Neurons, Connections, and Microcircuits of the Inferior Colliculus

  1. Ito, Tetsufumi 1
  2. Malmierca, Manuel S. 234
  1. 1 Kanazawa University
    info

    Kanazawa University

    Kanazawa, Japón

    ROR https://ror.org/02hwp6a56

  2. 2 Instituto de Neurociencias de Castilla y León
    info

    Instituto de Neurociencias de Castilla y León

    Salamanca, España

  3. 3 Universidad de Salamanca
    info

    Universidad de Salamanca

    Salamanca, España

    ROR https://ror.org/02f40zc51

  4. 4 Instituto de Investigación Biomédica de Salamanca
    info

    Instituto de Investigación Biomédica de Salamanca

    Salamanca, España

    ROR https://ror.org/03em6xj44

Llibre:
The Mammalian Auditory Pathways: Synaptic Organization and Microcircuits

Editorial: Springer

ISSN: 0947-2657 2197-1897

ISBN: 9783319717968 9783319717982

Any de publicació: 2018

Pàgines: 127-167

Tipus: Capítol de llibre

DOI: 10.1007/978-3-319-71798-2_6 GOOGLE SCHOLAR lock_openAccés obert editor

Resum

In this chapter, the neural circuitry of the inferior colliculus (IC) is described at a cellular level. The IC is subdivided into the central nucleus (ICC) and surrounding cortices that receive specific combinations of inputs and generate diverse outputs. Neuronal types in the IC can be distinguished by their dendritic arborization patterns, neurochemical profiles, and physiological properties. Based on these properties, neuronal types organizing the ICC appear to be different from those organizing the IC cortex. The IC receives ascending inputs from the cochlear nuclei, superior olivary complex, and nuclei of the lateral lemniscus, and the IC receives descending inputs from the auditory cortex and nonauditory inputs from various nuclei. Each input source forms terminal fields in particular zones of the IC. Massive commissural and local inputs are also present. One well-characterized cell type, the large GABAergic IC neuron, receives convergent input from all of these sources. The IC neurons project to the auditory thalamus as well as to lower brain stem nuclei. Anatomical and physiological features suggest that ICC acts as an auditory integration center, and IC cortex acts as a multimodal integration center and novelty detector. These data support the view that the lemniscal and nonlemniscal pathways emerge at the midbrain level.

Referències bibliogràfiques

  • Ahuja, T. K., & Wu, S. H. (2007). Intrinsic membrane properties and synaptic response characteristics of neurons in the rat’s external cortex of the inferior colliculus. Neuroscience, 145(3), 851–865.
  • Anderson, L. A., & Malmierca, M. S. (2013). The effect of auditory cortex deactivation on stimulus-specific adaptation in the inferior colliculus of the rat. European Journal of Neuroscience, 37(1), 52–62.
  • Aubrey, K. R., Rossi, F. M., Ruivo, R., Alboni, S., Bellenchi, G. C., Le Goff, A., et al. (2007). The transporters GlyT2 and VIAAT cooperate to determine the vesicular glycinergic phenotype. The Journal of Neuroscience, 27(23), 6273–6281.
  • Ayala, Y. A., & Malmierca, M. S. (2012). Stimulus-specific adaptation and deviance detection in the inferior colliculus. Frontiers in Neural Circuits, 6, 89. https://doi.org/10.3389/fncir.2012.00089 .
  • Ayala, Y. A., & Malmierca, M. S. (2015). Cholinergic modulation of stimulus-specific adaptation in the inferior colliculus. The Journal of Neuroscience, 35(35), 12261–12272.
  • Ayala, Y. A., Udeh, A., Dutta, K., Bishop, D., Malmierca, M. S., & Oliver, D. L. (2015). Differences in the strength of cortical and brainstem inputs to SSA and non-SSA neurons in the inferior colliculus. Scientific Reports, 5, 10383. https://doi.org/10.1038/srep10383 .
  • Bartlett, E. L., & Smith, P. H. (1999). Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. Journal of Neurophysiology, 81(5), 1999–2016.
  • Bartlett, E. L., Stark, J. M., Guillery, R. W., & Smith, P. H. (2000). Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience, 100(4), 811–828.
  • Caicedo, A., & Herbert, H. (1993). Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. The Journal of Comparative Neurology, 328(3), 377–392.
  • Cant, N. B., & Benson, C. G. (2006). Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): Differences in distribution of projections from the cochlear nuclei and the superior olivary complex. The Journal of Comparative Neurology, 495(5), 511–528.
  • Cant, N. B., & Benson, C. G. (2007). Multiple topographically organized projections connect the central nucleus of the inferior colliculus to the ventral division of the medial geniculate nucleus in the gerbil, Meriones unguiculatus. The Journal of Comparative Neurology, 503(3), 432–453.
  • Casseday, J. H., Fremouw, T., & Covey, E. (2002). The inferior colliculus: A hub for the central auditory system. In D. Oertel, R. R. Fay, & A. N. Popper (Eds.), Integrative functions in the mammalian auditory pathway (pp. 238–318). New York: Springer.
  • Chandrasekaran, L., Xiao, Y., & Sivaramakrishnan, S. (2013). Functional architecture of the inferior colliculus revealed with voltage-sensitive dyes. Frontiers in Neural Circuits, 7, 41. https://doi.org/10.3389/fncir.2013.00041 .
  • Chen, C., Rodriguez, F. C., Read, H. L., & Escabi, M. A. (2012). Spectrotemporal sound preferences of neighboring inferior colliculus neurons: Implications for local circuitry and processing. Frontiers in Neural Circuits, 6, 62. https://doi.org/10.3389/fncir.2012.00062 .
  • Chernock, M. L., Larue, D. T., & Winer, J. A. (2004). A periodic network of neurochemical modules in the inferior colliculus. Hearing Research, 188(1-2), 12–20.
  • Coleman, J. R., & Clerici, W. J. (1987). Sources of projections to subdivisions of the inferior colliculus in the rat. The Journal of Comparative Neurology, 262(2), 215–226.
  • Coote, E. J., & Rees, A. (2008). The distribution of nitric oxide synthase in the inferior colliculus of guinea pig. Neuroscience, 154(1), 218–225.
  • Covey, E., & Carr, C. E. (2005). The auditory midbrain in bats and birds. In J. A. Winer & C. E. Schreiner (Eds.), The inferior colliculus (pp. 493–536). New York: Springer.
  • Dolan, D. F., & Nuttall, A. L. (1988). Masked cochlear whole-nerve response intensity functions altered by electrical stimulation of the crossed olivocochlear bundle. Journal of the Acoustical Society of America, 83(3), 1081–1086.
  • Duque, D., Perez-Gonzalez, D., Ayala, Y. A., Palmer, A. R., & Malmierca, M. S. (2012). Topographic distribution, frequency, and intensity dependence of stimulus-specific adaptation in the inferior colliculus of the rat. The Journal of Neuroscience, 32(49), 17762–17774.
  • Faingold, C. L., Gehlbach, G., & Caspary, D. M. (1989). On the role of GABA as an inhibitory neurotransmitter in inferior colliculus neurons: Iontophoretic studies. Brain Research, 500(1-2), 302–312.
  • Faingold, C. L., Boersma Anderson, C. A., & Caspary, D. M. (1991). Involvement of GABA in acoustically evoked inhibition in inferior colliculus neurons. Hearing Research, 52(1), 201–216.
  • Faye-Lund, H., & Osen, K. K. (1985). Anatomy of the inferior colliculus in rat. Anatomy and Embryology (Berlin), 171(1), 1–20.
  • Fremeau, R. T., Jr., Troyer, M. D., Pahner, I., Nygaard, G. O., Tran, C. H., Reimer, R. J., Bellocchio, E. E., Fortin, D., Storm-Mathisen, J., & Edwards, R. H. (2001). The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron, 31(2), 247–260.
  • Games, K. D., & Winer, J. A. (1988). Layer V in rat auditory cortex: Projections to the inferior colliculus and contralateral cortex. Hearing Research, 34(1), 1–25.
  • Geis, H. R., & Borst, J. G. (2013). Large GABAergic neurons form a distinct subclass within the mouse dorsal cortex of the inferior colliculus with respect to intrinsic properties, synaptic inputs, sound responses, and projections. The Journal of Comparative Neurology, 521(1), 189–202.
  • González-Hernández, T. H., Meyer, G., & Ferres-Torres, R. (1986). The commissural interconnections of the inferior colliculus in the albino mouse. Brain Research, 368(2), 268–276.
  • Grimsley, C. A., Sanchez, J. T., & Sivaramakrishnan, S. (2013). Midbrain local circuits shape sound intensity codes. Frontiers in Neural Circuits, 7, 174. https://doi.org/10.3389/fncir.2013.00174 .
  • Gruters, K. G., & Groh, J. M. (2012). Sounds and beyond: Multisensory and other non-auditory signals in the inferior colliculus. Frontiers in Neural Circuits, 6, 96. https://doi.org/10.3389/fncir.2012.00096 .
  • Henderson, Z., & Sherriff, F. E. (1991). Distribution of choline acetyltransferase immunoreactive axons and terminals in the rat and ferret brainstem. The Journal of Comparative Neurology, 314(1), 147–163.
  • Herbert, H., Aschoff, A., & Ostwald, J. (1991). Topography of projections from the auditory cortex to the inferior colliculus in the rat. The Journal of Comparative Neurology, 304(1), 103–122.
  • Hernández, O., Rees, A., & Malmierca, M. S. (2006). A GABAergic component in the commissure of the inferior colliculus in rat. Neuroreport, 17(15), 1611–1614.
  • Hu, B., Senatorov, V., & Mooney, D. (1994). Lemniscal and non-lemniscal synaptic transmission in rat auditory thalamus. The Journal of Physiology, 479(2), 217–231.
  • Itaya, S. K., & Van Hoesen, G. W. (1982). Retinal innervation of the inferior colliculus in rat and monkey. Brain Research, 233(1), 45–52.
  • Ito, T., & Oliver, D. L. (2010). Origins of glutamatergic terminals in the inferior colliculus identified by retrograde transport and expression of VGLUT1 and VGLUT2 genes. Frontiers in Neuroanatomy, 4, 135. https://doi.org/10.3389/fnana.2010.00135 .
  • Ito, T., & Oliver, D. L. (2012). The basic circuit of the IC: Tectothalamic neurons with different patterns of synaptic organization send different messages to the thalamus. Frontiers in Neural Circuits, 6, 48. https://doi.org/10.3389/fncir.2012.00048 .
  • Ito, T., & Oliver, D. L. (2014). Local and commissural IC neurons make axosomatic inputs on large GABAergic tectothalamic neurons. The Journal of Comparative Neurology, 522(15), 3539–3554.
  • Ito, T., Hioki, H., Nakamura, K., Tanaka, Y., Nakade, H., Kaneko, T., Iino, S., & Nojyo, Y. (2007). Gamma-aminobutyric acid-containing sympathetic preganglionic neurons in rat thoracic spinal cord send their axons to the superior cervical ganglion. The Journal of Comparative Neurology, 502(1), 113–125.
  • Ito, T., Bishop, D. C., & Oliver, D. L. (2009). Two classes of GABAergic neurons in the inferior colliculus. The Journal of Neuroscience, 29(44), 13860–13869.
  • Ito, T., Bishop, D. C., & Oliver, D. L. (2011). Expression of glutamate and inhibitory amino acid vesicular transporters in the rodent auditory brainstem. The Journal of Comparative Neurology, 519(2), 316–340.
  • Ito, T., Hioki, H., Sohn, J., Okamoto, S., Kaneko, T., Iino, S., & Oliver, D. L. (2015). Convergence of lemniscal and local excitatory inputs on large GABAergic tectothalamic neurons. The Journal of Comparative Neurology, 523, 2277–2296.
  • Joris, P. X., & Yin, T. C. (1995). Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. Journal of Neurophysiology, 73(3), 1043–1062.
  • Kandler, K., & Herbert, H. (1991). Auditory projections from the cochlear nucleus to pontine and mesencephalic reticular nuclei in the rat. Brain Research, 562(2), 230–242.
  • Klepper, A., & Herbert, H. (1991). Distribution and origin of noradrenergic and serotonergic fibers in the cochlear nucleus and inferior colliculus of the rat. Brain Research, 557(1-2), 190–201.
  • Kudo, M., & Niimi, K. (1980). Ascending projections of the inferior colliculus in the cat: An autoradiographic study. The Journal of Comparative Neurology, 191(4), 545–556.
  • Kulesza, R. J., Vinuela, A., Saldana, E., & Berrebi, A. S. (2002). Unbiased stereological estimates of neuron number in subcortical auditory nuclei of the rat. Hearing Research, 168(1-2), 12–24.
  • Kuo, R. I., & Wu, G. K. (2012). The generation of direction selectivity in the auditory system. Neuron, 73(5), 1016–1027.
  • Kuwada, S., Batra, R., Yin, T. C. T., Oliver, D. L., Haberly, L. B., & Stanford, T. R. (1997). Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. The Journal of Neuroscience, 17(19), 7565–7581.
  • LeDoux, J. E., Ruggiero, D. A., & Reis, D. J. (1985). Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. The Journal of Comparative Neurology, 242(2), 182–213.
  • Lesicko, A., & Llano, D. (2015). Connectional and neurochemical modularity of the mouse inferior colliculus. Abstract PS-564, Association for Research in Otolaryngology Midwinter Meeting, February 21–25, Baltimore, MD.
  • Li, Y., Evans, M. S., & Faingold, C. L. (1998). In vitro electrophysiology of neurons in subnuclei of rat inferior colliculus. Hearing Research, 121(1-2), 1–10.
  • Linke, R. (1999). Differential projection patterns of superior and inferior collicular neurons onto posterior paralaminar nuclei of the thalamus surrounding the medial geniculate body in the rat. European Journal of Neuroscience, 11(1), 187–203.
  • Loftus, W. C., Bishop, D. C., Saint Marie, R. L., & Oliver, D. L. (2004). Organization of binaural excitatory and inhibitory inputs to the inferior colliculus from the superior olive. The Journal of Comparative Neurology, 472(3), 330–344.
  • Loftus, W. C., Bishop, D. C., & Oliver, D. L. (2010). Differential patterns of inputs create functional zones in central nucleus of inferior colliculus. The Journal of Neuroscience, 30(40), 13396–13408.
  • Loftus, W. C., Malmierca, M. S., Bishop, D. C., & Oliver, D. L. (2008). The cytoarchitecture of the inferior colliculus revisited: A common organization of the lateral cortex in rat and cat. Neuroscience, 154(1), 196–205.
  • Malmierca, M. S. (2015). Auditory system. In G. Paxinos (Ed.), The rat nervous system (4th ed., pp. 865–946). Amsterdam: Academic Press.
  • Malmierca, M. S., & Ryugo, D. K. (2011). Descending connections of auditory cortex to the midbrain and brainstem. In J. A. Winer & C. E. Schreiner (Eds.), The auditory cortex (pp. 189–208). New York: Springer.
  • Malmierca, M. S., Blackstad, T. W., Osen, K. K., Karagulle, T., & Molowny, R. L. (1993). The central nucleus of the inferior colliculus in rat: A Golgi and computer reconstruction study of neuronal and laminar structure. The Journal of Comparative Neurology, 333(1), 1–27.
  • Malmierca, M. S., Rees, A., Le Beau, F. E., & Bjaalie, J. G. (1995). Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. The Journal of Comparative Neurology, 357(1), 124–144.
  • Malmierca, M. S., Hernández, O., Falconi, A., Lopez-Poveda, E. A., Merchán, M., & Rees, A. (2003). The commissure of the inferior colliculus shapes frequency response areas in rat: An in vivo study using reversible blockade with microinjection of kynurenic acid. Experimental Brain Research, 153(4), 522–529.
  • Malmierca, M. S., Hernández, O., & Rees, A. (2005). Intercollicular commissural projections modulate neuronal responses in the inferior colliculus. European Journal of Neuroscience, 21(10), 2701–2710.
  • Malmierca, M. S., Izquierdo, M. A., Cristaudo, S., Hernandez, O., Pérez-González, D., Covey, E., et al. (2008). A discontinuous tonotopic organization in the inferior colliculus of the rat. The Journal of Neuroscience, 28(18), 4767–4776.
  • Malmierca, M. S., Hernandez, O., Antunes, F. M., & Rees, A. (2009). Divergent and point-to-point connections in the commissural pathway between the inferior colliculi. The Journal of Comparative Neurology, 514(3), 226–239.
  • Malmierca, M. S., Blackstad, T. W., & Osen, K. K. (2011). Computer-assisted 3-D reconstructions of Golgi-impregnated neurons in the cortical regions of the inferior colliculus of rat. Hearing Research, 274(1-2), 13–26.
  • Matsuda, W., Furuta, T., Nakamura, K. C., Hioki, H., Fujiyama, F., Arai, R., et al. (2009). Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. The Journal of Neuroscience, 29(2), 444–453.
  • Merchán, M., Aguilar, L. A., Lopez-Poveda, E. A., & Malmierca, M. S. (2005). The inferior colliculus of the rat: Quantitative immunocytochemical study of GABA and glycine. Neuroscience, 136(3), 907–925.
  • Mitani, A., Shimokouchi, M., & Nomura, S. (1983). Effects of stimulation of the primary auditory cortex upon colliculogeniculate neurons in the inferior colliculus of the cat. Neuroscience Letters, 42(2), 185–189.
  • Moller, A. R., & Rees, A. (1986). Dynamic properties of the responses of single neurons in the inferior colliculus of the rat. Hearing Research, 24(3), 203–215.
  • Morest, D. K., & Oliver, D. L. (1984). The neuronal architecture of the inferior colliculus in the cat: Defining the functional anatomy of the auditory midbrain. The Journal of Comparative Neurology, 222(2), 209–236.
  • Motts, S. D., & Schofield, B. R. (2009). Sources of cholinergic input to the inferior colliculus. Neuroscience, 160(1), 103–114.
  • Nakagawa, H., Ikeda, M., Houtani, T., Ueyama, T., Baba, K., Kondoh, A., et al. (1995). Immunohistochemical evidence for enkephalin and neuropeptide Y in rat inferior colliculus neurons that provide ascending or commissural fibers. Brain Research, 690(2), 236–240.
  • Netser, S., Zahar, Y., & Gutfreund, Y. (2011). Stimulus-specific adaptation: Can it be a neural correlate of behavioral habituation? The Journal of Neuroscience, 31(49), 17811–17820.
  • Nwabueze-Ogbo, F. C., Popelar, J., & Syka, J. (2002). Changes in the acoustically evoked activity in the inferior colliculus of the rat after functional ablation of the auditory cortex. Physiological Research, 51(Supplement 1), 95–104.
  • Okoyama, S., Ohbayashi, M., Ito, M., & Harada, S. (2006). Neuronal organization of the rat inferior colliculus participating in four major auditory pathways. Hearing Research, 218(1-2), 72–80.
  • Oliver, D. L. (1984). Neuron types in the central nucleus of the inferior colliculus that project to the medial geniculate body. Neuroscience, 11(2), 409–424.
  • Oliver, D. L. (2005). Neuronal organization in the inferior colliculus. In J. A. Winer & C. E. Schreiner (Eds.), The inferior colliculus (pp. 69–114). New York: Springer.
  • Oliver, D. L., & Morest, D. K. (1984). The central nucleus of the inferior colliculus in the cat. The Journal of Comparative Neurology, 222(2), 237–264.
  • Oliver, D. L., & Huerta, M. F. (1992). Inferior and superior colliculi. In D. B. Webster, A. N. Popper, & R. R. Fay (Eds.), The mammalian auditory pathway: Neuroanatomy (pp. 168–221). New York: Springer.
  • Oliver, D. L., Kuwada, S., Yin, T. C., Haberly, L. B., & Henkel, C. K. (1991). Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. The Journal of Comparative Neurology, 303(1), 75–100.
  • Oliver, D. L., Winer, J. A., Beckius, G. E., & Saint Marie, R. L. (1994). Morphology of GABAergic neurons in the inferior colliculus of the cat. The Journal of Comparative Neurology, 340(1), 27–42.
  • Oliver, D. L., Beckius, G. E., Bishop, D. C., & Kuwada, S. (1997). Simultaneous anterograde labeling of axonal layers from lateral superior olive and dorsal cochlear nucleus in the inferior colliculus of the cat. The Journal of Comparative Neurology, 382(2), 215–229.
  • Oliver, D. L., Beckius, G. E., Bishop, D. C., Loftus, W. C., & Batra, R. (2003). Topography of interaural temporal disparity coding in projections of medial superior olive to inferior colliculus. The Journal of Neuroscience, 23(19), 7438–7449.
  • Oliver, D. L., Izquierdo, M. A., & Malmierca, M. S. (2011). Persistent effects of early augmented acoustic environment on the auditory brainstem. Neuroscience, 184, 75–87.
  • Ono, M., Yanagawa, Y., & Koyano, K. (2005). GABAergic neurons in inferior colliculus of the GAD67-GFP knock-in mouse: Electrophysiological and morphological properties. Neuroscience Research, 51(4), 475–492.
  • Orton, L. D., & Rees, A. (2014). Intercollicular commissural connections refine the representation of sound frequency and level in the auditory midbrain. eLife, 3, e03764.
  • Palmer, A. R., Shackleton, T. M., Sumner, C. J., Zobay, O., & Rees, A. (2013). Classification of frequency response areas in the inferior colliculus reveals continua not discrete classes. The Journal of Physiology, 591(16), 4003–4025.
  • Pérez-González, D., Malmierca, M. S., & Covey, E. (2005). Novelty detector neurons in the mammalian auditory midbrain. European Journal of Neuroscience, 22(11), 2879–2885.
  • Pérez-González, D., Malmierca, M. S., Moore, J. M., Hernández, 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. Journal of Neurophysiology, 95(2), 823–836.
  • Pérez-González, D., Hernández, O., Covey, E., & Malmierca, M. S. (2012). GABAA-mediated inhibition modulates stimulus-specific adaptation in the inferior colliculus. PLoS One, 7(3), e34297. https://doi.org/10.1371/journal.pone.0034297 .
  • Peruzzi, D., Sivaramakrishnan, S., & Oliver, D. L. (2000). Identification of cell types in brain slices of the inferior colliculus. Neuroscience, 101(2), 403–416.
  • Poon, P. W., Chen, X., & Cheung, Y. M. (1992). Differences in FM response correlate with morphology of neurons in the rat inferior colliculus. Experimental Brain Research, 91(1), 94–104.
  • Rajan, R. (1990). Electrical stimulation of the inferior colliculus at low rates protects the cochlea from auditory desensitization. Brain Research, 506(2), 192–204.
  • Rees, A., & Moller, A. R. (1987). Stimulus properties influencing the responses of inferior colliculus neurons to amplitude-modulated sounds. Hearing Research, 27(2), 129–143.
  • Reetz, G., & Ehret, G. (1999). Inputs from three brainstem sources to identified neurons of the mouse inferior colliculus slice. Brain Research, 816(2), 527–543.
  • Saint Marie, R. L. (1996). Glutamatergic connections of the auditory midbrain: Selective uptake and axonal transport of D-[3H]aspartate. The Journal of Comparative Neurology, 373(2), 255–270.
  • Saint Marie, R. L., Stanforth, D. A., & Jubelier, E. M. (1997). Substrate for rapid feedforward inhibition of the auditory forebrain. Brain Research, 765(1), 173–176.
  • Saldaña, E., & Merchán, M. A. (1992). Intrinsic and commissural connections of the rat inferior colliculus. The Journal of Comparative Neurology, 319(3), 417–437.
  • Saldaña, E., & Merchán, M. A. (2005). Intrinsic and commissural connections of the inferior colliculus. In J. A. Winer & C. E. Schreiner (Eds.), The inferior colliculus (pp. 155–181). New York: Springer.
  • Saldaña, E., Feliciano, M., & Mugnaini, E. (1996). Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. The Journal of Comparative Neurology, 371(1), 15–40.
  • Schreiner, C. E., & Langner, G. (1988). Periodicity coding in the inferior colliculus of the cat. II. Topographical organization. Journal of Neurophysiology, 60(6), 1823–1840.
  • Schreiner, C. E., & Langner, G. (1997). Laminar fine structure of frequency organization in auditory midbrain. Nature, 388(6640), 383–386.
  • Shammah-Lagnado, S. J., Alheid, G. F., & Heimer, L. (1996). Efferent connections of the caudal part of the globus pallidus in the rat. The Journal of Comparative Neurology, 376(3), 489–507.
  • Shera, C. A. (2015). The spiral staircase: Tonotopic microstructure and cochlear tuning. The Journal of Neuroscience, 35(11), 4683–4690.
  • Shneiderman, A., & Henkel, C. K. (1987). Banding of lateral superior olivary nucleus afferents in the inferior colliculus: A possible substrate for sensory integration. The Journal of Comparative Neurology, 266(4), 519–534.
  • Sivaramakrishnan, S., & Oliver, D. L. (2001). Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. The Journal of Neuroscience, 21(8), 2861–2877.
  • Sivaramakrishnan, S., Sanchez, J. T., & Grimsley, C. A. (2013). High concentrations of divalent cations isolate monosynaptic inputs from local circuits in the auditory midbrain. Frontiers in Neural Circuits, 7, 175. https://doi.org/10.3389/fncir.2013.00175 .
  • Smith, P. H. (1992). Anatomy and physiology of multipolar cells in the rat inferior collicular cortex using the in vitro brain slice technique. The Journal of Neuroscience, 12(9), 3700–3715.
  • Sun, H., & Wu, S. H. (2008). Modification of membrane excitability of neurons in the rat's dorsal cortex of the inferior colliculus by preceding hyperpolarization. Neuroscience, 154(1), 257–272.
  • Tan, M. L., Theeuwes, H. P., Feenstra, L., & Borst, J. G. (2007). Membrane properties and firing patterns of inferior colliculus neurons: An in vivo patch-clamp study in rodents. Journal of Neurophysiology, 98(1), 443–453.
  • Tanaka, I., & Ezure, K. (2004). Overall distribution of GLYT2 mRNA-containing versus GAD67 mRNA-containing neurons and colocalization of both mRNAs in midbrain, pons, and cerebellum in rats. Neuroscience Research, 49(2), 165–178.
  • Tokunaga, A., Sugita, S., & Otani, K. (1984). Auditory and non-auditory subcortical afferents to the inferior colliculus in the rat. Journal für Hirnforschung, 25(4), 461–472.
  • Tongjaroenbuangam, W., Jongkamonwiwat, N., Phansuwan-Pujito, P., Casalotti, S. O., Forge, A., Dodson, H., et al. (2006). Relationship of opioid receptors with GABAergic neurons in the rat inferior colliculus. European Journal of Neuroscience, 24(7), 1987–1994.
  • Ulanovsky, N., Las, L., & Nelken, I. (2003). Processing of low-probability sounds by cortical neurons. Nature Neuroscience, 6(4), 391–398.
  • Venkataraman, Y., & Bartlett, E. L. (2013). Post-natal development of synaptic properties of the gabaergic projection from inferior colliculus to auditory thalamus. Journal of Neurophysiology, 109(12), 2866–2882.
  • Wallace, M. N., Shackleton, T. M., & Palmer, A. R. (2012). Morphological and physiological characteristics of laminar cells in the central nucleus of the inferior colliculus. Frontiers in Neural Circuits, 6, 55. https://doi.org/10.3389/fncir.2012.00055 .
  • White, J. S., & Warr, W. B. (1983). The dual origins of the olivocochlear bundle in the albino rat. The Journal of Comparative Neurology, 219(2), 203–214.
  • Whitley, J. M., & Henkel, C. K. (1984). Topographical organization of the inferior collicular projection and other connections of the ventral nucleus of the lateral lemniscus in the cat. The Journal of Comparative Neurology, 229(2), 257–270.
  • Wiberg, M., Westman, J., & Blomqvist, A. (1987). Somatosensory projection to the mesencephalon: An anatomical study in the monkey. The Journal of Comparative Neurology, 264(1), 92–117.
  • Willard, F. H., & Ryugo, D. (1983). Anatomy of the central auditory system. In J. F. Willot (Ed.), The auditory psychobiology of the mouse (pp. 201–304). Springfield, IL: Charles C. Thomas.
  • Winer, J. A., Saint Marie, R. L., Larue, D. T., & Oliver, D. L. (1996). GABAergic feedforward projections from the inferior colliculus to the medial geniculate body. Proceedings of the National Academy of Sciences of the United States of America, 93(15), 8005–8010.
  • Wynne, B., & Robertson, D. (1997). Somatostatin and substance P-like immunoreactivity in the auditory brainstem of the adult rat. Journal of Chemical Neuroanatomy, 12(4), 259–266.
  • Wynne, B., Harvey, A. R., Robertson, D., & Sirinathsinghji, D. J. (1995). Neurotransmitter and neuromodulator systems of the rat inferior colliculus and auditory brainstem studied by in situ hybridization. Journal of Chemical Neuroanatomy, 9(4), 289–300.
  • Yasui, Y., Nakano, K., Kayahara, T., & Mizuno, N. (1991). Non-dopaminergic projections from the substantia nigra pars lateralis to the inferior colliculus in the rat. Brain Research, 559(1), 139–144.
  • Zhang, H., & Kelly, J. B. (2010). Time dependence of binaural responses in the rat’s central nucleus of the inferior colliculus. Hearing Research, 268(1-2), 271–280.