Experimental Brain Research

, Volume 39, Issue 1, pp 87–104 | Cite as

Thalamocortical transformation of responses to complex auditory stimuli

  • O. Creutzfeldt
  • F. -C. Hellweg
  • Chr. Schreiner
Article

Summary

In unanesthetized guinea pigs, thalamic (CGM), and cortical (auditory I) neurons were recorded simultaneously. Nine of 69 neuron pairs showed a positive cross-correlation of their spontaneous activities, with increased discharge probability of the cortical neuron beginning 2–5 ms after the discharge of the CGM-neuron. The individual neurons of such pairs had an identical CF and the same spectral responsiveness.

The responses of cortical neurons to pure tones were much more phasic than those of the corresponding CGM-neurons. Thalamic neurons could be driven up to much higher AM- and FM-modulation frequencies (100 Hz) than cortical neurons, which usually ceased to follow AM-frequencies above 20 Hz. Stronger or weaker suppression of tonic response components in cortical and thalamic neurons and the lower AM-range of cortical neurons is related to stronger or weaker intracortical and intrathalamic inhibition respectively. Response characteristics to FM-stimuli are similar to those of AM-stimuli.

All CGM and cortical neurons responded to a variety of natural calls of the same or of other species. Responses of CGM-cells represented more components of a call than cortical cells even if the two cells were synaptically connected. In cortical cells, repetitive elements of a call were not represented if the repetition rate was too high. High modulation frequencies within a call, such as those of the fundamental frequency, could still be separated in the response of some CGM-neurons, but never in those of cortical neurons. Both CGM and cortical cells responded essentially to transients (amplitude or frequency modulations) within a call, if spectral components of such elements were within the spectral sensitivity of the cell. Spectral components outside the spectral sensitivity range could result in suppression of spontaneous discharge rate. Responses of cortical and CGM-cells, and thus the representation of call elements by neuronal responses, varied with the intensity of a call. It is suggested that, at higher levels of the auditory system, essential information about the temporal features of complex sounds may be represented by neural responses to transients in various spectral regions.

Key words

Auditory system CGM Auditory cortex Thalamocortical transmission Complex sounds 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abeles M, Goldstein MH (1972) Responses of single units in the primary auditory cortex of the cat to tone and tone pairs. Brain Res 42: 337–352Google Scholar
  2. Cleland BG, Dubin RW, Levick WR (1971) Simultaneous recordings of input and output of lateral geniculate neurons. Nature (New Biol) 231: 191–192Google Scholar
  3. Creutzfeldt OD (1977) Generality of the functional structure of the neocortex. Naturwissenschaften 64: 507–517Google Scholar
  4. Creutzfeldt O, Ito M (1968) Functional synaptic organization of primary visual cortex neurons in the cat. Exp Brain Res 6: 324–352Google Scholar
  5. Creutzfeldt O, Kuhnt U, Benevento L (1974) An intracellular analysis of visual cortical responses to moving stimuli: Responses in a co-operative neuronal network. Exp Brain Res 21: 251–274Google Scholar
  6. Creutzfeldt O, Lux HD, Watanabe S (1966) Electrophysiology of cortical nerve cells. In: Purpura DP, Yahr MD (eds) The thalamus. Columbia University Press, New York, pp 209–231Google Scholar
  7. Creutzfeldt OD, Nothdurft HC (1978) Representation of complex visual stimuli in the brain. Naturwissenschaften 65: 307–318Google Scholar
  8. Dubin MW, Cleland BG (1977) The organization of visual inputs to interneurones of the lateral geniculate nucleus of the cat. J Neurophysiol 40: 410–427Google Scholar
  9. Dunlop CW, Itzkowic DJ, Aitkin LM (1969) Tone-burst response patterns of single units in the cats medial geniculate cortex. Brain Res 16: 149–164Google Scholar
  10. Etholm B, Gjerstad LI, Skrede KK (1976) Size and duration of inhibition in the medial geniculate body in unanesthetized cats. Acta Otolaryngol 81: 102–112Google Scholar
  11. Evans EF, Ross HF, Whitfield IC (1965) The spatial distribution of unit characteristic frequency in the primary auditory cortex of the cat. J Physiol (Lond) 179: 238–247Google Scholar
  12. Galambos R, Davis H (1943) The response of single auditory nerve fibres to acoustic stimulation. J Neurophysiol 6: 39–57Google Scholar
  13. Galambos R (1952) Microelectrode studies on medial geniculate body of cat. III. Response to pure tones. J Neurophysiol 15: 381–400Google Scholar
  14. Goldstein MH, Abeles M (1976) Single unit activity in the auditory cortex. In: Keidel WE, Neff WD (eds) Handbook of sensory physiology, Vol V/2. Springer, Berlin Heidelberg New YorkGoogle Scholar
  15. Funkenstein HH, Winter P (1973) Responses to acoustic stimuli of units in the auditory cortex of awake squirrel monkeys. Exp Brain Res 18: 464–488CrossRefGoogle Scholar
  16. Hellweg FC, Koch R, Vollrath M (1977) Representation of the cochlea in the neocortex of guinea pigs. Exp Brain Res 29: 467–474Google Scholar
  17. Hellweg FC, Schultz W, Creutzfeldt OD (1977) Extracellular and intracellular recordings from cat's cortical whisker projection area: Thalamo-cortical response transformation. J Neurophysiol 40: 463–479Google Scholar
  18. Hind JE, Davies PW, Woolsey CN, Benjamin RM, Welkes WS, Thompson RF (1960) Unit activity in the auditory cortex. In: Rasmussen GL, Windle WF (eds) Neural Mechanisms of the Auditory and Vestibular Systems, Chapt 10. Ch. C. Thomas, Springfield, Ill.Google Scholar
  19. Katsuki Y, Sumi T, Uchiyama H, Watanabe T (1962) Electric response of auditory neurons in cat to sound stimulation. J Neurophysiol 25: 569–588Google Scholar
  20. Kiang NY-S (1965) Discharge patterns of single fibers in the cat's auditory nerve. MIT Press, Cambridge, Mass.Google Scholar
  21. Lee BB, Cleland BG, Creutzfeldt OD (1977) The retinal input to cells in area 17 of the cat's cortex. Exp Brain Res 30: 527–538Google Scholar
  22. Merzenich MM, Knight PL, Roth GL (1975) Representation of the cochlea within primary auditory cortex in the cat. J Neurophysiol 38: 231–249Google Scholar
  23. Møller AR (1969) Unit responses in the rat cochlear nucleus to repetitive transient sounds. Acta Physiol Scand 75: 542–551Google Scholar
  24. Møller AR (1972) Coding of amplitude and frequency modulated sounds in the cochlear nucleus of the rat. Acta Physiol Scand 86: 223–238Google Scholar
  25. Nacimiento AC, Lux HD, Creutzfeldt OD (1964) Postsynaptische Potentiale von Nervenzellen des motorischen Cortex nach elektrischer Reizung spezifischer und unspezifischer Thalamuskerne. Pflügers Arch 281: 152–169Google Scholar
  26. Newman JD (1978) Central nervous system processing of sounds in primates. In: Steklis H, Raleigh MJ (eds) Neurobiology of social communication in primates. An evolutionary perspective. Academic Press, New YorkGoogle Scholar
  27. Pfeiffer R (1966) Classification of response patterns of spike discharge for units in the cochlear nucleus: Tone-burst stimulation. Exp Brain Res 1: 220–235Google Scholar
  28. Ribeaupierre F de, Goldstein MH, Yeni-Komishen G (1972a) Intracellular study of the cat's primary auditory cortex. Brain Res 48: 185–204Google Scholar
  29. Ribeaupierre F de, Goldstein MH, Yeni-Komishen G (1972b) Cortical coding of repetitive acoustic pulses. Brain Res 48: 205–225Google Scholar
  30. Scheich H (1970) In: Bullock TH (ed) Recognition of complex acoustic signals. Dahlem Konferenzen, Abakon Vlgs. Ges., BerlinGoogle Scholar
  31. Schreiner Chr (1979) Temporal suppression and speech processing. In: Creutzfeldt O, Scheich H, Schreiner Chr (eds) Hearing mechanisms and speech. Exp Brain Res (Suppl II). Springer, Berlin Heidelberg New YorkGoogle Scholar
  32. Swarbrick L, Whitfield IC (1972) Auditory cortical units selectively responsive to stimulus “shape”. J Physiol (Lond) 224: 68–69PGoogle Scholar
  33. Watanabe T, Katsuki Y (1974) Response patterns of single auditory neurones of the cat to species specific vocalization. Jap J Physiol 24: 135–155Google Scholar
  34. Watanabe T, Sakai H (1978) Responses of the cat's collicular auditory neuron to human speech. J Acoust Soc Am 64: 333–337Google Scholar
  35. Webster WR, Aitkin LM (1975) Central auditory processing. In: Gazzaniga MS, Blakemore C (eds) Handbook of psychology. Academic Press, New YorkGoogle Scholar
  36. Whitfield IC, Evans EF (1965) Responses of auditory cortical neurons to stimuli of changing frequency. J Neurophysiol 28: 656–672Google Scholar
  37. Winter P, Funkenstein HH (1973) The effect of species specific vocalizations on the discharge of auditory cortical cells in the awake squirrel monkey (saimiri sciureus). Exp Brain Res 18: 489–504Google Scholar

Copyright information

© Springer-Verlag 1980

Authors and Affiliations

  • O. Creutzfeldt
    • 1
  • F. -C. Hellweg
    • 1
  • Chr. Schreiner
    • 1
  1. 1.Department of NeurobiologyMax-Planck-Institute of Biophysical ChemistryGöttingenFederal Republic of Germany

Personalised recommendations