Advertisement

Brain Structure and Function

, Volume 223, Issue 3, pp 1391–1407 | Cite as

The effect of inhibition on stimulus-specific adaptation in the inferior colliculus

  • Yaneri A. Ayala
  • Manuel S. Malmierca
Original Article

Abstract

The inferior colliculus is a center of convergence for inhibitory and excitatory synaptic inputs that may be activated simultaneously by sound stimulation. Stimulus repetition may generate response habituation by changing the efficacy of neuron’s synaptic inputs. Specialized IC neurons reduce their response to repetitive tones, but restore their firing when a different and infrequent tone occurs, a phenomenon known as stimulus specific adaptation. Here, using the microiontophoresis technique, we determined the role of GABAA-, GABAB-, and glycinergic receptors in stimulus-specific adaptation (SSA). We found that blockade of postsynaptic GABAB receptors selectively modulated response adaptation to repetitive sounds, whereas blockade of presynaptic GABAB receptors exerted a gain control effect on neuron excitability. Adaptation decreased when postsynaptic GABAB receptors were blocked, but increased if the blockade affected the presynaptic GABAB receptors. A dual, paradoxical effect was elicited by blockade of glycinergic receptors, i.e., both increase and decrease in adaptation. Moreover, simultaneous co-application of GABAA, GABAB, and glycinergic antagonists demonstrated that local GABA- and glycine-mediated inhibition contributes to only about 50% of SSA. Therefore, inhibition via chemical synapses dynamically modulate the strength and dynamics of stimulus-specific adaptation, but does not generate it.

Keywords

Inhibition GABAB receptors Glycinergic receptors SSA Microiontophoresis Auditory 

Notes

Acknowledgements

This work was supported by the Spanish Ministerio de Economía y Competitividad Grants SAF2016-75803-P and Junta de Castilla y León Grant SA343U14 to MSM. YAA held PhD fellowships from the Mexican Consejo Nacional de Ciencia y Tecnología and Secretaría de Educación Pública. We thank to Dr. Nell B. Cant and Edward Bartlett for their thoughtful comments on a previous version of the manuscript. In addition, we thank Collen Gabel for her assistance in performing strychnine experiments and Otto García-Garibay for his help to generate Figs. 1b–5b.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Anderson LA, Christianson GB, Linden JF (2009) Stimulus-specific adaptation occurs in the auditory thalamus. J Neurosci 29:7359–7363.  https://doi.org/10.1523/JNEUROSCI.0793-09.2009 CrossRefPubMedGoogle Scholar
  2. Antunes FM, Malmierca MS (2011) Effect of auditory cortex deactivation on stimulus-specific adaptation in the medial geniculate body. J Neurosci 31:17306–17316.  https://doi.org/10.1523/JNEUROSCI.1915-11.2011 CrossRefPubMedGoogle Scholar
  3. Antunes FM, Nelken I, Covey E, Malmierca MS (2010) Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat. PLoS One 5:e14071.  https://doi.org/10.1371/journal.pone.0014071 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ayala YA, Malmierca MS (2013) Stimulus-specific adaptation and deviance detection in the inferior colliculus Front Neural Circuits 6:89.  https://doi.org/10.3389/fncir.2012.00089 PubMedGoogle Scholar
  5. Ayala YA, Malmierca MS (2014) Cholinergic modulation of stimulus-specific adaptation in the inferior colliculus. In: Paper presented at the 9th FENS forum of neuroscience, MilanGoogle Scholar
  6. Ayala YA, Malmierca MS (2015) Modulation of auditory deviant saliency in the inferior colliculus. In: Paper presented at the ARO midwinter meeting, BaltimoreGoogle Scholar
  7. Ayala YA, Perez-Gonzalez D, Duque D, Nelken I, Malmierca MS (2013) Frequency discrimination and stimulus deviance in the inferior colliculus and cochlear nucleus. Front Neural Circuits 6:119.  https://doi.org/10.3389/fncir.2012.00119 PubMedPubMedCentralGoogle Scholar
  8. Ayala YA, Udeh A, Dutta K, Bishop D, Malmierca MS, Oliver DL (2015) Differences in the strength of cortical and brainstem inputs to SSA and non-SSA neurons in the inferior colliculus. Sci Rep 5:10383.  https://doi.org/10.1038/srep10383 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Ayala YA, Pérez-González D, Duque D, Palmer AR, Malmierca MS (2016) Extracellular recording of euronal activity combined with microiontophoretic application of neuroactive substances in awake mice. J Vis Exp.  https://doi.org/10.3791/53914 PubMedGoogle Scholar
  10. Binns KE, Salt TE (1995) Excitatory amino acid receptors modulate habituation of the response to visual stimulation in the cat superior colliculus. Vis Neurosci 12:563–571CrossRefPubMedGoogle Scholar
  11. Binns KE, Salt TE (1997) Different roles for GABAA and GABAB receptors in visual processing in the rat superior colliculus. J Physiol 504(Pt 3):629–639CrossRefPubMedPubMedCentralGoogle Scholar
  12. Burger RM, Pollak GD (1998) Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus. J Neurophysiol 80:1686–1701CrossRefPubMedGoogle Scholar
  13. Calford MB (1983) The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J Neurosci 3:2350–2364PubMedGoogle Scholar
  14. Carandini M (2007) Melting the iceberg: contrast invariance in visual cortex. Neuron 54:11–13.  https://doi.org/10.1016/j.neuron.2007.03.019 CrossRefPubMedGoogle Scholar
  15. Charara A, Pare JF, Levey AI, Smith Y (2005) Synaptic and extrasynaptic GABA-A and GABA-B receptors in the globus pallidus: an electron microscopic immunogold analysis in monkeys. Neuroscience 131:917–933CrossRefPubMedGoogle Scholar
  16. Dimitrov AG, Cummins GI, Mayko ZM, Portfors CV (2014) Inhibition does not affect the timing code for vocalizations in the mouse auditory midbrain. Front Physiol 5:140.  https://doi.org/10.3389/fphys.2014.00140 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Duque D, Malmierca MS (2014) Stimulus-specific adaptation in the inferior colliculus of the mouse: anesthesia and spontaneous activity effects. Brain Struct Funct.  https://doi.org/10.1007/s00429-014-0862-1 PubMedGoogle Scholar
  18. 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 32:17762–17774.  https://doi.org/10.1523/JNEUROSCI.3190-12.2012 CrossRefPubMedGoogle Scholar
  19. Duque D, Malmierca MS, Caspary DM (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.  https://doi.org/10.1113/jphysiol.2013.261941 CrossRefPubMedGoogle Scholar
  20. Duque D, Ayala YA, Malmierca MS (2015) Deviance detection in auditory subcortical structures: what can we learn from neurochemistry and neural connectivity? Cell Tissue Res.  https://doi.org/10.1007/s00441-015-2134-7 PubMedGoogle Scholar
  21. Duque D, Wang X, Nieto-Diego J, Krumbholz K, Malmierca MS (2016) Neurons in the inferior colliculus of the rat show stimulus-specific adaptation for frequency, but not for intensity. Sci Rep 6:24114.  https://doi.org/10.1038/srep24114 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Eytan D, Brenner N, Marom S (2003) Selective adaptation in networks of cortical neurons. J Neurosci 23:9349–9356PubMedGoogle Scholar
  23. Faingold CL, Boersma Anderson CA, Caspary DM (1991) Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons. Hear Res 52:201–216CrossRefPubMedGoogle Scholar
  24. Faure PA, Fremouw T, Casseday JH, Covey E (2003) Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus. J Neurosci 23:3052–3065PubMedGoogle Scholar
  25. Friauf E, Fischer AU, Fuhr MF (2015) Synaptic plasticity in the auditory system: a review. Cell Tissue Res.  https://doi.org/10.1007/s00441-015-2176-x PubMedCentralGoogle Scholar
  26. Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185–204CrossRefPubMedGoogle Scholar
  27. Hammond C (2015) The ionotropic GABAA receptor, chap 9. In: Cellular and molecular neurophysiology, 4th edn. Academic Press, Constance HammondGoogle Scholar
  28. Hernandez O, Espinosa N, Perez-Gonzalez D, Malmierca MS (2005) The inferior colliculus of the rat: a quantitative analysis of monaural frequency response areas. Neuroscience 132:203–217.  https://doi.org/10.1016/j.neuroscience.2005.01.001 CrossRefPubMedGoogle Scholar
  29. Ito T, Bishop DC, Oliver DL (2015) Functional organization of the local circuit in the inferior colliculus. Anat Sci Int.  https://doi.org/10.1007/s12565-015-0308-8 PubMedPubMedCentralGoogle Scholar
  30. Jamal L, Zhang H, Finlayson PG, Porter LA, Zhang H (2011) The level and distribution of the GABA(B)R2 receptor subunit in the rat’s central auditory system. Neuroscience 181:243–256.  https://doi.org/10.1016/j.neuroscience.2011.02.050 CrossRefPubMedGoogle Scholar
  31. Jamal L, Khan AN, Butt S, Patel CR, Zhang H (2012) The level and distribution of the GABA(B)R1 and GABA(B)R2 receptor subunits in the rat’s inferior colliculus. Front Neural Circuits 6:92.  https://doi.org/10.3389/fncir.2012.00092 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kelly JB, Caspary DM (2005) Pharmacology of the inferior colliculus. In: Winer JA, Schreiner CE (eds) the inferior colliculus. Springer, New York, pp 248–281CrossRefGoogle Scholar
  33. Kraus N, McGee T, Littman T, Nicol T, King C (1994) Nonprimary auditory thalamic representation of acoustic change. J Neurophysiol 72:1270–1277CrossRefPubMedGoogle Scholar
  34. LeBeau FE, Malmierca MS, Rees A (2001) Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci 21:7303–7312PubMedGoogle Scholar
  35. Luo B, Wang HT, Su YY, Wu SH, Chen L (2011) Activation of presynaptic GABAB receptors modulates GABAergic and glutamatergic inputs to the medial geniculate body. Hear Res 280:157–165.  https://doi.org/10.1016/j.heares.2011.05.018 CrossRefPubMedGoogle Scholar
  36. Ma CL, Kelly JB, Wu SH (2002) Presynaptic modulation of GABAergic inhibition by GABA(B) receptors in the rat’s inferior colliculus. Neuroscience 114:207–215CrossRefPubMedGoogle Scholar
  37. Magnusson AK, Park TJ, Pecka M, Grothe B, Koch U (2008) Retrograde GABA signaling adjusts sound localization by balancing excitation and inhibition in the brainstem. Neuron 59:125–137.  https://doi.org/10.1016/j.neuron.2008.05.011 CrossRefPubMedGoogle Scholar
  38. Malmierca MS, Hernandez O, Rees A (2005) Intercollicular commissural projections modulate neuronal responses in the inferior colliculus. Eur J Neurosci 21:2701–2710.  https://doi.org/10.1111/j.1460-9568.2005.04103.x CrossRefPubMedGoogle Scholar
  39. Malmierca MS, Izquierdo MA, Cristaudo S, Hernandez O, Perez-Gonzalez D, Covey E, Oliver DL (2008) A discontinuous tonotopic organization in the inferior colliculus of the rat. J Neurosci 28:4767–4776.  https://doi.org/10.1523/JNEUROSCI.0238-08.2008 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Malmierca MS, Cristaudo S, Perez-Gonzalez D, Covey E (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29:5483–5493.  https://doi.org/10.1523/JNEUROSCI.4153-08.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Malmierca MS, Blackstad TW, Osen KK (2011) Computer-assisted 3-D reconstructions of Golgi-impregnated neurons in the cortical regions of the inferior colliculus of rat. Hear Res 274(1–2):13–26CrossRefPubMedGoogle Scholar
  42. Maravall M (2013) Adaptation and sensory coding. In: Quiroga RQ, Panzeri S (eds) Principles of neural coding. CRC Press, Boca Raton, pp 357–377CrossRefGoogle Scholar
  43. Merrill EG, Ainsworth A (1972) Glass-coated platinum-plated tungsten microelectrodes. Med Biol Eng 10:662–672CrossRefPubMedGoogle Scholar
  44. Milbrandt JC, Albin RL, Caspary DM (1994) Age-related decrease in GABAB receptor binding in the Fischer 344 rat inferior colliculus. Neurobiol Aging 15:699–703CrossRefPubMedGoogle Scholar
  45. Mott D (2015) The metabotropic GABAB receptors, chapter 11. In: Cellular and molecular neurophysiology, 4th edn. Academic Press, Constance HammondGoogle Scholar
  46. Näätänen R (1992) Attention and brain function. Lawrence Erlbaum, HillsdaleGoogle Scholar
  47. Nelken I (2014) Stimulus-specific adaptation and deviance detection in the auditory system: experiments and models. Biol Cybern 108:655–663.  https://doi.org/10.1007/s00422-014-0585-7 CrossRefPubMedGoogle Scholar
  48. Nelson PC, Young ED (2010) Neural correlates of context-dependent perceptual enhancement in the inferior colliculus. J Neurosci 30:6577–6587.  https://doi.org/10.1523/JNEUROSCI.0277-10.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Nieto-Diego J, Malmierca MS (2016) Topographic distribution of stimulus-specific adaptation across auditory cortical fields in the anesthetized rat. PLoS Biol 14:1002397.  https://doi.org/10.1371/journal.pbio.1002397 CrossRefGoogle Scholar
  50. Olpe HR et al (1990) CGP 35348: a centrally active blocker of GABAB receptors. Eur J Pharmacol 187:27–38CrossRefPubMedGoogle Scholar
  51. Ong J, Bexis S, Marino V, Parker DA, Kerr DI, Froestl W (2001) CGP 36216 is a selective antagonist at GABA(B) presynaptic receptors in rat brain. Eur J Pharmacol 415:191–195CrossRefPubMedGoogle Scholar
  52. Oyster CW, Takahashi ES (1975) Responses of rabbit superior colliculus neurons to repeated visual stimuli. J Neurophysiol 38:301–312CrossRefPubMedGoogle Scholar
  53. Pérez-González D, Malmierca MS (2012) Variability of the time course of stimulus-specific adaptation in the inferior colliculus. Front Neural Circuits 6:107.  https://doi.org/10.3389/fncir.2012.00107 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Pérez-González D, Malmierca MS, Covey E (2005) Novelty detector neurons in the mammalian auditory midbrain. Eur J Neurosci 22:2879–2885.  https://doi.org/10.1111/j.1460-9568.2005.04472.x CrossRefPubMedGoogle Scholar
  55. Pérez-González D, Malmierca MS, Moore JM, Hernandez O, Covey E (2006) Duration selective neurons in the inferior colliculus of the rat: topographic distribution and relation of duration sensitivity to other response properties. J Neurophysiol 95:823–836.  https://doi.org/10.1152/jn.00741.2005 CrossRefPubMedGoogle Scholar
  56. Pérez-González D, Hernandez O, Covey E, Malmierca MS (2012) GABA(A)-mediated inhibition modulates stimulus-specific adaptation in the inferior colliculus. PLoS One 7:e34297.  https://doi.org/10.1371/journal.pone.0034297 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Pham TM, Nurse S, Lacaille J-C (1998) Distinct GABAB actions via synaptic and extrasynaptic receptors in rat hippocampus in vitro. J Neurophysiol 80:297–308CrossRefPubMedGoogle Scholar
  58. Rees A (1990) A close-field sound system for auditory neurophysiology. J Physiol 430:6Google Scholar
  59. Scanziani M (2000) GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25:673–681CrossRefPubMedGoogle Scholar
  60. Sivaramakrishnan S, Sterbing-D’Angelo SJ, Filipovic B, D’Angelo WR, Oliver DL, Kuwada S (2004) GABA(A) synapses shape neuronal responses to sound intensity in the inferior colliculus. J Neurosci 24:5031–5043.  https://doi.org/10.1523/JNEUROSCI.0357-04.2004 CrossRefPubMedGoogle Scholar
  61. Staubli U, Scafidi J, Chun D (1999) GABAB receptor antagonism: facilitatory effects on memory parallel those on LTP induced by TBS but not HFS. J Neurosci 19:4609–4615PubMedGoogle Scholar
  62. Sun H, Wu SH (2008) Physiological characteristics of postinhibitory rebound depolarization in neurons of the rat’s dorsal cortex of the inferior colliculus studied in vitro. Brain Res 1226:70–81.  https://doi.org/10.1016/j.brainres.2008.06.010 CrossRefPubMedGoogle Scholar
  63. Sun H, Wu SH (2009) The physiological role of pre- and postsynaptic GABA(B) receptors in membrane excitability and synaptic transmission of neurons in the rat’s dorsal cortex of the inferior colliculus. Neuroscience 160:198–211.  https://doi.org/10.1016/j.neuroscience.2009.02.011 CrossRefPubMedGoogle Scholar
  64. Sun H, Ma CL, Kelly JB, Wu SH (2006) GABAB receptor-mediated presynaptic inhibition of glutamatergic transmission in the inferior colliculus. Neurosci Lett 399:151–156.  https://doi.org/10.1016/j.neulet.2006.01.049 CrossRefPubMedGoogle Scholar
  65. Ulanovsky N, Las L, Nelken I (2003) Processing of low-probability sounds by cortical neurons. Nat Neurosci 6:391–398.  https://doi.org/10.1038/nn1032 CrossRefPubMedGoogle Scholar
  66. Ulanovsky N, Las L, Farkas D, Nelken I (2004) Multiple time scales of adaptation in auditory cortex neurons. J Neurosci 24:10440–10453.  https://doi.org/10.1523/JNEUROSCI.1905-04.2004 CrossRefPubMedGoogle Scholar
  67. Valdés-Baizabal C, Parras GG, Ayala YA, Malmierca MS (2017) Endocannabinoid modulation of stimulus-specific adaptation in inferior colliculus neurons of the rat. Scientific Rep 7(1).  https://doi.org/10.1038/s41598-017-07460-w
  68. Vaughn MD, Pozza MF, Lingenhöhl K (1996) Excitatory acoustic responses in the inferior colliculus of the rat are increased by GABAB receptor blockade. Neuropharmacology 35(12):1761–1767CrossRefPubMedGoogle Scholar
  69. 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 29:13837–13849.  https://doi.org/10.1523/JNEUROSCI.3475-09.2009 CrossRefPubMedGoogle Scholar
  70. Wang H, Han Y-F, Chan Y-S, He J (2014) Stimulus-specific adaptation at the synapse level in vitro. PLoS One 9(12):114537.  https://doi.org/10.1371/journal.pone.0114537 CrossRefGoogle Scholar
  71. Williams AJ, Fuzessery ZM (2011) Differential roles of GABAergic and glycinergic input on FM selectivity in the inferior colliculus of the pallid bat. J Neurophysiol 106:2523–2535.  https://doi.org/10.1152/jn.00569.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Winkler I, Denham SL, Nelken I (2009) Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cognit Sci 13:532–540.  https://doi.org/10.1016/j.tics.2009.09.003 CrossRefGoogle Scholar
  73. Zhang Y, Wu SH (2000) Long-term potentiation in the inferior colliculus studied in rat brain slice. Hear Res 147:92–103CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Auditory Neuroscience Laboratory, Institute of Neuroscience of Castilla Y LeónUniversity of SalamancaSalamancaSpain
  2. 2.Department of Cell Biology and Pathology, Faculty of MedicineUniversity of SalamancaSalamancaSpain
  3. 3.Instituto de NeurobiologíaUniversidad Nacional Autónoma de MéxicoQuerétaroMexico

Personalised recommendations