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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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
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
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
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
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, Milan
Ayala YA, Malmierca MS (2015) Modulation of auditory deviant saliency in the inferior colliculus. In: Paper presented at the ARO midwinter meeting, Baltimore
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
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
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
Binns KE, Salt TE (1995) Excitatory amino acid receptors modulate habituation of the response to visual stimulation in the cat superior colliculus. Vis Neurosci 12:563–571
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):629–639
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 80:1686–1701
Calford MB (1983) The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J Neurosci 3:2350–2364
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
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 131:917–933
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
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
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
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
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
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
Eytan D, Brenner N, Marom S (2003) Selective adaptation in networks of cortical neurons. J Neurosci 23:9349–9356
Faingold CL, Boersma Anderson CA, Caspary DM (1991) Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons. Hear Res 52:201–216
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 23:3052–3065
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
Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185–204
Hammond C (2015) The ionotropic GABAA receptor, chap 9. In: Cellular and molecular neurophysiology, 4th edn. Academic Press, Constance Hammond
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
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
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
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
Kelly JB, Caspary DM (2005) Pharmacology of the inferior colliculus. In: Winer JA, Schreiner CE (eds) the inferior colliculus. Springer, New York, pp 248–281
Kraus N, McGee T, Littman T, Nicol T, King C (1994) Nonprimary auditory thalamic representation of acoustic change. J Neurophysiol 72:1270–1277
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 21:7303–7312
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
Ma CL, Kelly JB, Wu SH (2002) Presynaptic modulation of GABAergic inhibition by GABA(B) receptors in the rat’s inferior colliculus. Neuroscience 114:207–215
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
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
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
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
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):13–26
Maravall M (2013) Adaptation and sensory coding. In: Quiroga RQ, Panzeri S (eds) Principles of neural coding. CRC Press, Boca Raton, pp 357–377
Merrill EG, Ainsworth A (1972) Glass-coated platinum-plated tungsten microelectrodes. Med Biol Eng 10:662–672
Milbrandt JC, Albin RL, Caspary DM (1994) Age-related decrease in GABAB receptor binding in the Fischer 344 rat inferior colliculus. Neurobiol Aging 15:699–703
Mott D (2015) The metabotropic GABAB receptors, chapter 11. In: Cellular and molecular neurophysiology, 4th edn. Academic Press, Constance Hammond
Näätänen R (1992) Attention and brain function. Lawrence Erlbaum, Hillsdale
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
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
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
Olpe HR et al (1990) CGP 35348: a centrally active blocker of GABAB receptors. Eur J Pharmacol 187:27–38
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 415:191–195
Oyster CW, Takahashi ES (1975) Responses of rabbit superior colliculus neurons to repeated visual stimuli. J Neurophysiol 38:301–312
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
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
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
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
Pham TM, Nurse S, Lacaille J-C (1998) Distinct GABAB actions via synaptic and extrasynaptic receptors in rat hippocampus in vitro. J Neurophysiol 80:297–308
Rees A (1990) A close-field sound system for auditory neurophysiology. J Physiol 430:6
Scanziani M (2000) GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25:673–681
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
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 19:4609–4615
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
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
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
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
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
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
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):1761–1767
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
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
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
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
Zhang Y, Wu SH (2000) Long-term potentiation in the inferior colliculus studied in rat brain slice. Hear Res 147:92–103
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Ayala, Y.A., Malmierca, M.S. The effect of inhibition on stimulus-specific adaptation in the inferior colliculus. Brain Struct Funct 223, 1391–1407 (2018). https://doi.org/10.1007/s00429-017-1546-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-017-1546-4