Skip to main content
SpringerLink
Log in

Absence of cross-modal reorganization in the primary auditory cortex of congenitally deaf cats

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

To investigate possible cross-modal reorganization of the primary auditory cortex (field A1) in congenitally deaf cats, after years of auditory deprivation, multiunit activity and local field potentials were recorded in lightly anesthetized animals and compared with responses obtained in hearing cats. Local field potentials were also used for current source-density analyses. For visual stimulation, phase-reversal gratings of three to five different spatial frequencies and three to five different orientations were presented at the point of central vision. Peripheral visual field was tested using hand-held stimuli (light bar-shaped stimulus of different orientations, moved in different directions and flashed) typically used for neurophysiological characterization of visual fields. From 200 multiunit recordings, no response to visual stimuli could be found in A1 of any of the investigated animals. Using the current source-density analysis of local field potentials, no local generators of field potentials could be found within A1, despite of the presence of small local field potentials. No multiunit responses to somatosensory stimulation (whiskers, face, pinna, head, neck, all paws, back, tail) could be obtained. In conclusion, there were no indications for a cross-modal reorganization (visual, somatosensory) of area A1 in congenitally deaf cats.

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

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

Notes

  1. "Deaf" refers to "congenitally deaf" throughout the manuscript

References

  • Aitkin LM, Dickhaus H, Schult W, Zimmermann M (1978) External nucleus of the 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 

  • Bavelier D, Neville HJ (2002) Cross-modal plasticity: where and how? Nat Rev Neurosci 3:443–452

    CAS  PubMed  Google Scholar 

  • Bavelier D, Tomann A, Hutton C et al. (2000) Visual attention to the periphery is enhanced in congenitally deaf individuals (abstract). J Neurosci 20:93

    Google Scholar 

  • Bernstein LE, Auer ET Jr, Moore JK et al. (2002) Visual speech perception without A1 activation. Neuroreport 13:311–315

    PubMed  Google Scholar 

  • Blakemore C, Zumbroich TJ (1987) Stimulus selectivity and functional organization in the lateral suprasylvian visual cortex of the cat. J Physiol (Lond) 389:569–603

    Google Scholar 

  • Brechmann A, Baumgart F, Scheich H (2002) Sound-level-dependent representation of frequency modulations in human auditory cortex: a low-noise fMRI study. J Neurophysiol 87:423–433

    PubMed  Google Scholar 

  • Bronchti G, Heil P, Sadka R, Hess A, Scheich H, Wollberg Z (2002) Auditory activation of "visual" cortical areas in the blind mole rat (Spalax ehrenbergi) Eur J Neurosci 16:311–29

    Google Scholar 

  • Büchel C, Price C, Frackowiak RS, Friston K (1998) Different activation patterns in the visual cortex of late and congenitally blind subjects. Brain 121:409–419

    Article  PubMed  Google Scholar 

  • Clarke S, Innocenti GM (1986) Organization of immature intrahemispheric connections. J Comp Neurol 251:1-22

    CAS  PubMed  Google Scholar 

  • Cohen LG, Weeks RA, Sadato N et al. (1999) Period of susceptibility for cross-modal plasticity in the blind. Ann Neurol 45:451–460

    CAS  PubMed  Google Scholar 

  • Diamond DM, Weinberger NM (1984) Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response. II. Secondary field (AII). Behav Neurosci 98:189–210

    Article  CAS  PubMed  Google Scholar 

  • Dreher B, Wang C, Turlejski KJ, Djavadian RL, Burke W (1996) Areas PMLS and 21a of cat visual cortex: two functionally distinct areas. Cereb Cortex 6:585–599

    CAS  PubMed  Google Scholar 

  • Eggermont JJ, Ponton CW, Don M, Waring MD, Kwong B (1997) Maturational delays in cortical evoked potentials in cochlear implant users. Acta Otolaryngol 117:161–163

    CAS  PubMed  Google Scholar 

  • Finney EM, Fine I, Dobkins KR (2001) Visual stimuli activate auditory cortex in the deaf. Nat Neurosci 4:1171–1173

    Article  CAS  PubMed  Google Scholar 

  • Gao W, Pallas SL (1999) Cross-modal reorganization of horizontal connectivity in auditory cortex without altering thalamocortical projections. J Neurosci 19:7940–7950

    CAS  PubMed  Google Scholar 

  • Giraud AL, Price CJ, Graham JM, Frackowiak RS (2001a) Functional plasticity of language-related brain areas after cochlear implantation. Brain 124:1307–1316

    Article  CAS  PubMed  Google Scholar 

  • Giraud A, Price CJ, Graham JM, Truy E, Frackowiak RS (2001b) Cross-modal plasticity underpins language recovery after cochlear implantation. Neuron 30:657–663

    Article  CAS  PubMed  Google Scholar 

  • Giraud AL, Truy E, Frackowiak R (2001c) Imaging plasticity in cochlear implant patients. Audiol Neurootol 6:381–393

    Article  CAS  PubMed  Google Scholar 

  • Hartmann R, Shepherd RK, Heid S, Klinke R (1997) Response of the A1 to electrical stimulation of the auditory nerve in the congenitally deaf white cat. Hear Res 112:115–133

    Article  CAS  PubMed  Google Scholar 

  • Heid S, Hartmann R, Klinke R (1998) A model for prelingual deafness, the congenitally deaf white cat—population statistics and degenerative changes. Hear Res 115:101–112

    Article  CAS  PubMed  Google Scholar 

  • Heil P, Bronchti G, Wollberg Z, Scheich H (1991) Invasion of visual cortex by the auditory system in the naturally blind mole rat. Neuroreport 2:735–738

    CAS  PubMed  Google Scholar 

  • Herbert DA, Mitchell RA (1971) Blood gas tensions and acid-base balance in awake cats. J Appl Physiol 30:434–436

    CAS  PubMed  Google Scholar 

  • Innocenti GM, Clarke S (1984) Bilateral transitory projection to visual areas from auditory cortex in kittens. Brain Res 316:143–148

    CAS  PubMed  Google Scholar 

  • Izraeli R, Koay G, Lamish M et al. (2002) Cross-modal neuroplasticity in neonatally enucleated hamsters: structure, electrophysiology and behaviour. Eur J Neurosci 15:693–712

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Korte M, Rauschecker JP (1993) Auditory spatial tuning of cortical neurons is sharpened in cats with early blindness. J Neurophysiol 70:1717–1721

    CAS  PubMed  Google Scholar 

  • Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2000) Congenital auditory deprivation reduces synaptic activity within the auditory cortex in a layer-specific manner. Cereb Cortex 10:714–726

    Article  CAS  PubMed  Google Scholar 

  • Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2001) Delayed maturation and sensitive periods in the auditory cortex. Audiol Neurootol 6:346–362

    Article  CAS  PubMed  Google Scholar 

  • Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2002) Hearing after congenital deafness: central auditory plasticity and sensory deprivation. Cereb Cortex 12:797–807

    Article  CAS  PubMed  Google Scholar 

  • Lee DS, Lee JS, Oh SH et al. (2001) Cross-modal plasticity and cochlear implants. Nature 409:149–150

    Article  CAS  Google Scholar 

  • Levanen S, Jousmaki V, Hari R (1998) Vibration-induced auditory-cortex activation in a congenitally deaf adult. Curr Biol 8:869–872

    CAS  PubMed  Google Scholar 

  • Melchner L von, Pallas SL, Sur M (2000) Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404:871–876

    Google Scholar 

  • Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37–100

    CAS  PubMed  Google Scholar 

  • Neville HJ (1990) Intermodal competition and compensation in development. Evidence from studies of the visual system in congenitally deaf adults. Ann NY Acad Sci 608:71–87

    CAS  PubMed  Google Scholar 

  • Nicolelis MA, Chapin JK, Lin RC (1991) Neonatal whisker removal in rats stabilizes a transient projection from the auditory thalamus to the primary somatosensory cortex. Brain Res 567:133–139

    Article  CAS  PubMed  Google Scholar 

  • Nishimura H, Hashikawa K, Doi K et al. (1999) Sign language "heard" in the auditory cortex. Nature 397:116

    Article  CAS  PubMed  Google Scholar 

  • Penhune VB, Zatorre RJ, Macdonald JD, Evans AC (1996) Interhemispheric anatomical differences in human A1: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex 6:661–672

    CAS  PubMed  Google Scholar 

  • Petitto LA, Zatorre RJ, Gauna K et al. (2000) Speech-like cerebral activity in profoundly deaf people processing signed languages: implications for the neural basis of human language. Proc Natl Acad Sci USA 97:13961–13966

    Article  CAS  PubMed  Google Scholar 

  • Ponton CW, Eggermont JJ (2001) Of kittens and kids: altered cortical maturation following profound deafness and cochlear implant use. Audiol Neurootol 6:363–380

    Article  CAS  PubMed  Google Scholar 

  • Proksch J, Bavelier D (2002) Changes in the spatial distribution of visual attention after early deafness. J Cogn Neurosci 14:687–701

    Article  PubMed  Google Scholar 

  • Rauschecker JP, Korte M (1993) Auditory compensation for early blindness in cat cerebral cortex. J Neurosci 13:4538–4548

    CAS  PubMed  Google Scholar 

  • Reale RA, Imig TJ (1980) Tonotopic organization in auditory cortex of the cat. J Comp Neurol 192:265–291

    CAS  PubMed  Google Scholar 

  • Rebillard G, Rebillard M, Carlier E, Pujol R (1976) Histo-physiological relationships in the deaf white cat auditory system. Acta Otolaryngol 82:48–56

    CAS  PubMed  Google Scholar 

  • Rebillard G, Carlier E, Rebillard M, Pujol R (1977) Enhancement of visual responses on the A1 of the cat after an early destruction of cochlear receptors. Brain Res 129:162–164

    Article  CAS  PubMed  Google Scholar 

  • Rebillard G, Rebillard M, Pujol R (1980) Factors affecting the recording of visual-evoked potentials from the deaf cat A1. Brain Res 188:252–254

    Article  CAS  PubMed  Google Scholar 

  • Robards MJ (1979) Somatic neurons in the brainstem and neocortex projecting to the external nucleus of the inferior colliculus: an anatomical study on the opossum. J Comp Neurol 184:547–566

    CAS  PubMed  Google Scholar 

  • Röder B, Teder-Salejarvi W, Sterr A et al. (1999a) Improved auditory spatial tuning in blind humans. Nature 400:162–166

    PubMed  Google Scholar 

  • Röder B, Rösler F, Neville HJ (1999b) Effects of interstimulus interval on auditory event-related potentials in congenitally blind and normally sighted humans. Neurosci Lett 264:53–56

    Article  PubMed  Google Scholar 

  • Röder B, Rösler F, Neville HJ (2000) Event-related potentials during auditory language processing in congenitally blind and sighted people. Neuropsychologia 38:1482–1502

    Article  PubMed  Google Scholar 

  • Röder B, Rösler F, Neville HJ (2001) Auditory memory in congenitally blind adults: a behavioral–electrophysiological investigation. Brain Res Cogn Brain Res 11:289–303

    PubMed  Google Scholar 

  • Ryugo DK, Rosenbaum BT, Kim PJ, Niparko JK, Saada AA (1998) Single unit recordings in the auditory nerve of congenitally deaf white cats: morphological correlates in the cochlea and cochlear nucleus. J Comp Neurol 397:532–548

    Article  CAS  PubMed  Google Scholar 

  • Sadato N, Pascual-Leone A, Grafman J et al. (1996) Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380:526–528

    CAS  PubMed  Google Scholar 

  • Schroeder CE, Lindsley RW, Specht C et al. (2001) Somatosensory input to auditory association cortex in the macaque monkey. J Neurophysiol 85:1322–1327

    CAS  PubMed  Google Scholar 

  • Sharma A, Dorman M, Spahr A, Todd NW (2002) Early cochlear implantation in children allows normal development of central auditory pathways. Ann Otol Rhinol Laryngol (Suppl) 189:38–41

    Google Scholar 

  • Shore SE, Vass Z, Wys NL, Altschuler RA (2000) Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419:271–285

    CAS  PubMed  Google Scholar 

  • Spear PD (1991) Functions of extrastriate visual cortex in nonprimate species. In: CronlyDillon J (ed) Vision and visual dysfunction. (The neural basis of visual function, vol 4) Macmillan, Basingstoke, pp 339–369

  • Stewart DL, Starr A (1970) Absence of visually influenced cells in auditory cortex of normal and congenitally deaf cats. Exp Neurol 28:525–528

    CAS  PubMed  Google Scholar 

  • Weeks R, Horwitz B, Aziz-Sultan A et al. (2000) A positron emission tomographic study of auditory localization in the congenitally blind. J Neurosci 20:2664–2672

    CAS  PubMed  Google Scholar 

  • Weinberger NM, Hopkins W, Diamond DM (1984) Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response. I. Primary field (AI). Behav Neurosci 98:171–188

    Article  CAS  PubMed  Google Scholar 

  • Wurth NN, Heid S, Kral A, Klinke R (1999) Morphology of neurons in the primary auditory cortex (A1) in normal and congenitally deaf cats—a study of DiI labeled cells. Göttingen, Neuradiology Report 27:318

  • Yaka R, Yinon U, Wollberg Z (1999) Auditory activation of cortical visual areas in cats after early visual deprivation. Eur J Neurosci 11:1301–1312

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Professor W. Singer for providing research facilities, Dr. Silvia Heid for her expertise in histology and help during the experiments, and Peter Hubka for introducing A.K. into MatLab programming. The technical assistance of Mrs. Maren Kurschat, Natalie Krimmel, and Regina Wagner is gratefully acknowledged. The work was supported by Deutsche Forschungsgemeinschaft (SFB 269 and EN 203/9–2).

Author information

Authors and Affiliations

  1. Physiologisches Institut II, J.W. Goethe Universität, Theodor-Stern-Kai 7, 60590, Frankfurt am Main, Germany

    A. Kral & R. Klinke

  2. Max-Planck-Institut für Hirnforschung, Deutschordenstrasse 46, 60590, Frankfurt am Main, Germany

    J.-H. Schröder

  3. Institut für Neurophysiologie und Pathophysiologie, Zentrum für Experimentelle Medizin, Universitätsklinikum Hamburg-Eppendorf, Martinistr. 52, 20246, Hamburg, Germany

    A. K. Engel

Authors
  1. A. Kral
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J.-H. Schröder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Klinke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. K. Engel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Kral.

Additional information

A.K. and J.-H.S. contributed equally to the study

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kral, A., Schröder, JH., Klinke, R. et al. Absence of cross-modal reorganization in the primary auditory cortex of congenitally deaf cats. Exp Brain Res 153, 605–613 (2003). https://doi.org/10.1007/s00221-003-1609-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-003-1609-z

Keywords

Search

Navigation