The unique role of the non-lemniscal pathway on stimulus-specific adaptation (SSA) in the auditory system
Keywords:
SSA, non-lemniscal, auditory, MMN, midbrain, thalamus, cerebral cortexAbstract
Stimulus-specific adaptation (SSA) is a special type of adaptation that allows neurons to cease responding only to repetitive, background stimuli, while preserving its responsiveness for other, new upcoming deviant stimuli. It emerges subcortically in non-lemniscal neurons of the inferior colliculi, propagating and evolving throughout the auditory pathway, until reaching its uppermost manifestation in the non-lemniscal areas of the auditory cortex. In this review, we will discuss the fundamental role of the non-lemniscal pathway in the generation of SSA, which is usually disregarded in cortical SSA research, despite being a major anatomical source of the mismatch negativity (MMN).
References
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Hu, B. (2003). “Functional organization of lemniscal and nonlemniscal auditory thalamus,” Exp. Brain Res., 153, 543-549. doi: 10.1007/s00221-003-1611-5
Irvine, D.R., and Huebner, H. (1979). “Acoustic response characteristics of neurons in nonspecific areas of cat cerebral cortex,” J. Neurophysiol., 42, 107-122. doi: 10.1152/jn.1979.42.1.107
Jones, E.G. (2003). “Chemically defined parallel pathways in the monkey auditory system,” Ann. NY Acad. Sci., 999, 218-233. doi: 10.1196/annals.1284.033
Lee, C.C., and Winer, J.A. (2008). “Connections of cat auditory cortex: I. Thalamo-cortical system;” J. Comp. Neurol., 507, 1879-1900. doi: 10.1002/cne.21611
Loftus, W.C., Malmierca, M.S., Bishop, D.C., and Oliver, D.L. (2008). “The cytoarchitecture of the inferior colliculus revisited: A common organization of the lateral cortex in rat and cat,” Neuroscience, 154, 196-205. doi: 10.1016/j.neuroscience.2008.01.019
Malmierca, M.S. (2003). “The structure and physiology of the rat auditory system: an overview,” in R.J. Bradley, R.A. Harris, and P. Jenner (Eds.), International Review of Neurobiology Vol. 56 (Academic Press), pp. 147–212.
Malmierca, M.S., Cristaudo, S., Pérez-González, D., and Covey, E. (2009). “Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat,” J. Neurosci., 29, 5483-5493. doi: 10.1523/jneurosci.4153-08.2009
Malmierca, M.S., and Hackett, T.A. (2010). “Structural organization of the ascending auditory pathway,” in D.R. Moore, A. Rees, and A.R. Palmer (Eds.), The Oxford Handbook of Auditory Science: The Auditory Brain (Oxford University Press), pp. 9-42.
Malmierca, M.S., and Ryugo, D.K. (2011). “Descending connections of auditory cortex to the midbrain and brain stem,” in The Auditory Cortex (Boston, MA: Springer), pp. 189-208. doi: 10.1007/978-1-4419-0074-6_9
Malmierca, M.S., Anderson, L.A., and Antunes, F.M. (2015). “The cortical modulation of stimulus-specific adaptation in the auditory midbrain and thalamus: a potential neuronal correlate for predictive coding,” Front. Sys. Neurosci., 9, 1-14. doi: 10.3389/fnsys.2015.00019
Megela, A.L., and Teyler, T.J. (1979). ”Habituation and the human evoked potential,” J. Comp. Physiol. Psychol., 93, 1154-1170. doi: 10.1037/h0077630
Näätänen, R., Paavilainen, P., Rinne, T., and Alho, K. (2007). “The mismatch negativity (MMN) in basic research of central auditory processing: A review,” Clin. Neurophysiol., 118, 2544-2590. doi: 10.1016/j.clinph.2007.04.026
Näätänen, R., Kujala, T., Escera, C., Baldeweg, T., Kreegipuu, K., Carlson, S., and Ponton, C. (2012). “The mismatch negativity (MMN) – A unique window to disturbed central auditory processing in ageing and different clinical conditions,” Clin. Neurophysiol., 123, 424-458. doi: 10.1016/j.clinph.2011.09.020
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Nelken, I., and Ulanovsky, N. (2007). Mismatch negativity and stimulus-specific adaptation in animal models,” J. Psychophysiol., 21, 214-223. doi: 10.1027/0269-8803.21.34.214
Nelken, I. (2014). “Stimulus-specific adaptation and deviance detection in the auditory system: experiments and models,” Biol. Cybern., 108, 655-663. doi: 10.1007/s00422-014-0585-7
Nieto-Diego, J., and Malmierca, M.S. (2016). “Topographic distribution of stimulus-specific adaptation across auditory cortical fields in the anesthetized rat,” PLoS Biol., 14, 1-30. doi: 10.1371/journal.pbio.1002397
Parras, G.G., Nieto-Diego, J., Carbajal, G.V., Valdés-Baizabal, C., Escera, C., and Malmierca, M.S. (2017). “Neurons along the auditory pathway exhibit a hierarchical organization of prediction error,” Nat. Commun., 8. doi: 10.1038/s41467-017-02038-6
Patel, C.R., Redhead, C., Cervi, A.L., and Zhang, H. (2012). “Neural sensitivity to novel sounds in the rat’s dorsal cortex of the inferior colliculus as revealed by evoked local field potentials,” Hear. Res., 286, 41-54. doi: 10.1016/j.heares.2012.02.007
Pérez-González, D., Hernández, O., Covey, E., Malmierca, M.S., and Schulze, H. (2012). “GABAA-mediated inhibition modulates stimulus-specific adaptation in the inferior colliculus,” PLoS One, e34297. doi: 10.1371/journal.pone.0034297
Pérez-González, D., Malmierca, M.S., and Covey, E. (2005). “Novelty detector neurons in the mammalian auditory midbrain,” Eur. J. Neurosci., 22, 2879-2885. doi: 10.1111/j.1460-9568.2005.04472.x
Pérez-González, D., and Malmierca, M. S. (2012). “Variability of the time course of stimulus-specific adaptation in the inferior colliculus,” Front. Neural Circuit., 6, 107. doi: 10.3389/fncir.2012.00107
Pérez-González, D., and Malmierca, M.S. (2014). “Adaptation in the auditory system: an overview,” Front. Integ. Neurosci., 8, 1-10. doi: 10.3389/fnint.2014.00019
Pincze, Z., Lakatos, P., Rajkai, C., Ulbert, I., and Karmos, G. (2001). “Separation of mismatch negativity and the N1 wave in the auditory cortex of the cat: a topographic study,” Clin. Neurophysiol., 112, 778-784. doi: 10.1016/S1388-2457(01)00509-0
Schreiner, C.E., and Cynader, M.S. (1984). “Basic functional organization of second auditory cortical field (AII) of the cat,” J. Neurophysiol., 51, 1284-1305. doi: 10.1152/jn.1984.51.6.1284
Shiramatsu, T.I., Kanzaki, R., Takahashi, H., Sams, M., and Näätänen, R. (2013). “Cortical mapping of mismatch negativity with deviance detection property in rat,” PLoS One, 8, e82663. doi: 10.1371/journal.pone.0082663
Tiitinen, H., May, P., Reinikainen, K., and Näätänen, R. (1994). “Attentive novelty detection in humans is governed by pre-attentive sensory memory,” Nature, 372, 90-92. doi: 10.1038/372090a0
Ulanovsky, N., Las, L., and Nelken, I. (2003). “Processing of low-probability sounds by cortical neurons,” Nat. Neurosci., 6, 391-398.
Ulanovsky, N., Las, L., Farkas, D., and Nelken, I. (2004). “Multiple time scales of adaptation in auditory cortex neurons,” J. Neurosci., 24.
Valdés-Baizabal, C., Parras, G.G., Ayala, Y.A., and Malmierca, M.S. (2017). “Endocannabinoid modulation of stimulus-specific adaptation in inferior colliculus neurons of the rat,” Sci. Rep., 6997. doi: 10.1038/s41598-017-07460-w
Zhao, L., Liu, Y., Shen, L., Feng, L., and Hong, B. (2011). “Stimulus-specific adaptation and its dynamics in the inferior colliculus of rat,” Neuroscience, 181, 163-174. doi: 10.1016/j.neuroscience.2011.01.060
Anderson, L.A., Christianson, G.B., and Linden, J.F. (2009). “Stimulus-specific adaptation occurs in the auditory thalamus,” J. Neurosci., 29, 7359-7363. doi: 10.1523/JNEUROSCI.0793-09.2009
Anderson, L.A., and Malmierca, M.S. (2013). “The effect of auditory cortex deactivation on stimulus-specific adaptation in the inferior colliculus of the rat,” Eur. J. Neurosci., 37, 52-62. doi: 10.1111/ejn.12018
Antunes, F.M., Nelken, I., Covey, E., and Malmierca, M.S. (2010). “Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat,” PLoS ONE, 5. doi: 10.1371/journal.pone.0014071
Antunes, F.M., and Malmierca, M.S. (2011). “Effect of auditory cortex deactivation on stimulus-specific adaptation in the medial geniculate body,” J. Neurosci., 31, 17306-17316.
Antunes, F.M., and Malmierca, M.S. (2014). “An overview of stimulus-specific adaptation in the auditory thalamus,” Brain Topogr., 27, 480-499. doi: 10.1007/s10548-013-0342-6
Ayala, Y.A., and Malmierca, M.S. (2013). “Stimulus-specific adaptation and deviance detection in the inferior colliculus,” Front. Neural Circuit., 6, 1-16. doi: 10.3389/fncir.2012.00089
Ayala, Y.A., and Malmierca, M.S. (2015). “Cholinergic modulation of stimulus-specific adaptation in the inferior colliculus,” J. Neurosci., 35, 12261-12272. doi: 10.1523/JNEUROSCI.0909-15.2015
Ayala, Y.A., Pérez-González, D., Duque, D., Nelken, I., and Malmierca, M.S. (2013). “Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus,” Front. Neural Circuit., 6, 119. doi: 10.3389/fncir.2012.00119
Ayala, Y.A., Pérez-González, D., and Malmierca, M.S. (2016). “Stimulus-specific adaptation in the inferior colliculus: The role of excitatory, inhibitory and modulatory inputs,” Biol. Psychol., 116, 10-22. doi: 10.1016/j.biopsycho.2015.06.016
Ayala, Y.A., and Malmierca, M.S. (2017). “The effect of inhibition on stimulus-specific adaptation in the inferior colliculus,” Brain Struct. Funct., 1-17. doi: 10.1007/s00429-017-1546-4
Ayala, Y.A., Udeh, A., Dutta, K., Bishop, D., Malmierca, M.S., and Oliver, D.L. (2015). “Differences in the strength of cortical and brainstem inputs to SSA and non-SSA neurons in the inferior colliculus,” Sci. Rep., 5, 10383. doi: 10.1038/srep10383
Diliberto, K.A., Altarriba, J., and Neill, W.T. (2000). “Novel popout and familiar popout in a brightness discrimination task,” Percept. Psychophys., 62, 1494-1500. doi: 10.3758/BF03212149
Duque, D., Perez-Gonzalez, D., Ayala, Y.A., Palmer, A.R., and Malmierca, M.S. (2012). “Topographic distribution, frequency, and intensity dependence of stimulus-specific adaptation in the inferior colliculus of the rat,” J. Neurosci., 32, 17762-17774. doi: 10.1523/jneurosci.3190-12.2012
Duque, D., Malmierca, M.S., and Caspary, D.M. (2014). “Modulation of stimulus-specific adaptation by GABA(A) receptor activation or blockade in the medial geniculate body of the anaesthetized rat,” J. Physiol., 592, 729-743. doi: 10.1113/jphysiol.2013.261941
Duque, D., and Malmierca, M.S. (2015). “Stimulus-specific adaptation in the inferior colliculus of the mouse: anesthesia and spontaneous activity effects,” Brain Struct. Funct., 220, 3385-3398. doi: 10.1007/s00429-014-0862-1
Duque, D., Wang, X., Nieto-Diego, J., Krumbholz, K., and Malmierca, M.S. (2016). “Neurons in the inferior colliculus of the rat show stimulus-specific adaptation for frequency, but not for intensity;” Sci. Rep., 6, 24114. doi: 10.1038/srep24114
Escera, C., and Malmierca, M.S. (2014). “The auditory novelty system: An attempt to integrate human and animal research,” Psychophysiology, 51, 111-123. doi: 10.1111/psyp.12156
Graybiel, A.M. (1973). “The thalamo-cortical projection of the so-called posterior nuclear group: A study with anterograde degeneration methods in the cat,” Brain Res., 49, 229-244. doi: 10.1016/0006-8993(73)90420-4
Gutfreund, Y. (2012). “Stimulus-specific adaptation, habituation and change detection in the gaze control system,” Biol. Cybern., 106, 657-668. doi: 10.1007/s00422-012-0497-3
Harms, L., Michie, P.T., and Näätänen, R. (2016). “Criteria for determining whether mismatch responses exist in animal models: Focus on rodents,” Biol. Psychol., 116, 28-35. doi: 10.1016/j.biopsycho.2015.07.006
Hu, B. (2003). “Functional organization of lemniscal and nonlemniscal auditory thalamus,” Exp. Brain Res., 153, 543-549. doi: 10.1007/s00221-003-1611-5
Irvine, D.R., and Huebner, H. (1979). “Acoustic response characteristics of neurons in nonspecific areas of cat cerebral cortex,” J. Neurophysiol., 42, 107-122. doi: 10.1152/jn.1979.42.1.107
Jones, E.G. (2003). “Chemically defined parallel pathways in the monkey auditory system,” Ann. NY Acad. Sci., 999, 218-233. doi: 10.1196/annals.1284.033
Lee, C.C., and Winer, J.A. (2008). “Connections of cat auditory cortex: I. Thalamo-cortical system;” J. Comp. Neurol., 507, 1879-1900. doi: 10.1002/cne.21611
Loftus, W.C., Malmierca, M.S., Bishop, D.C., and Oliver, D.L. (2008). “The cytoarchitecture of the inferior colliculus revisited: A common organization of the lateral cortex in rat and cat,” Neuroscience, 154, 196-205. doi: 10.1016/j.neuroscience.2008.01.019
Malmierca, M.S. (2003). “The structure and physiology of the rat auditory system: an overview,” in R.J. Bradley, R.A. Harris, and P. Jenner (Eds.), International Review of Neurobiology Vol. 56 (Academic Press), pp. 147–212.
Malmierca, M.S., Cristaudo, S., Pérez-González, D., and Covey, E. (2009). “Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat,” J. Neurosci., 29, 5483-5493. doi: 10.1523/jneurosci.4153-08.2009
Malmierca, M.S., and Hackett, T.A. (2010). “Structural organization of the ascending auditory pathway,” in D.R. Moore, A. Rees, and A.R. Palmer (Eds.), The Oxford Handbook of Auditory Science: The Auditory Brain (Oxford University Press), pp. 9-42.
Malmierca, M.S., and Ryugo, D.K. (2011). “Descending connections of auditory cortex to the midbrain and brain stem,” in The Auditory Cortex (Boston, MA: Springer), pp. 189-208. doi: 10.1007/978-1-4419-0074-6_9
Malmierca, M.S., Anderson, L.A., and Antunes, F.M. (2015). “The cortical modulation of stimulus-specific adaptation in the auditory midbrain and thalamus: a potential neuronal correlate for predictive coding,” Front. Sys. Neurosci., 9, 1-14. doi: 10.3389/fnsys.2015.00019
Megela, A.L., and Teyler, T.J. (1979). ”Habituation and the human evoked potential,” J. Comp. Physiol. Psychol., 93, 1154-1170. doi: 10.1037/h0077630
Näätänen, R., Paavilainen, P., Rinne, T., and Alho, K. (2007). “The mismatch negativity (MMN) in basic research of central auditory processing: A review,” Clin. Neurophysiol., 118, 2544-2590. doi: 10.1016/j.clinph.2007.04.026
Näätänen, R., Kujala, T., Escera, C., Baldeweg, T., Kreegipuu, K., Carlson, S., and Ponton, C. (2012). “The mismatch negativity (MMN) – A unique window to disturbed central auditory processing in ageing and different clinical conditions,” Clin. Neurophysiol., 123, 424-458. doi: 10.1016/j.clinph.2011.09.020
Nelken, I. (2004). “Processing of complex stimuli and natural scenes in the auditory cortex,” Curr. Opin. Neurobiol., 14, 474-480. doi: 10.1016/j.conb.2004.06.005
Nelken, I., and Ulanovsky, N. (2007). Mismatch negativity and stimulus-specific adaptation in animal models,” J. Psychophysiol., 21, 214-223. doi: 10.1027/0269-8803.21.34.214
Nelken, I. (2014). “Stimulus-specific adaptation and deviance detection in the auditory system: experiments and models,” Biol. Cybern., 108, 655-663. doi: 10.1007/s00422-014-0585-7
Nieto-Diego, J., and Malmierca, M.S. (2016). “Topographic distribution of stimulus-specific adaptation across auditory cortical fields in the anesthetized rat,” PLoS Biol., 14, 1-30. doi: 10.1371/journal.pbio.1002397
Parras, G.G., Nieto-Diego, J., Carbajal, G.V., Valdés-Baizabal, C., Escera, C., and Malmierca, M.S. (2017). “Neurons along the auditory pathway exhibit a hierarchical organization of prediction error,” Nat. Commun., 8. doi: 10.1038/s41467-017-02038-6
Patel, C.R., Redhead, C., Cervi, A.L., and Zhang, H. (2012). “Neural sensitivity to novel sounds in the rat’s dorsal cortex of the inferior colliculus as revealed by evoked local field potentials,” Hear. Res., 286, 41-54. doi: 10.1016/j.heares.2012.02.007
Pérez-González, D., Hernández, O., Covey, E., Malmierca, M.S., and Schulze, H. (2012). “GABAA-mediated inhibition modulates stimulus-specific adaptation in the inferior colliculus,” PLoS One, e34297. doi: 10.1371/journal.pone.0034297
Pérez-González, D., Malmierca, M.S., and Covey, E. (2005). “Novelty detector neurons in the mammalian auditory midbrain,” Eur. J. Neurosci., 22, 2879-2885. doi: 10.1111/j.1460-9568.2005.04472.x
Pérez-González, D., and Malmierca, M. S. (2012). “Variability of the time course of stimulus-specific adaptation in the inferior colliculus,” Front. Neural Circuit., 6, 107. doi: 10.3389/fncir.2012.00107
Pérez-González, D., and Malmierca, M.S. (2014). “Adaptation in the auditory system: an overview,” Front. Integ. Neurosci., 8, 1-10. doi: 10.3389/fnint.2014.00019
Pincze, Z., Lakatos, P., Rajkai, C., Ulbert, I., and Karmos, G. (2001). “Separation of mismatch negativity and the N1 wave in the auditory cortex of the cat: a topographic study,” Clin. Neurophysiol., 112, 778-784. doi: 10.1016/S1388-2457(01)00509-0
Schreiner, C.E., and Cynader, M.S. (1984). “Basic functional organization of second auditory cortical field (AII) of the cat,” J. Neurophysiol., 51, 1284-1305. doi: 10.1152/jn.1984.51.6.1284
Shiramatsu, T.I., Kanzaki, R., Takahashi, H., Sams, M., and Näätänen, R. (2013). “Cortical mapping of mismatch negativity with deviance detection property in rat,” PLoS One, 8, e82663. doi: 10.1371/journal.pone.0082663
Tiitinen, H., May, P., Reinikainen, K., and Näätänen, R. (1994). “Attentive novelty detection in humans is governed by pre-attentive sensory memory,” Nature, 372, 90-92. doi: 10.1038/372090a0
Ulanovsky, N., Las, L., and Nelken, I. (2003). “Processing of low-probability sounds by cortical neurons,” Nat. Neurosci., 6, 391-398.
Ulanovsky, N., Las, L., Farkas, D., and Nelken, I. (2004). “Multiple time scales of adaptation in auditory cortex neurons,” J. Neurosci., 24.
Valdés-Baizabal, C., Parras, G.G., Ayala, Y.A., and Malmierca, M.S. (2017). “Endocannabinoid modulation of stimulus-specific adaptation in inferior colliculus neurons of the rat,” Sci. Rep., 6997. doi: 10.1038/s41598-017-07460-w
Zhao, L., Liu, Y., Shen, L., Feng, L., and Hong, B. (2011). “Stimulus-specific adaptation and its dynamics in the inferior colliculus of rat,” Neuroscience, 181, 163-174. doi: 10.1016/j.neuroscience.2011.01.060
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2018-02-06
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Carbajal, G. V., & Malmierca, M. S. (2018). The unique role of the non-lemniscal pathway on stimulus-specific adaptation (SSA) in the auditory system. Proceedings of the International Symposium on Auditory and Audiological Research, 6, 95–106. Retrieved from https://proceedings.isaar.eu/index.php/isaarproc/article/view/2017-12
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2017/2. Neural mechanisms, modeling, and physiological correlates of adaptation
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