Skip to main content
SpringerLink
Log in

The role of the inferior colliculus in a genetic model of audiogenic seizures

  • Review Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Previous studies have shown the functional importance of the inferior colliculus (IC) for the propagation and initiation of audiogenic seizures in several models of epilepsy in rats. A review of the cell types and cytoarchitecture of the IC, including its three major subdivisions, is presented. Significant increases in GABA levels and the number of GABAergic neurons are found in the central nucleus of the IC (ICCN) of genetically epilepsy-prone rats (GEPR-9s) as compared to Sprague-Dawley rats that do not display audiogenic seizures. Two independent anatomical methods were used to determine the number of GABAergic neurons, immunocytochemistry and in situ hybridization. In both types of preparation, the labeled cells in the ICCN appeared to be of different sizes but the number of small cells with diameters less than 15 μm showed the greatest increase. Nisslstained sections showed that the total number of neurons in the ICCN was increased in GEPR-9s and indicated that the increase in GABAergic neurons was not due to a change in the phenotype of collicular neurons from non-GABAergic to GABAergic. The number of small neurons in Nissl-stained sections of the ICCN was shown to correlate with seizure severity in the offspring of crosses made between Sprague-Dawley rats and GEPR-9s. Furthermore, the GEPR-3s that display moderate seizures showed a significant increase in the number of small neurons in the ICCN, and the magnitude of this increase was predicted from this correlation. Finally, the use of knife cuts through the midbrain indicated that the ICCN sends an important projection to the external nucleus and that this projection plays a vital role in the propagation of seizure activity from the site of seizure initiation in the ICCN. It remains to be resolved how the increase in small GABAergic neurons in the ICCN is responsible for the known pharmacological defects observed at GABAergic synapses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams JC (1979) Ascending projections to the inferior colliculus. J Comp Neurol 183:519–538

    Google Scholar 

  • Adams JC (1980) Crossed and descending projections to the inferior colliculus. Neurosci Lett 19:1–5

    Google Scholar 

  • Aitkin LM, Boyd J (1975) Responses of single units in cerebellar vermis of the cat of monoaural and binaural stimuli. J Neurophysiol 38:418–429

    Google Scholar 

  • Aitkin LM, Phillips SC (1984) The interconnections of the inferior colliculi through their commissure. J Comp Neurol 228:210–216

    Google Scholar 

  • Aitkin LM, Dickhaus H, Schult W, Zimmermann M (1978) External nucleus of inferior colliculus: auditory and spinal somatosensory afferents and their interactions. J Neurophysiol 41:837–847

    Google Scholar 

  • Aitkin LM, Kenyon CE, Philpott P (1981) The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus. J Comp Neurol 196:25–40

    Google Scholar 

  • Aitkin LM, Irvine DRF, Webster WR (1984) Central neural mechanisms of hearing. In: Brookhart JM, Mountcastle UB, Dariansmith I, Geiger SR (eds) Handbook of physiology — the nervous system. American Physiological Society, Bethesda, pp 675–737

    Google Scholar 

  • Brecha NC, Weigmann C (1994) Expression of GAT-1, a high affinity gamma-aminobutyric acid plasma membrane transporter in the rat retina. J Comp Neurol 345:60

    Google Scholar 

  • Browning RA (1986) Neuroanatomical localization of structures responsible for seizures in the GEPR: lesion studies. Life Sci 39:857–867

    Google Scholar 

  • Browning RA, Nelson DK, Mogharreban N, Jobe PC, Laird II HE (1985) Effect of midbrain and pontine tegmental lesions on audiogenic seizures in genetically epilepsy-prone rats. Epilepsia 26:175–183

    Google Scholar 

  • Browning RA, Lanker ML, Faingold CL (1989a) Injections of noradrenergic and GABAergic agonists into the inferior colliculus: effects on audiogenic seizures in genetically epilepsyprone rats. Epilepsy Res 4:119–125

    Google Scholar 

  • Browning RA, Wade DR, Marcinczyk M, Long GL, Jobe PC (1989b) Regional brain abnormalities in norepinephrine uptake and dopamine β-hydroxylase activity in the genetically epilepsy-prone rat. J Pharmacol Exp Therap 249:229–235

    Google Scholar 

  • Buckmaster PS, Schwartzkroin PA (1994) Hyperexcitability in the dentate gyrus of the epileptic Mongolian gerbil. Epilepsy Res 18:23–28

    Google Scholar 

  • Cajal SR y (1911) Histologie du Système Nerveux de l'Homme et des Vertébrés, vol 2. Paris

  • Carey CL, Webster DB (1971) Ascending and descending projections of the inferior colliculus in the kangaroo rat (Dipodomys merriami). Brain Behav Evol 4:401–412

    Google Scholar 

  • Chakravarty DN, Faingold CL, Terry WJ, Naritoku DK (1993) Audiogenic seizures in the genetically epilepsy-prone rat induce c-fos proto-oncogene expression in the inferior colliculus and periaqueductal gray. Soc Neurosci Abstr 19:605

    Google Scholar 

  • Chapman AG, Faingold CL, Hart GP, Bowker HM, Meldrum BS (1986) Brain regional amino acid levels in seizure-susceptible rats: changes related to sound-induced seizures. Neurochem Int 8:273–279

    Google Scholar 

  • Chocholova L (1962) The role of the cerebral cortex in audiogenic seizure in the rat. Physiol Bohemoslov 11:452–463

    Google Scholar 

  • Coleman JR, Clerici WJ (1987) Sources of projections to subdivisions of the inferior colliculus in the rat. J Comp Neurol 262:215–226

    Google Scholar 

  • Dailey JW, Reigel CE, Mishra PK, Jobe PC (1989) Neurobiology of seizure predisposition in the genetically epilepsy-prone rat. Epilepsy Res 3:3–17

    Google Scholar 

  • Dailey JW, Lasley SM, Burger RL, Bettendorf AF, Mishra PK, Jobe PC (1991a) Amino acids, monoamines and audiogenic seizures in genetically epilepsy-prone rats: effects of aspartamine. Epilepsy Res 8:122–133

    Google Scholar 

  • Dailey JW, Mishra PK, Ko KH, Penny JE, Jobe PC (1991b) Noradenergic abnormalities in the central nervous system of seizurenaive genetically epilepsy-prone rats. Epilepsia 32:168–173

    Google Scholar 

  • Dailey JW, Mishra PK, Ko KH, Penny JE, Jobe PC (1992) Serotoninergic abnormalities in the central nervous system of seizurenaive genetically epilepsy-prone rats. Life Sci 50:319–326

    Google Scholar 

  • Druga R, Syka J (1984a) Ascending and descending projections to the inferior colliculus of the rat. Physiol Bohemoslov 33:31–42

    Google Scholar 

  • Druga R, Syka J (1984b) Neocortical projections to the inferior colliculus in the rat: an experimental study using anterograde degeneration techniques. Physiol Bohemoslov 33:251–254

    Google Scholar 

  • Duplisse BR (1976) Mechanism of susceptibility of rats to AGS. Doctoral dissertation, University of Arizona, Tucson, USA

    Google Scholar 

  • Edwards SB, Ginsburgh CL, Henkel CK, Stein BE (1979) Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184:309–330

    Google Scholar 

  • Faingold CL, Naritoku DK (1992) The genetically epilepsy-prone rat: neuronal networks and actions of amino acid neurotransmitters. In: Faingold CL, Fromm GH (eds) Drugs for control of epilepsy: actions on neuronal networks involved in seizure disorders. CRC Press, Boca Raton, Florida, pp 277–308

    Google Scholar 

  • Faingold CL, Gehlbach GT, Caspary DM (1986a) Decreased effectiveness of GABA-mediated inhibition in the inferior colliculus of the genetically epilepsy-prone rat. Exp Neurol 93:145–159

    Google Scholar 

  • Faingold CL, Travis MA, Gehlbach G, Hoffmann WE, Jobe PC, Laird II HE, Caspary DM (1986b) Neuronal response abnormalities in the inferior colliculus of the genetically epilepsyprone rat. Electroencephalogr Clin Neurophysiol 63:296–305

    Google Scholar 

  • Faingold CL, Millan MH, Boersma CA, Meldrum BS (1988) Excitant amino acids and audiogenic seizures in the genetically epilepsy-prone rat. I. Afferent seizure initiation pathway. Exp Neurol 99:678–686

    Google Scholar 

  • Faingold CL, Walsh EJ, Maxwell JK, Randall ME (1990) Audiogenic seizure severity and hearing deficits in the genetically epilepsy-prone rat. Exp Neurol 108:55–60

    Google Scholar 

  • Faingold CL, Naritoku DK, Copley CA, Randall ME, Riaz A, Boersma, Anderson CA, Arneric SP (1992) Glutamate in the inferior colliculus plays a critical role in audiogenic seizure initiation. Epilepsy Res 13:95–105

    Google Scholar 

  • Faingold CL, Marcinczyk MJ, Casebeer DJ, Randall ME, Arneric SP, Browning RA (1994a) GABA in the inferior colliculus plays a critical role in control of audiogenic seizures. Brain Res 640:40–47

    Google Scholar 

  • Faingold CL, Randall ME, Boersma Anderson CA (1994b) Blockade of GABA uptake with tiagabine inhibits audiogenic seizures and reduces neuronal firing in the inferior colliculus of the genetically epilepsy-prone rat. Exp Neurol 126:225–232

    Google Scholar 

  • Farias PA, Low SQ, Peterson GM, Ribak CE (1992) Morphological evidence for altered synaptic organization and structure in the hippocampal formation of seizure-sensitive gerbils. Hippocampus 2:229–246

    Google Scholar 

  • Faye-Lund H, Osen KK (1985) Anatomy of the inferior colliculus in rat. Anat Embryol 171:1–20

    Google Scholar 

  • Fitzpatrick KA (1975) Cellular architecture and topographic organization of the inferior colliculus of the squirrel monkey. J Comp Neurol 164:185–208

    Google Scholar 

  • Friauf E, Kandler K (1990) Auditory projections to the inferior colliculus of the rat are present by birth. Neurosci Lett 120:58–61

    Google Scholar 

  • Geneic P, Morest DK (1971) The neuronal architecture of the human posterior colliculus. Acta Otolaryngol 295:1–33

    Google Scholar 

  • González-Hernández TH, Meyer G, Ferres-Torres R, Castañeyra-Perdomo A, Pérez-Delgado MM (1987) Afferent connections of the inferior colliculus in the albino mouse. J Hirnforsch 28:315–324

    Google Scholar 

  • González-Hernández TH, Galindo-Mireles D, Castañeyra-Perdomo A, Ferres-Torres R (1991) Divergent projections of projecting neurons of the inferior colliculus to the medial geniculate body and the contralateral inferior colliculus in the rat. Hearing Res 52:17–22

    Google Scholar 

  • Harrison JM (1978) Functional properties of the auditory system of the brainstem. In: Masterton RB (ed) Handbook of behavioral neurobiology. Plenum Press, New York, pp 409–458

    Google Scholar 

  • Hjeresen DL, Franck JE, Amend DL (1987) Ontogeny of seizure incidence, latency, and severity in genetically epilepsy-prone rats. Dev Psychobiol 20:355–363

    Google Scholar 

  • Holmes GL, Thompson JL, Marchi TA, Gabriel PS, Hogan MA, Carl FG, Feldman DS (1990) Effects of seizures on learning, memory, and behavior in the genetically epilepsy-prone rat. Ann Neurol 27:24–32

    Google Scholar 

  • Itaya SK, Hoesen GW van (1982) Retinal innervation of the inferior colliculus in rat and monkey. Brain Res 233:45–52

    Google Scholar 

  • Jobe PC, Brown RD (1980) Auditory pharmacology. Trends Pharmacol Sci 1:202–206

    Google Scholar 

  • Jobe PC, Laird HE (1981) Neurotransmitter abnormalities as determinants of seizure susceptibility and intensity in the genetic models of epilepsy. Biochem Pharmacol 30:3137–3144

    Google Scholar 

  • Jobe PC, Picchioni AL, Chin L (1973a) Role of brain norepinephrine in audiogenic seizure in the rat. J Pharmacol Exp Ther 184:1–10

    Google Scholar 

  • Jobe PC, Picchioni AL, Chin L (1973b) Role of brain 5-hydroxytryptamine in audiogenic seizures in the rat. Life Sci 13:1–13

    Google Scholar 

  • Jobe PC, Dailey JW, Brown RD (1981) Effect of Ro-4-12284 on audiogenic seizure susceptibility and intensity in epilepsyprone rats. Life Sci 28:2031–2038

    Google Scholar 

  • Jobe PC, Laird II HE, Ko KH, Ray R, Dailey JW (1982) Abnormalities in monoamine levels in the central nervous system of the genetically epilepsy prone rat. Epilepsia 23:359–366

    Google Scholar 

  • Jobe PC, Ko KH, Dailey JW (1984) Abnormalities in norepinephrine turnover rate in the central nervous system of the genetically epilepsy-prone rat. Brain Res 290:357–360

    Google Scholar 

  • Jobe PC, Dailey JW, Reigel CE (1986) Noradrenergic and serotonergic determinants of seizure susceptibility and severity in genetically epilepsy-prone rats Life Sci 39:775–782

    Google Scholar 

  • Kesner RP (1966) Subcortical mechanisms of audiogenic seizures in the rat. Exp Neurol 15:192–205

    Google Scholar 

  • Kudo M, Niimi K (1978) Ascending projections of the inferior colliculus onto the medial geniculate body in the cat studied by anterograde and retrograde tracing techniques. Brain Res 155:113–117

    Google Scholar 

  • Laird II HE (1974) 5-Hydroxytryptamine as an inhibitory modulator of audiogenic seizures. Doctoral dissertation, University of Arizona, Tuscon, USA

    Google Scholar 

  • Laird II HE, Chin L, Picchioni AL (1974) Enhancement of audiogenic seizure intensity by p-chloromethamphetamine. Proc West Pharmacol Soc 17:46–50

    Google Scholar 

  • Laird II HE, Dailey JW, Jobe PC (1984) Neurotransmitter abnormalities in genetically epilepsy-prone rodents. Fed Proc Fed Am Soc Exp Biol 43:2505–2509

    Google Scholar 

  • Lauterborn JC, Ribak CE (1989) Differences in dopamine β-hydroxylase immunoreactivity between the brains of genetically epilepsy-prone and Sprague-Dawley rats. Epilepsy Res 4:161–176

    Google Scholar 

  • LeDoux JE, Ruggiero DA, Reis DJ (1985) Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. J Comp Neurol 242:182–213

    Google Scholar 

  • Ludvig N, Moshé SL (1989) Different behavioral and electrographic effects of acoustic stimulation and dibutyryl cyclic AMP injection into the inferior colliculus in normal and in genetically epilepsy-prone rats. Epilepsy Res 3:185–190

    Google Scholar 

  • Mills SA, Savage DD (1988) Evidence of hypothyroidism in the genetically epilepsy-prone rat. Epilepsy Res 2:102–110

    Google Scholar 

  • Millan MH, Meldrum BS, Faingold CL (1986) Induction of audiogenic seizure susceptibility by focal infusion of excitant amino acid or bicuculline into the inferior colliculus of normal rats. Exp Neurol 91:634–639

    Google Scholar 

  • Millan MH, Meldrum BS, Boersma CA, Faingold CL (1988) Excitant amino acids and audiogenic seizures in the genetically epilepsy-prone rat. II. Efferent seizure propagating pathway. Exp Neurol 99:687–698

    Google Scholar 

  • Mishra PK, Dailey JW, Reigel CE, Tomsic ML, Jobe PC (1988) Sex-specific distinctions in audiogenic convulsions exhibited by severe seizure genetically epilepsy-prone rats (GEPR-9s). Epilepsy Res 2:309–316

    Google Scholar 

  • Mishra PK, Dailey JW, Reigel CE, Jobe PC (1989) Audiogenic convulsions in moderate seizure genetically epilepsy-prone rats (GEPR-3s). Epilepsy Res 3:191–198

    Google Scholar 

  • Moore JK, Moore RY (1987) Glutamic acid decarboxylase-like immunoreactivity in brainstem auditory nuclei of the rat. J Comp Neurol 260:157–174

    Google Scholar 

  • Moore RY, Goldberg JM (1963) Ascending projections of the inferior colliculus in the cat. J Comp Neurol 121:109–135

    Google Scholar 

  • 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 222:209–236

    Google Scholar 

  • Noort J van (1969) The structure and connections of the inferior colliculus. Van Gorcum, Assen

    Google Scholar 

  • Olazábal UE, Moore JK (1989) Nigrotectal projection to the inferior colliculus: horseradish peroxidase transport and tyrosine hydroxylase immunohistochemical studies in rats, cats and bats. J Comp Neurol 282:98–118

    Google Scholar 

  • Oliver DL, Morest DK (1984) The central nucleus of the inferior colliculus of the cat. J Comp Neurol 222:237–264

    Google Scholar 

  • Paloff AM, Usunoff KG, Hinova-Palova DV, Ivanov DP (1985) Retinal innervation of the inferior colliculus in adult cats: electron microscopic observations. Neurosci Lett 54:339–344

    Google Scholar 

  • Penny JE, Brown RD, Hodges KB, Kupetz SA, Glenn DW, Jobe PC (1983) Cochlear morphology of the audiogenic-seizure susceptible (AGS) or genetically epilepsy-prone rat (GEPR). Acta Otolaryngol 95:1–12

    Google Scholar 

  • Peterson GM, Ribak CE, Oertel WH (1985) A regional increase in the number of GABAergic neurons and terminals in the seizure-sensitive gerbil. Brain Res 340:384–389

    Google Scholar 

  • Reigel CE, Jobe PC, Dailey JW, Savage DD (1989) Ontogeny of sound-induced seizures in the genetically epilepsy-prone rat. Epilepsy Res 4:63–71

    Google Scholar 

  • Ribak CE (1991) Epilepsy and the cortex — anatomy. In: Peters A, Jones EG (eds) Cerebral cortex, vol 9. Plenum Press, New York, pp 427–483

    Google Scholar 

  • Ribak CE, Byun MY, Ruiz GT, Reiffenstein RJ (1988a) Increased levels of amino acid neurotransmitters in the inferior colliculus of the genetically epilepsy-prone rat. Epilepsy Res 2:9–13

    Google Scholar 

  • Ribak CE, Roberts RC, Byun MY, Kim HL (1988b) Anatomical and behavioral analyses of the inheritance of audiogenic seizures in the progeny of genetically epilepsy-prone and Sprague-Dawley rats. Epilepsy Res 2:345–355

    Google Scholar 

  • Ribak CE, Lauterborn JC, Navetta MS, Gall CM (1993) The inferior colliculus of GEPRs contains greater numbers of cells that express glutamate decarboxylase (GAD67) mRNA. Epilepsy Res 14:105–113

    Google Scholar 

  • Ribak CE, Khurana V, Lien NT (1994) The effect of midbrain collicular knife cuts on audiogenic seizure severity in the genetically epilepsy-prone rat. J Hirnforsch 35:303–311

    Google Scholar 

  • Roberts RC, Ribak CE (1987a) GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil. J Comp Neurol 258:267–280

    Google Scholar 

  • Roberts RC, Ribak CE (1987b) An electron microscopic study of GABAergic neurons and terminals in the central nucleus of the inferior colliculus of the rat. J Neurocytol 16:333–345

    Google Scholar 

  • Roberts RC, Ribak CE (1988) The ultrastructure of the central nucleus of the inferior colliculus of the genetically epilepsy-prone rat. Epilepsy Res 2:196–214

    Google Scholar 

  • Roberts RC, Kim HL, Ribak CE (1985a) Increased numbers of neurons occur in the inferior colliculus of the young genetically epilepsy-prone rat. Dev Brain Res 23:277–281

    Google Scholar 

  • Roberts RC, Ribak CE, Oertel WH (1985b) Increased numbers of GABAergic neurons occur in the inferior colliculus of an audiogenic model of genetic epilepsy. Brain Res 361:324–338

    Google Scholar 

  • Rockel AJ, Jones EG (1973a) The neuronal organization of the inferior colliculus of the adult cat. I. Central nucleus. J Comp Neurol 147:11–60

    Google Scholar 

  • Rockel AJ, Jones EG (1973b) Observations of the fine structure of the inferior colliculus of the cat. J Comp Neurol 147:61–92

    Google Scholar 

  • Ryugo DK, Killackey HP (1975) The neuronal organization and efferent connections of the inferior colliculus of the rat. Soc Neurosci Abstr 40:30

    Google Scholar 

  • Saldaña E, Merchán MA (1992) Intrinsic and commissural connections of the rat inferior colliculus. J Comp Neurol 319:417–437

    Google Scholar 

  • Schweizer H (1981) The connections of the inferior colliculus and the organization of the brainstem auditory system in the greater horseshoe bat (Rhinolophus ferrumequinum) J Comp Neurol 201:25–49

    Google Scholar 

  • Seeburg PH (1993) The molecular biology of mammalian glutamate receptor channels. Trends Neurosci 16:359–365

    Google Scholar 

  • Smith PH (1992) Anatomy and physiology of multipolar cells in the rat inferior collicular cortex using the in vitro brain slice technique. J Neurosci 12:3700–3715

    Google Scholar 

  • Thompson JL, Carl FG, Holmes GL (1991) Effects of age on seizure susceptibility in genetically epilepsy-prone rats (GEPR-9s). Epilepsia 32:161–167

    Google Scholar 

  • Tsutsui J, Terra VC, Oliveira JAC, Garcia-Cairasco N (1992) Neuroethological evaluation of audiogenic seizures and audiogenic-like seizures induced by microinjection of bicuculline into the inferior colliculus. I. Effects of midcollicular knife cuts. Behav Brain Res 52:7–17

    Google Scholar 

  • Wada JA, Terao A, White B, Jung E (1970) Inferior colliculus lesion and audiogenic seizure susceptibility. Exp Neurol 28:326–332

    Google Scholar 

  • Willard FH, Ryugo DK (1983) Anatomy of the central auditory system. In: Willott JF (ed) The auditory psychobiology of the mouse. Thomas, Springfield, pp 201–304

    Google Scholar 

  • Yasui Y, Kayahara T, Kuga Y, Nakano K (1990a) Direct projections from the globus pallidus to the inferior colliculus in the rat. Neurosci Lett 115:121–125

    Google Scholar 

  • Yasui Y, Kayahara T, Nakano K, Mizuno N (1990b) The subparafascicular thalamic nucleus of the rat receives projection fibers from the inferior colliculus and auditory cortex. Brain Res 537:323–327

    Google Scholar 

  • Zook JM, Casseday JH (1982) Origin of ascending projections to the inferior colliculus in the mustache bat, Pteronotus parnellii. J Comp Neurol 207:14–28

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Neurobiology, University of California, 92717, Irvine, CA, USA

    Charles E. Ribak & Catherine L. Morin

Authors
  1. Charles E. Ribak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Catherine L. Morin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ribak, C.E., Morin, C.L. The role of the inferior colliculus in a genetic model of audiogenic seizures. Anat Embryol 191, 279–295 (1995). https://doi.org/10.1007/BF00534681

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00534681

Key words

Search

Navigation