Abstract
The inferior colliculus (IC) is a well-established target of descending projections from the auditory cortex (AC). However, our understanding of these pathways has been limited by an incomplete picture of their functional influence within the three-dimensional space of the IC. Our goal was to study the properties and spatial representation of corticofugal input in the IC of guinea pigs with a high degree of spatial resolution. We systematically mapped neural activity in the IC using two types of silicon substrate probes that allow for simultaneous recording at multiple neural sites. One probe provided a high resolution in the dorsal-ventral plane and the other provided spatial resolution in the medial-lateral plane. Electrical stimulation of the ipsilateral AC produced excitatory responses in the IC with thresholds usually below 5–10 µA. First spike latencies were predominantly in the 6–20 ms range, although latencies from 3–5 ms were also observed. Broadly distributed unimodal spike patterns with modal latencies greater than 30 ms were occasionally seen. The excitatory responses to cortical stimulation were mostly unimodal and occasionally bimodal with a wide range of spike distribution patterns and response durations. Excitation was often followed by suppression of spontaneous activity. Suppression of acoustic responses was observed even when there was little or no response to electrical stimulation, suggesting spatial-temporal integration. A few of the responding neurons showed purely inhibitory responses to electrical stimulation, suggesting that there are disynaptic routes of corticocollicular inhibition. Detailed spatial mapping revealed that the response patterns and their durations had a characteristic spatial distribution in the IC.
Similar content being viewed by others
References
Aitkin LM (1986) The auditory midbrain. Structure and function in the central auditory pathway. Humana Press, Clifton, NJ
Andersen RA, Snyder RL, Merzenich MM (1980) The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII and anterior auditory cortical fields of the cat. J Comp Neurol 191:479–494
Beyerl BD (1978) Afferent projections to the central nucleus of the inferior colliculus in the rat. Brain Res 145:209–223
Bledsoe SC Jr, Nagase S, Miller JM, Altschuler RA (1995) Deafness-induced plasticity in the mature central auditory system. Neuroreport 7:225–229
Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (1995) Gamma (40Hz-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47–60
Bragin A, Hetke J, Wilson CL, Anderson DJ, Engel Jr J, Buzsaki G (2000) Multiple site silicon-based probes for chronic recordings in freely moving rats: implantation, recording and histological verification. J Neurosci Meth 98:77–82
Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat. J Comp Neurol 197:705–722
Chen J, Wise KD, Hetke JF, Bledsoe SC Jr (1997) A multichannel neural probe for selective chemical delivery at the cellular level. IEEE Trans Biomed Eng 44:760–769
Druga R, Syka J (1984) Ascending and descending projections to the inferior colliculus in the rat. Physiol Bohemoslov 33:31–42
Druga R, Syka J, Rajkowska G (1997) Projections of auditory cortex onto the inferior colliculus in the rat. Physiol Res 46:215–222
Feliciano M, Potashner SJ (1995) Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus. J Neurochem 65:1348–1357
Fitzpatrick KA, Imig TA (1978) Projections of auditory cortex upon the thalamus and midbrain in the owl monkey. J Comp Neurol 177:537–556
Gao E, Suga N (1998) Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc Natl Acad Sci USA 95:12663–12670
Gao E, Suga N (2000) Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proc Natl Acad Sci USA 97:8081–8086
Harris KD, Henze DA, Csicsvari J, Hirase H, Buzaki G (2000) Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J Neurophysiol 84:401–414
Hoogerwerf AC, Wise KD (1994) A three-dimensional microelectrode array for chronic neural recording. IEEE Trans Biomed Engr 41:1136–1146
Huffman RF, Henson OW Jr (1990) The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus. Brain Res Rev 15:295–323
Jane JA, Masterton RB, Diamond IT (1965) The function of the tectum for attention to auditory stimuli in the cat. J Comp Neurol 125:165–191
Jen PH, Chen QC, Sun XD (1998) Corticofugal regulation of auditory sensitivity in the bat inferior colliculus. J Comp Physiol A 183:683–697
Ji J, Wise KD (1992) An implantable CMOS circuit interface for multiplexed microelectrode recording arrays. IEEE J Solid-State Circuits 27:433–443
Kelly JP, Wong D (1981) Laminar connections of the cat’s auditory cortex. Brain Res 212:1–15
Klinke R, Kral A, Heid S, Tillein J, Hartmann R (1999) Recruitment of the auditory cortex in congenitally deaf cats by long-term cochlear electrostimulation. Science 285:1729–1733
Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2002) Hearing after congenital deafness: a central auditory plasticity and sensory deprivation. Cereb Cortex 12:797–807
Langner G, Wallhauser-Franke E (1999) Computer simulation of a tinnitus model based on labelling of tinnitus activity in the auditory cortex. In: Hazell JWP (ed) Proceedings of the 6th International Tinnitus Seminar. Hawthorn, Harleston, pp 132–135
Ma X, Suga N (2001a) Plasticity of bat’s central auditory system evoked by focal electric stimulation of auditory and/or somatosensory cortices. J Neurophysiol 85:1078–1087
Ma X, Suga N (2001b) Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats. Proc Natl Acad Sci USA 98:14060–14065
Mensinger AF, Anderson DJ, Buchko CJ, Johnson MA, Martin DC, Tresco PA, Silver RB, Highstein SM (2000) Chronic recording of regenerating VIIIth nerve axons with a sieve electrode. J Neurophysiol 83:611–615
Muhlnickel W, Elbert T, Taub E, Flor H (1998) Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci USA 95:10340–10343
Najafi K, Wise KD, Mochizuki T (1985) A high-yield IC-compatible multichannel recording array. IEEE Trans Electron Devices 32:1206–1211
Oliver DL, Winer JA, Beckius GE, Saint Marie RL (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat. J Comp Neurol 340:27–42
Redies H, Sieben U, Creutzfeldt OD (1989) Functional subdivisions in the auditory cortex of the guinea pig. J Comp Neurol 282:473–488
Saldana E, Feliciano M, Mugnaini E (1996) Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J Comp Neurol 371:15–40
Sakai M, Suga N (2001) Plasticity of cochleotopic (frequency) map in specialized and nonspecialized auditory cortex. Proc Natl Acad Sci USA 98:3507–3512
Shneiderman A, Oliver DL, Henkel CK (1988) Connections of the dorsal nucleus of the lateral lemniscus: an inhibitory parallel pathway in the ascending auditory system? J Comp Neurol 276:188–208
Suga N, Gao E, Zhang Y, Ma X, Olsen JF (2000) The corticofugal system for hearing: recent progress. Proc Natl Acad Sci USA 97:11807–11814
Sun X, Jen PHS, Sun D, Zhang S (1989) Corticofugal influences on the responses of bat inferior collicular neurons to sound stimulation. Brain Res 495:1–8
Syka J (2002) Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. Physiol Rev 82:601–636
Syka J, Popelar J (1984) Inferior colliculus in the rat: neuronal responses to stimulation of the auditory cortex. Neurosci Letters, 51:235–240.
Syka J, Popelar J, Druga R, Vlkova A (1988) Descending central auditory pathway- structure and function. In: Syka J, Masterton RB (eds) Auditory pathway, structure and function. Plenum Press, New York, pp 279–292
Torterolo P, Zurita P, Pedemonte M, Vellut RA (1998) Auditory cortical efferent actions upon inferior colliculus unitary activity in the guinea pig. Neurosci Letters 249:172–176
Winer JA, Larue DT, Diehl JJ, Hefti BJ (1998) Auditory cortical projections to the cat inferior colliculus. J Comp Neurol 400:147–174
Winer JA, Chernock ML, Larue DT, Cheung SW (2002) Descending projections to the inferior colliculus from the posterior thalamus and the auditory cortex in rat, cat, and monkey. Hear Res 168:181–195
Yan J, Ehret G (2001) Corticofugal reorganization of the midbrain tonotopic map in mice. Neuroreport 2:3313–3316
Yan J, Ehret G (2002) Corticofugal modulation of midbrain sound processing in the house mouse. Eur J Neurosci 16:119–128
Yan J, Suga N (1996) Corticofugal modulation of time-domain processing of biosonar information in bats. Science 273:1100–1103
Yan J, Suga N (1999) Corticofugal amplification of facilitative auditory responses of subcortical combination-sensitive neurons in the mustached bat. J Neurophysiol 81:817–824
Yan W, Suga N (1998) Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat Neurosci 1:54–58
Zhang Y, Suga N (1997) Corticofugal amplification of subcortical responses to single-tone stimuli in the mustached bat. J Neurophysiol 78:3489–3492
Zhang Y, Suga N (2000) Modulation of responses and frequency tuning of thalamic and collicular neurons by cortical activation in mustached bats. J Neurophysiol 84:325–333
Zhang Y, Suga N, Yan J (1997) Corticofugal modulation of frequency processing in the bat auditory system. Nature 387:900–903
Zhou X, Jen PHS (2000) Corticofugal inhibition compresses all types of rate-intensity functions of inferior collicular neurons in the big brown bat. Brain Res 881:62–68
Acknowledgements
We are grateful to Sufen Shang for skilled technical assistance and data processing and to Chris Ellinger for invaluable electronic support. The Center for Neural Communication Technology (CNCT) in the Department of Electrical Engineering and Computer Science supplied the multichannel electrodes used in this study. This work was supported by National Institutes of Health grants NIH-NIDCD DC00078, NIH-NIBIB EB00308 and NIH-NCRR RR09754.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bledsoe, S.C., Shore, S.E. & Guitton, M.J. Spatial representation of corticofugal input in the inferior colliculus: a multicontact silicon probe approach. Exp Brain Res 153, 530–542 (2003). https://doi.org/10.1007/s00221-003-1671-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-003-1671-6