Stimulus-specific adaptation and deviance detection in the auditory system: experiments and models

Biological Cybernetics

Volumn 108, Issue 5, 2014, Pages 655-663

  Nelken, Israel ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Auditory cortex; Electrophysiology; Inferior colliculus; Synaptic depression

Indexed keywords

MAMMALS;

AUDITORY CORTEX; AUDITORY SYSTEMS; COMPUTATIONAL TASK; FULLY COMPATIBLE; INFERIOR COLLICULUS; MAMMALIAN SPECIES; SPECIFIC ADAPTATIONS; SYNAPTIC DEPRESSION;

ELECTROPHYSIOLOGY;

ADAPTATION; ANIMAL; AUDITORY CORTEX; AUDITORY NERVOUS SYSTEM; AUDITORY STIMULATION; BIOLOGICAL MODEL; HUMAN; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY;

ACOUSTIC STIMULATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; AUDITORY CORTEX; AUDITORY PATHWAYS; HUMANS; MODELS, NEUROLOGICAL; SIGNAL DETECTION, PSYCHOLOGICAL;

EID: 84919877787     PISSN: 03401200     EISSN: 14320770     Source Type: Journal    
DOI: 10.1007/s00422-014-0585-7     Document Type: Review

References (57)

1. Anderson LA, Christianson GB, Linden JF (2009) Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci 29(22):7359–7363. doi:10.1523/JNEUROSCI.0793-09.2009
2. Antunes FM, Nelken I, Covey E, Malmierca MS (2010) Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS ONE 5(11):e14071. doi:10.1371/journal.pone.0014071
3. Ayala YA, Perez-Gonzalez D, Duque D, Nelken I, Malmierca MS (2012) Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus. Front Neural Circuits 6:119. doi:10.3389/fncir.2012.00119
4. Bauerle P, von der Behrens W, Kossl M, Gaese BH (2011) Stimulus-specific adaptation in the gerbil primary auditory thalamus is the result of a fast frequency-specific habituation and is regulated by the corticofugal system. J Neurosci 31(26):9708–9722. doi:10.1523/JNEUROSCI.5814-10.2011
5. Bendixen A, Prinz W, Horvath J, Trujillo-Barreto NJ, Schroger E (2008) Rapid extraction of auditory feature contingencies. Neuroimage 41(3):1111–1119. doi:10.1016/j.neuroimage.2008.03.040
6. Bendixen A, Roeber U, Schroger E (2007) Regularity extraction and application in dynamic auditory stimulus sequences. J Cogn Neurosci 19(10):1664–1677. doi:10.1162/jocn.2007.19.10.1664
7. Bendixen A, Schroger E (2008) Memory trace formation for abstract auditory features and its consequences in different attentional contexts. Biol Psychol 78(3):231–241. doi:10.1016/j.biopsycho.2008.03.005
8. Corfas G, Dudai Y (1989) Habituation and dishabituation of a cleaning reflex in normal and mutant Drosophila. J Neurosci 9(1):56–62
9. Duque D, Perez-Gonzalez D, Ayala YA, Palmer AR, Malmierca MS (2012) Topographic distribution, frequency, and intensity dependence of stimulus-specific adaptation in the inferior colliculus of the rat. J Neurosci 32(49):17762–17774. doi:10.1523/JNEUROSCI.3190-12.2012
10. Edeline JM (2003) The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems. Exp Brain Res 153(4):554–572
11. Edeline JM, Pham P, Weinberger NM (1993) Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behav Neurosci 107(4):539–551
12. Ehret G, Merzenich MM (1985) Auditory midbrain responses parallel spectral integration phenomena. Science 227(4691):1245–1247
13. Farley BJ, Quirk MC, Doherty JJ, Christian EP (2010) Stimulus-specific adaptation in auditory cortex is an NMDA-independent process distinct from the sensory novelty encoded by the mismatch negativity. J Neurosci 30(49):16475–16484. doi:10.1523/JNEUROSCI.2793-10.2010
14. Fishman YI, Steinschneider M (2012) Searching for the mismatch negativity in primary auditory cortex of the awake monkey: deviance detection or stimulus specific adaptation? J Neurosci 32(45):15747–15758. doi:10.1523/JNEUROSCI.2835-12.2012
15. Gordon N, Shackleton TM, Palmer AR, Nelken I (2008) Responses of neurons in the inferior colliculus to binaural disparities: Insights from the use of Fisher information and mutual information. J Neurosci Methods 169(2):391–404
16. Grimm S, Escera C (2012) Auditory deviance detection revisited: evidence for a hierarchical novelty system. Int J Psychophysiol 85(1):88–92. doi:10.1016/j.ijpsycho.2011.05.012
17. Grimm S, Escera C, Slabu L, Costa-Faidella J (2011) Electrophysiological evidence for the hierarchical organization of auditory change detection in the human brain. Psychophysiology 48(3):377–384. doi:10.1111/j.1469-8986.2010.01073.x
18. Gutfreund Y (2012) Stimulus-specific adaptation, habituation and change detection in the gaze control system. Biol Cybern. doi:10.1007/s00422-012-0497-3
19. Harper NS, McAlpine D (2004) Optimal neural population coding of an auditory spatial cue. Nature 430(7000):682–686
20. Hershenhoren I, Taaseh N, Nelken I (2012) Intracellular correlates of stimulus-specific adaptation. J Mol Neurosci 48:S53–S53
21. Jacobsen T, Schroger E, Horenkamp T, Winkler I (2003) Mismatch negativity to pitch change: varied stimulus proportions in controlling effects of neural refractoriness on human auditory event-related brain potentials. Neurosci Lett 344(2):79–82. doi:10.1016/S0304-3940(03)00408-7
22. Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279(5357):1714–1718
23. Loebel A, Nelken I, Tsodyks M (2007) Processing of sounds by population spikes in a model of primary auditory cortex. Front Neurosci 1(1):197–209. doi:10.3389/neuro.01.1.1.015.2007
24. Malmierca MS, Cristaudo S, Perez-Gonzalez D, Covey E (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29(17):5483–5493. doi:10.1523/JNEUROSCI.4153-08.2009
25. Metherate R (2010) Functional connectivity and cholinergic modulation in auditory cortex. Neurosci Biobehav Rev 35(10):2058–2063. doi:10.1016/j.neubiorev.2010.11.010
26. Mill R, Coath M, Wennekers T, Denham SL (2011a) Abstract stimulus-specific adaptation models. Neural Comput 23(2):435–476. doi:10.1162/NECO_a_00077
27. Mill R, Coath M, Wennekers T, Denham SL (2011b) A neurocomputational model of stimulus-specific adaptation to oddball and Markov sequences. PLoS Comput Biol 7(8):e1002117. doi:10.1371/journal.pcbi.1002117
28. Mill R, Coath M, Wennekers T, Denham SL (2012) Characterising stimulus-specific adaptation using a multi-layer field model. Brain Res 1434:178–188. doi:10.1016/j.brainres.2011.08.063
29. Miller LM, Escabi MA, Read HL, Schreiner CE (2001) Functional convergence of response properties in the auditory thalamocortical system. Neuron 32(1):151–160
30. Moore BCJ (1993) Frequency analysis and pitch perception. In: Yost WA, Popper AN, Fay RR (eds) Human psychophysics. Springer, New York, pp 56–115
31. Moshitch D, Las L, Ulanovsky N, Bar-Yosef O, Nelken I (2006) Responses of neurons in primary auditory cortex (A1) to pure tones in the halothane-anesthetized cat. J Neurophysiol 95(6):3756–3769
32. Movshon JA, Lennie P (1979) Pattern-selective adaptation in visual cortical neurones. Nature 278(5707):850–852
33. Nelken I, Bar-Yosef O (2008) Neurons and objects: the case of auditory cortex. Front Neurosci 2(1):107–113. doi:10.3389/neuro.01.009.2008
34. Nelken I, Ulanovsky N (2007) Change detection, mismatch negativity and stimulus-specific adaptation in animal models. J Psychophysiol 21:214–223
35. Nelken I, Yaron A, Polterovich A, Hershenhoren I (2013) Stimulus-specific adaptation beyond pure tones. Adv Exp Med Biol 787:411–418. doi:10.1007/978-1-4614-1590-9_45
36. Netser S, Zahar Y, Gutfreund Y (2011) Stimulus-specific adaptation: can it be a neural correlate of behavioral habituation? J Neurosci 31(49):17811–17820. doi:10.1523/JNEUROSCI.4790-11.2011
37. Patel CR, Redhead C, Cervi AL, 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(1–2):41–54. doi:10.1016/j.heares.2012.02.007
38. Perez-Gonzalez D, Hernandez O, Covey E, Malmierca MS (2012) GABA(A)-mediated inhibition modulates stimulus-specific adaptation in the inferior colliculus. PLoS One 7(3):e34297. doi:10.1371/journal.pone.0034297
39. Reches A, Gutfreund Y (2008) Stimulus-specific adaptations in the gaze control system of the barn owl. J Neurosci 28(6):1523–1533
40. Reches A, Netser S, Gutfreund Y (2010) Interactions between stimulus-specific adaptation and visual auditory integration in the forebrain of the barn owl. J Neurosci 30(20):6991–6998. doi:10.1523/JNEUROSCI.5723-09.2010
41. Sanchez-Vives MV, Nowak LG, McCormick DA (2000) Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J Neurosci 20(11):4267–4285
42. Scholes C, Palmer AR, Sumner CJ (2011) Forward suppression in the auditory cortex is frequency-specific. Eur J Neurosci 33(7):1240–1251. doi:10.1111/j.1460-9568.2010.07568.x
43. Slabu L, Escera C, Grimm S, Costa-Faidella J (2010) Early change detection in humans as revealed by auditory brainstem and middle-latency evoked potentials. Eur J Neurosci 32(5):859–865. doi:10.1111/j.1460-9568.2010.07324.x
44. Taaseh N, Yaron A, Nelken I (2011) Stimulus-specific adaptation and deviance detection in the rat auditory cortex. PLoS ONE 6(8):e23369. doi:10.1371/journal.pone.0023369
45. Talwar SK, Gerstein GL (1998) Auditory frequency discrimination in the white rat. Hear Res 126(1–2):135–150
46. Thomas JM, Morse C, Kishline L, O’Brien-Lambert A, Simonton A, Miller KE, Covey E (2012) Stimulus-specific adaptation in specialized neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus. Hear Res 291(1–2):34–40. doi:10.1016/j.heares.2012.06.004
47. Tsodyks M, Uziel A, Markram H (2000) Synchrony generation in recurrent networks with frequency-dependent synapses. J Neurosci 20(1):RC50
48. Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24(46):10440–10453
49. Ulanovsky N, Las L, Nelken I (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6(4):391–398
50. von der Behrens W, Bauerle P, Kossl M, Gaese BH (2009) Correlating stimulus-specific adaptation of cortical neurons and local field potentials in the awake rat. J Neurosci 29(44):13837–13849. doi:10.1523/JNEUROSCI.3475-09.2009
51. Wehr M, Zador AM (2005) Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47(3):437–445
52. Westerman LA, Smith RL (1984) Rapid and short-term adaptation in auditory nerve responses. Hear Res 15:249–260
53. Winkler I, Denham SL, Nelken I (2009) Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cogn Sci 13(12):532–540. doi:10.1016/j.tics.2009.09.003
54. Yarden TS, Nelken I (2012) Stimulus-Specific Adaptation in a model of primary auditory cortex. J Mol Neurosci 48:S126–S126
55. Yaron A, Hershenhoren I, Nelken I (2012) Sensitivity to complex statistical regularities in rat auditory cortex. Neuron 76(3):603–615. doi:10.1016/j.neuron.2012.08.025
56. Yu XJ, Xu XX, He S, He J (2009) Change detection by thalamic reticular neurons. Nat Neurosci 12(9):1165–1170. doi:10.1038/nn.2373
57. Zhao L, Liu Y, Shen L, Feng L, 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