2), 171- 179. doi: 10.1016/j.heares.2007.01.005 DOI: https://doi.org/10.1016/j.heares.2007.01.005

Kisley, M. A., & Gerstein, G. L. (2001). Daily variation and appetitive conditioning-induced plasticity of auditory cortex receptive fields. Eur J Neurosci, 13(10), 1993-2003. DOI: https://doi.org/10.1046/j.0953-816x.2001.01568.x

Kluge, C., Bauer, M., Leff, A. P., Heinze, H. J., Dolan, R. J., & Driver, J. (2011). Plasticity of human auditory-evoked fields induced by shock conditioning and contingency reversal. Proc Natl Acad Sci U S A, 108(30), 12545-12550. doi: 10.1073/pnas.1016124108 DOI: https://doi.org/10.1073/pnas.1016124108

Knecht, S., Breitenstein, C., Bushuven, S., Wailke, S., Kamping, S., Floel, A., . . . Ringelstein, E. B. (2004). Levodopa: faster and better word learning in normal humans. Ann.Neurol., 56(1), 20-26. DOI: https://doi.org/10.1002/ana.20125

Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., & Hommer, D. (2001). Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport, 12(17), 3683-3687. DOI: https://doi.org/10.1097/00001756-200112040-00016

Kral, A., & Sharma, A. (2012). Developmental neuroplasticity after cochlear implantation. Trends Neurosci, 35(2), 111-122. doi:10.1016/j.tins.2011.09.004 DOI: https://doi.org/10.1016/j.tins.2011.09.004

Liu, R. C., & Schreiner, C. E. (2007). Auditory cortical detection and discrimination correlates with communicative significance. PLoS Biol, 5(7), e173. doi: 10.1371/journal.pbio.0050173 DOI: https://doi.org/10.1371/journal.pbio.0050173

Ljungberg, T., Apicella, P., & Schultz, W. (1992). Responses of monkey dopamine neurons during learning of behavioral reactions. Journal of Neurophysiology, 67(1), 145-163. DOI: https://doi.org/10.1152/jn.1992.67.1.145

Manunta, Y., & Edeline, J. M. (1997). Effects of noradrenaline on frequency tuning of rat auditory cortex neurons. Eur.J Neurosci, 9(4), 833-847. DOI: https://doi.org/10.1111/j.1460-9568.1997.tb01433.x

Manunta, Y., & Edeline, J. M. (1998). Effects of noradrenaline on rate-level function of auditory cortex neurons: is there a “gating” effect of noradrenaline? Experimental Brain Research, 118(3), 361-372. DOI: https://doi.org/10.1007/s002210050290

Manunta, Y., & Edeline, J. M. (1999). Effects of noradrenaline on frequency tuning of auditory cortex neurons during wakefulness and slow-wave sleep. Eur J Neurosci, 11(6), 2134-2150. DOI: https://doi.org/10.1046/j.1460-9568.1999.00633.x

Manunta, Y., & Edeline, J. M. (2004). Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. Journal of Neurophysiology, 92(3), 1445-1463. DOI: https://doi.org/10.1152/jn.00079.2004

May, A. (2011). Experience-dependent structural plasticity in the adult human brain. [Review]. Trends Cogn Sci, 15(10), 475-482. doi:10.1016/j.tics.2011.08.002 DOI: https://doi.org/10.1016/j.tics.2011.08.002

Meyer, M., Elmer, S., & Jancke, L. (2012). Musical expertise induces neuroplasticity of the planum temporale. Ann N Y Acad Sci, 1252, 116-123. doi:10.1111/j.1749-6632.2012.06450.x DOI: https://doi.org/10.1111/j.1749-6632.2012.06450.x

Miasnikov, A. A., McLin, D., & Weinberger, N. M. (2001). Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity. Neuroreport, 12(7), 1537-1542. DOI: https://doi.org/10.1097/00001756-200105250-00047

Monte-Silva, K., Liebetanz, D., Grundey, J., Paulus, W., & Nitsche, M. A. (2010). Dosage-dependent non-linear effect of L-dopa on human motor cortex plasticity. J Physiol, 588(18), 3415-3424. doi:10.1113/jphysiol.2010.190181 DOI: https://doi.org/10.1113/jphysiol.2010.190181

Moore, D. R., & Shannon, R. V. (2009). Beyond cochlear implants: awakening the deafened brain. [Review]. Nat Neurosci, 12(6), 686-691. doi: 10.1038/nn.2326 DOI: https://doi.org/10.1038/nn.2326

Morris, J. S., Friston, K. J., & Dolan, R. J. (1998). Experience-dependent modulation of tonotopic neural responses in human auditory cortex. Proc.R.Soc.Lond.B.Biol.Sci., 265(1397), 649-657. DOI: https://doi.org/10.1098/rspb.1998.0343

Ohl, F. W., & Scheich, H. (1996). Differential frequency conditioning enhances spectral contrast sensitivity of units in auditory cortex (field Al) of the alert Mongolian gerbil. Eur J Neurosci, 8(5), 1001-1017. DOI: https://doi.org/10.1111/j.1460-9568.1996.tb01587.x

Ohl, F. W., & Scheich, H. (1997). Learning-induced dynamic receptive field changes in primary auditory cortex of the unanaesthetized Mongolian gerbil. J Comp Physiol A, 181(6), 685-696. DOI: https://doi.org/10.1007/s003590050150

Ohl, F. W., & Scheich, H. (2005). Learning-induced plasticity in animal and human auditory cortex. Curr.Opin.Neurobiol., 15(4), 470-477. DOI: https://doi.org/10.1016/j.conb.2005.07.002

Ohl, F. W., Scheich, H., & Freeman, W. J. (2001). Change in pattern of ongoing cortical activity with auditory category learning. Nature, 412(6848), 733-736. DOI: https://doi.org/10.1038/35089076

Pienkowski, M., & Eggermont, J. J. (2011). Cortical tonotopic map plasticity and behavior. Neurosci Biobehav Rev, 35(10), 2117-2128. doi:10.1016/j.neubiorev.2011.02.002 DOI: https://doi.org/10.1016/j.neubiorev.2011.02.002

Polley, D. B., Steinberg, E. E., & Merzenich, M. M. (2006). Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci, 26(18), 4970-4982. doi:10.1523/JNEUROSCI.3771-05.2006 DOI: https://doi.org/10.1523/JNEUROSCI.3771-05.2006

Puschmann, S., Brechmann, A., & Thiel, C. M. (2013). Learning-dependent plasticity in human auditory cortex during appetitive operant conditioning.Hum Brain Mapp, 34(11). 2841-2851. doi:10.1002/hbm.22107 DOI: https://doi.org/10.1002/hbm.22107

Scheich, H., Brechmann, A., Brosch, M., Budinger, E., Ohl, F. W., Selezneva, E., . . . Wetzel, W. (2011). Behavioral semantics of learning and crossmodal processing in auditory cortex: the semantic processor concept. Hear Res, 271(1-2), 3-15. doi:10.1016/j.heares.2010.10.006 DOI: https://doi.org/10.1016/j.heares.2010.10.006

Scheidtmann, K. (2004). Advances in adjuvant pharmacotherapy for motor rehabilitation: Effects of levodopa. Restor Neurol Neurosci, 22(3-5), 393-398. DOI: https://doi.org/10.3233/RNN-2004-00271

Schneider, P., Scherg, M., Dosch, H. G., Specht, H. J.,Gutschalk, A., & Rupp, A. (2002). Morphology of Heschl’s gyrus reflects enhanced activation in the auditory cortex of musicians. Nat Neurosci, 5(7), 688-694. doi: 10.1038/nn871 DOI: https://doi.org/10.1038/nn871

Schreiner, C. E., & Polley, D. B. (2014). Auditory map plasticity: diversity in causes and consequences. Curr Opin Neurobiol, 24C, 143- 56. doi: 10.1016/j.conb.2013.11.009 DOI: https://doi.org/10.1016/j.conb.2013.11.009

Schultz, W., Apicella, P., & Ljungberg, T. (1993). Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. The Journal of Neuroscience, 13(3), 900-913. DOI: https://doi.org/10.1523/JNEUROSCI.13-03-00900.1993

Schultz, W., Dayan, P., & Montague, P. R. (1997). A neural substrate of prediction and reward. Science, 275(5306), 1593-1599. DOI: https://doi.org/10.1126/science.275.5306.1593

Spierer, L., De Lucia, M., Bernasconi, F., Grivel, J., Bourquin, N. M., Clarke, S., & Murray, M. M. (2011). Learning-induced plasticity in human audition: objects, time, and space. Hear Res, 271(1-2), 88-102. doi:10.1016/j.heares.2010.03.086 DOI: https://doi.org/10.1016/j.heares.2010.03.086

Stark, H., & Scheich, H. (1997). Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: a long-term microdialysis study of metabolites. J Neurochem, 68(2), 691-697. DOI: https://doi.org/10.1046/j.1471-4159.1997.68020691.x

Thiel, C. M. (2007). Pharmacological modulation of learning-induced plasticity in human auditory cortex. Restor Neurol Neurosci, 25(3-4), 435-443. DOI: https://doi.org/10.3233/RNN-2007-253426

Thiel, C. M., Bentley, P., & Dolan, R. J. (2002). Effects of cholinergic enhancement on conditioningrelated responses in human auditory cortex. Eur J Neurosci, 16(11), 2199-2206. DOI: https://doi.org/10.1046/j.1460-9568.2002.02272.x

Thiel, C. M., Friston, K. J., & Dolan, R. J. (2002). Cholinergic modulation of experience-dependent plasticity in human auditory cortex. Neuron, 35(3), 567-574. DOI: https://doi.org/10.1016/S0896-6273(02)00801-2

van Wassenhove, V., & Nagarajan, S. S. (2007). Auditory cortical plasticity in learning to discriminate modulation rate. J Neurosci, 27(10), 2663-2672. doi:10.1523/JNEUROSCI.4844-06.2007 DOI: https://doi.org/10.1523/JNEUROSCI.4844-06.2007

Weinberger, N. M. (2004). Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci, 5(4), 279-290. DOI: https://doi.org/10.1038/nrn1366

Weinberger, N. M. (2007). Auditory associative memory and representational plasticity in the primary auditory cortex.. Hear Res, 229(1-2), 54-68. doi: 10.1016/j.heares.2007.01.004 DOI: https://doi.org/10.1016/j.heares.2007.01.004

Weinberger, N. M., Javid, R., & Lepan, B. (1993). Longterm retention of learning-induced receptive-field plasticity in the auditory cortex. Proc Natl Acad Sci USA, 90(6), 2394-2398. DOI: https://doi.org/10.1073/pnas.90.6.2394

Weis, T., Brechmann, A., Puschmann, S., & Thiel, C. M. (2013). Feedback that confirms reward expectation triggers auditory cortex activity. J Neurophysiol, 110(8):1860-8. doi: 10.1152/jn.00128.2013. DOI: https://doi.org/10.1152/jn.00128.2013

Weis, T., Puschmann, S., Brechmann, A., & Thiel, C. M. (2012). Effects of L-dopa during auditory instrumental learning in humans. PLoS One, 7(12), e52504. doi: 10.1371/journal.pone.0052504 DOI: https://doi.org/10.1371/journal.pone.0052504

Wittmann, B. C., Schott, B. H., Guderian, S., Frey, J. U., Heinze, H. J., & Duzel, E. (2005). Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron, 45(3), 459-467. DOI: https://doi.org/10.1016/j.neuron.2005.01.010

Downloads

Published

2014-11-20

How to Cite

Puschmann, S., Weis, T., & Thiel, C. M. (2014). How dopamine shapes representations in auditory cortex. Actualidades En Psicología, 28(117), 67-78. https://doi.org/10.15517/ap.v28i117.14137