Abstract
The inferior colliculus (IC) is the first integration center of the auditory system. After the transformation of sound to neural signals in the cochlea, the signals are analyzed by brainstem auditory nuclei that, in turn, transmit this information to the IC. However, the neural circuitry that underlies this integration is unclear. This review consists of two parts: one is about the cell type which is likely to integrate sound information, and the other is about a technique which is useful for studying local circuitry. Large GABAergic (LG) neurons receive dense excitatory axosomatic terminals that originate from the lower brainstem auditory nuclei as well as local IC neurons. Dozens of axons coming from both local and lower brainstem neurons converge on a single LG soma. Excitatory neurons in IC can innervate many nearby LG somata in the same fibrodendritic lamina. The combination of local and ascending inputs is well suited for auditory integration. LG neurons are one of the main sources of inhibition in the medial geniculate body (MGB). LG neurons and the tectothalamic inhibitory system are present in a wide variety of mammalian species. This suggests that the circuitry of excitatory and inhibitory tectothalamic projections may have evolved earlier than GABAergic interneurons in the MGB, which are found in fewer species. Cellular-level functional imaging provides both morphological and functional information about local circuitry. In the last part of this review, we describe an in vivo calcium imaging study that sheds light on the functional organization of the IC.









Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Adams JC (1979) Ascending projections to the inferior colliculus. J Comp Neurol 183(3):519–538
Altschuler RA, Tong L, Holt AG, Oliver DL (2008) Immunolocalization of vesicular glutamate transporters 1 and 2 in the rat inferior colliculus. Neuroscience 154(1):226–232
Arnault P, Roger M (1990) Ventral temporal cortex in the rat: connections of secondary auditory areas Te2 and Te3. J Comp Neurol 302(1):110–123
Bandyopadhyay S, Shamma SA, Kanold PO (2010) Dichotomy of functional organization in the mouse auditory cortex. Nat Neurosci 13(3):361–368
Bartlett EL, Smith PH (1999) Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. J Neurophysiol 81(5):1999–2016
Cant NB (1982) Identification of cell types in the anteroventral cochlear nucleus that project to the inferior colliculus. Neurosci Lett 32(3):241–246
Cant NB, Benson CG (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. J Comp Neurol 495(5):511–528
Casseday JH, Ehrlich D, Covey E (1994) Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science 264(5160):847–850
Casseday JH, Fremouw T, Covey E (2002) The inferior colliculus: a hub for the central auditory system. In: Oertel D, Fay RR, Popper AN (eds) Integrative functions in the mammalian auditory pathway. Springer, New York, pp 238–318
Chernock ML, Larue DT, Winer JA (2004) A periodic network of neurochemical modules in the inferior colliculus. Hear Res 188(1–2):12–20
Covey E, Casseday JH (1991) The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathways for analyzing temporal features of sound. J Neurosci 11(11):3456–3470
Fay RR (1988) Hearing in vertebrates: a psychophysics databook. Hill-Fay Associates, Winnetka
Faye-Lund H, Osen KK (1985) Anatomy of the inferior colliculus in rat. Anat Embryol (Berl) 171(1):1–20
Furuta T, Tomioka R, Taki K, Nakamura K, Tamamaki N, Kaneko T (2001) In vivo transduction of central neurons using recombinant Sindbis virus: Golgi-like labeling of dendrites and axons with membrane-targeted fluorescent proteins. J Histochem Cytochem 49(12):1497–1508
Geis HR, Borst JG (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. J Comp Neurol 521(1):189–202
Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90(3):983–1012
Herbert H, Aschoff A, Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304(1):103–122
Hioki H, Nakamura H, Ma YF, Konno M, Hayakawa T, Nakamura KC, Fujiyama F, Kaneko T (2010) Vesicular glutamate transporter 3-expressing nonserotonergic projection neurons constitute a subregion in the rat midbrain raphe nuclei. J Comp Neurol 518(5):668–686
Holderith N, Lorincz A, Katona G, Rozsa B, Kulik A, Watanabe M, Nusser Z (2012) Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat Neurosci 15(7):988–997
Itaya SK, Van Hoesen GW (1982) Retinal innervation of the inferior colliculus in rat and monkey. Brain Res 233(1):45–52
Ito T, Oliver DL (2010) Origins of glutamatergic terminals in the inferior colliculus identified by retrograde transport and expression of VGLUT1 and VGLUT2 genes. Front Neuroanat 4:135
Ito T, Oliver DL (2012) The basic circuit of the IC: tectothalamic neurons with different patterns of synaptic organization send different messages to the thalamus. Front Neural Circuits 6:48
Ito T, Oliver DL (2014) Local and commissural IC neurons make axosomatic inputs on large GABAergic tectothalamic neurons. J Comp Neurol 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. J Comp Neurol 502(1):113–125
Ito T, Bishop DC, Oliver DL (2009) Two classes of GABAergic neurons in the inferior colliculus. J Neurosci 29(44):13860–13869
Ito T, Bishop DC, Oliver DL (2011) Expression of glutamate and inhibitory amino acid vesicular transporters in the rodent auditory brainstem. J Comp Neurol 519(2):316–340
Ito T, Hirose J, Murase K, Ikeda H (2014) Determining auditory-evoked activities from multiple cells in layer 1 of the dorsal cortex of the inferior colliculus of mice by in vivo calcium imaging. Brain Res 1590:45–55
Ito T, Hioki H, Sohn J, Okamoto S, Kaneko T, Iino S, Oliver DL (2015) Convergence of lemniscal and local excitatory inputs on large GABAergic tectothalamic neurons. J Comp Neurol 523(15):2277–2296
Jones EG (2007) The medial geniculate complex. The thalamus, 2nd edn. Cambridge University, New York, pp 875–923
Joris PX, Smith PH (2008) The volley theory and the spherical cell puzzle. Neuroscience 154(1):65–76
Kimura A, Donishi T, Okamoto K, Tamai Y (2005) Topography of projections from the primary and non-primary auditory cortical areas to the medial geniculate body and thalamic reticular nucleus in the rat. Neuroscience 135(4):1325–1342
Kimura A, Yokoi I, Imbe H, Donishi T, Kaneoke Y (2012) Auditory thalamic reticular nucleus of the rat: anatomical nodes for modulation of auditory and cross-modal sensory processing in the loop connectivity between the cortex and thalamus. J Comp Neurol 520(7):1457–1480
Kuo RI, Wu GK (2012) The generation of direction selectivity in the auditory system. Neuron 73(5):1016–1027
Kuwada S, Batra R, Yin TC, Oliver DL, Haberly LB, Stanford TR (1997) Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat. J Neurosci 17(19):7565–7581
Lee CC, Sherman SM (2010) Topography and physiology of ascending streams in the auditory tectothalamic pathway. Proc Natl Acad Sci U S A 107(1):372–377
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. Eur J Neurosci 11(1):187–203
Loftus WC, Bishop DC, Oliver DL (2010) Differential patterns of inputs create functional zones in central nucleus of inferior colliculus. J Neurosci 30(40):13396–13408
Malmierca MS, Blackstad TW, Osen KK, Karagulle T, Molowny RL (1993) The central nucleus of the inferior colliculus in rat: a Golgi and computer reconstruction study of neuronal and laminar structure. J Comp Neurol 333(1):1–27
Matsuda W, Furuta T, Nakamura KC, Hioki H, Fujiyama F, Arai R, Kaneko T (2009) Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J Neurosci 29(2):444–453
Mellott JG, Foster NL, Nakamoto KT, Motts SD, Schofield BR (2014) Distribution of GABAergic cells in the inferior colliculus that project to the thalamus. Front Neuroanat 8:17
Merchan M, Aguilar LA, Lopez-Poveda EA, Malmierca MS (2005) The inferior colliculus of the rat: quantitative immunocytochemical study of GABA and glycine. Neuroscience 136(3):907–925
Morest DK (1971) Dendrodendritic synapses of cells that have axons: the fine structure of the Golgi type II cell in the medial geniculate body of the cat. Z Anat Entwicklungsgesch 133(2):216–246
Morest DK (1975) Synaptic relationships of Golgi type II cells in the medial geniculate body of the cat. J Comp Neurol 162(2):157–193
Morest DK, Oliver DL (1984) The neuronal architecture of the inferior colliculus in the cat: defining the functional anatomy of the auditory midbrain. J Comp Neurol 222(2):209–236
Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294(5550):2348–2351
Nakagawa H, Ikeda M, Houtani T, Ueyama T, Baba K, Kondoh A, Yamamoto T, Yamashita T, Sugimoto T (1995) Immunohistochemical evidence for enkephalin and neuropeptide Y in rat inferior colliculus neurons that provide ascending or commissural fibers. Brain Res 690(2):236–240
Oliver DL (1984) Dorsal cochlear nucleus projections to the inferior colliculus in the cat: a light and electron microscopic study. J Comp Neurol 224(2):155–172
Oliver DL (1987) Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: possible substrates for binaural interaction. J Comp Neurol 264(1):24–46
Oliver DL (2005) Neuronal organization in the inferior colliculus, chapter 2. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 69–114
Oliver DL, Morest DK (1984) The central nucleus of the inferior colliculus in the cat. J Comp Neurol 222(2):237–264
Oliver DL, Kuwada S, Yin TC, Haberly LB, Henkel CK (1991) Dendritic and axonal morphology of HRP-injected neurons in the inferior colliculus of the cat. J Comp Neurol 303(1):75–100
Oliver DL, Winer JA, Beckius GE, Saint Marie RL (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat. J Comp Neurol 340(1):27–42
Oliver DL, Beckius GE, Shneiderman A (1995) Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: a study using electron microscopic autoradiography. J Comp Neurol 360(1):17–32
Ono M, Ito T (2015) Functional organization of the mammalian auditory midbrain. J Physiol Sci
Ono M, Yanagawa Y, Koyano K (2005) GABAergic neurons in inferior colliculus of the GAD67-GFP knock-in mouse: electrophysiological and morphological properties. Neurosci Res 51(4):475–492
Peruzzi D, Bartlett E, Smith PH, Oliver DL (1997) A monosynaptic GABAergic input from the inferior colliculus to the medial geniculate body in rat. J Neurosci 17(10):3766–3777
Poon PW, Chen X, Cheung YM (1992) Differences in FM response correlate with morphology of neurons in the rat inferior colliculus. Exp Brain Res 91(1):94–104
Roger M, Arnault P (1989) Anatomical study of the connections of the primary auditory area in the rat. J Comp Neurol 287(3):339–356
Rothschild G, Nelken I, Mizrahi A (2010) Functional organization and population dynamics in the mouse primary auditory cortex. Nat Neurosci 13(3):353–360
Saint Marie RL, Stanforth DA, Jubelier EM (1997) Substrate for rapid feedforward inhibition of the auditory forebrain. Brain Res 765(1):173–176
Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17(15):5858–5867
Shi CJ, Cassell MD (1997) Cortical, thalamic, and amygdaloid projections of rat temporal cortex. J Comp Neurol 382(2):153–175
Sivaramakrishnan S, Oliver DL (2001) Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. J Neurosci 21(8):2861–2877
Spirou GA, Rager J, Manis PB (2005) Convergence of auditory-nerve fiber projections onto globular bushy cells. Neuroscience 136(3):843–863
Sturm J, Nguyen T, Kandler K (2014) Development of intrinsic connectivity in the central nucleus of the mouse inferior colliculus. J Neurosci 34(45):15032–15046
Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467(1):60–79
Vater M, Kossl M, Horn AK (1992) GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats. J Comp Neurol 325(2):183–206
Wallace MN, Shackleton TM, Palmer AR (2012) Morphological and physiological characteristics of laminar cells in the central nucleus of the inferior colliculus. Front Neural Circuits 6:55
Whitley JM, Henkel CK (1984) Topographical organization of the inferior collicular projection and other connections of the ventral nucleus of the lateral lemniscus in the cat. J Comp Neurol 229(2):257–270
Winer JA (2005) Three systems of descending projections to the inferior colliculus. In: Winer JA, Schreiner CE (eds) The inferior colliculus. Springer, New York, pp 231–247
Winer JA, Larue DT (1996) Evolution of GABAergic circuitry in the mammalian medial geniculate body. Proc Natl Acad Sci U S A 93(7):3083–3087
Winer JA, Saint Marie RL, Larue DT, Oliver DL (1996) GABAergic feedforward projections from the inferior colliculus to the medial geniculate body. Proc Natl Acad Sci U S A 93(15):8005–8010
Xiong XR, Liang F, Zingg B, Ji XY, Ibrahim LA, Tao HW, Zhang LI (2015) Auditory cortex controls sound-driven innate defense behaviour through corticofugal projections to inferior colliculus. Nat Commun 6:7224
Young ED, Oertel D (2004) Cochlear nucleus. In: Shepard GM (ed) The synaptic organization of the brain, 5th edn. Oxford University, Oxford, pp 125–163
Acknowledgments
Most of this study is based on long-term collaboration with many people in the Department of Anatomy, University of Fukui (Professor Satoshi Iino), Department of Morphological Brain Science, Kyoto University (Professor Takeshi Kaneko), and Department of Human and Artificial Intelligence Systems, University of Fukui (Professor Kazuyuki Murase and late Professor Hiroshi Ikeda). Authors are grateful to Professors Eric D. Young (Johns Hopkins University), Masahiko Takada (Kyoto University), Yuchio Yanagawa (Gunma University), and Hiroshi Riquimaroux (Doshisha University) for providing brain samples. This work was supported by grants from the Japan Society for the Promotion of Science (grant number 22700365 and 25430034, T.I.), the Uehara Memorial Foundation (T.I.), the Ichiro Kanehara Foundation (T.I.), NOVARTIS Foundation for the Promotion of Science (T.I.), Research and Education Program for Life Science of University of Fukui (T.I.), and NIH R01 DC00189 (D.L.O.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
Ito, T., Bishop, D.C. & Oliver, D.L. Functional organization of the local circuit in the inferior colliculus. Anat Sci Int 91, 22–34 (2016). https://doi.org/10.1007/s12565-015-0308-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12565-015-0308-8