Skip to main content
Log in

Processing of binaural stimuli by cat superior olivary complex neurons

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

A method was developed to record stereotactically from the cat Superior Olivary Complex (SOC) using glass micropipettes. Sound stimulation was given through a closed system that permitted independent variation of interaural time (Δtime) and intensity (Δint) differences. The most common binaural units found (n = 34) were ipsilateral excitatory, contralateral inhibitory (EI1), cells of the Lateral Superior Olive (LSO). Some Medial Superior Olive (MSO) cells and presumed MSO ascending afferents were found but, as noted by other authors, we found it difficult to obtain single unit recordings from this nucleus. The LSO EI cells were mostly sensitive to higher frequencies and showed Peristimulus Time Histograms (PSTHs) consisting of a sharp “On” response followed by a plateau when stimulated with Best Frequency (BF) tone bursts or noise bursts. This “On” response was sensitive to Δtime and Δint such that ipsilateral time lead or intensity increase resulted in a stronger response. The response reached a minimum around zero Δtime or Δint. No sharp peaks or dips were seen in the physiological range needed for localization, instead the response increased with increasing ipsilateral lead or intensity to the maximum values tested (2048 μs Δtime, 30 dB Δint). In the physiological range the Δtime and Δint response were complementary (both increasing response as ipsilaterality was increased). Provided enough sound energy in the unit's sensitive region was present, the same Δtime curves were produced when BF tone bursts, masked tone bursts, “sharp onset” tone bursts or noise bursts were used. Changing the Δtime of the carrier of the tone burst alone had no effect (except for one cell with a BF of 560 Hz), only the relative time of arrival of the stimulus envelope seemed to be important. In contrast to these LSO EI cells MSO-type units showed EI or EE predominantly low frequency phase-locked responses. When stimulated with interaurally phase shifted (Δpha) BF tones the unit response was a cyclic function of Δpha. Some cells (all that were tested, n = 6 including the 560 Hz LSO EI cell) showed these cyclic responses when stimulated with noise bursts or non-BF tones. However, these “characteristic delays” were not necessarily in the physiological range, i.e. we could find no evidence that these units were responding to Δtime/Δpha values corresponding to a particular sound source direction. In both LSO and MSO it seems that integration of information higher in the CNS from a population of these cells is necessary for unambiguous coding of sound source direction. The time intensity trading ratios measured in two MSO type cells (11 and 26 μ/dB) were clearly different to those measured in LSO EI cells (n = 6, 99–550 μs/dB). These ratios correspond approximately to those of the psychophysical Δtime and Δint images measured by Hafter and Jeffress (1968).

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

Access this article

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

  • Blauert J (1974) Räumliches Hören. Hirzel, Stuttgart. English version: Spatial Hearing. MIT Press, Boston, Mass. (1983) (in press)

    Google Scholar 

  • Boudreau J, Tsuchitani C (1968) Binaural interaction in the cat Superior Olive S-segment. J Neurophysiol 31: 445–454

    Google Scholar 

  • Brownell WE (1975) Organisation of the cat trapezoid body and the discharge characteristics of its fibres. Brain Res 94: 413–433

    Google Scholar 

  • Brownell WE, Manis PB, Ritz LA (1979) Ipsilateral inhibitory responses in the cat Lateral Superior Olive. Brain Res 177: 189–193

    Google Scholar 

  • Bullock TH (ed) (1977) Recognition of complex acoustic signals. Life sciences research reports, vol 5. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Caird DM, Göttl KH, Klinke R (1980) Interaural attenuation in the cat, measured with single fibre data. Hear Res 3: 257–263

    Google Scholar 

  • Casseday JH, Neff WD (1973) Localisation of pure tones. J Acoust Soc Am 54: 365–372

    Google Scholar 

  • Clark GM, Dunlop CW (1968) Field potentials in the cat medial Superior Olivary Nucleus. Exp Neurol 20: 31–42

    Google Scholar 

  • Crow G, Rupert AL, Moushegian G (1978) Phase locking in monaural and binaural medullary neurons: Implications for binaural phenomena. J Acoust Soc Am 64: 493–501

    Google Scholar 

  • Elverland HH (1977) Ascending and intrinsic connections of the Superior Olivary Complex in the cat. Exp Brain Res 32: 117–134

    Google Scholar 

  • Galambos R, Schwartzkopf J, Rupert A (1959) Micro electrode study of Superior Olivary Nuclei. Am J Physiol 197: 527–536

    Google Scholar 

  • Goldberg JM, Brown PB (1968) Functional organisation of dog Superior Olivary Complex: Functional and anatomical study. J Neurophysiol 31: 639–656

    Google Scholar 

  • Goldberg JM, Brown PB (1969) Response of binaural neurons of dog Superior Olivary Complex to dichotic tonal stimuli: Some physiological mechanisms of sound localization. J Neurophysiol 32: 613–636

    CAS  PubMed  Google Scholar 

  • Goldberg JM, Smith FD, Adrian HO (1963) Response of single units of the Superior Olivary Complex of the cat to acoustic stimulation: Laterality of afferent projections. Anat Rec 145: 232

    Google Scholar 

  • Guinan JJ, Norris BE, Swift SH (1967) A paucity of unit responses in the accessory Superior Olivary Nucleus of barbiturate anesthetized cats. J Acoust Soc Am 41: 1585

    Google Scholar 

  • Guinan JJ, Guinan SS, Norris BE (1972a) Single auditory units in the Superior Olivary Complex. I. Responses to sounds and classification based on physiological properties. Int J Neurosci 4: 101–120

    Google Scholar 

  • Guinan JJ, Norris BE, Guinan SS (1972b) Single auditory units in the Superior Olivary Complex. II. Locations of unit categories and tonotopic organisation. Int J Neurosci 4: 147–166

    Google Scholar 

  • Hafter ER, Jeffress LA (1968) Two image lateralisation of tones and clicks. J Acoust Soc Am 44: 563–569

    Google Scholar 

  • Hall JL (1965) Binaural interaction in the accessory Superior Olivary Nucleus of the cat. J Acoust Soc Am 37: 814–823

    Google Scholar 

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

    Google Scholar 

  • Harnischfeger G (1979) An improved method for extracellular marking of electrode tip positions in nervous tissue. Neurosci Methods 1: 195–200

    Google Scholar 

  • Harnischfeger G (1980) Brainstem units of echolocating bats code binaural time differences in the microsecond range. Naturwissenschaften 67: 314–315

    Google Scholar 

  • Henning GB (1980) Some observations on the lateralisation of complex waveforms. J Acoust Soc Am 68: 446–454

    Google Scholar 

  • Inbody SB, Feng AS (1981) Binaural response characteristics of single neurons in the Medial Superior Olivary Nucleus of the albino rat. Brain Res 210: 361–366

    Google Scholar 

  • Irving R, Harrison JM (1967) The Superior Olivary Complex and audition a comparative study. J Comp Neurol 130: 77–86

    Google Scholar 

  • Jenkins WM, Masterton RB (1982) Sound localization: Effects of unilateral lesions in central auditory system. J Neurophysiol 47: 987–1016

    Google Scholar 

  • Masterton RB, Jane JA, Diamond IT (1967) Role of brainstem auditory structures in sound localization. I. Trapezoid body Superior Olive and Lateral Lemniscus. J Neurophysiol 30: 341–359

    Google Scholar 

  • Masterton RB, Jane JA, Diamond IT (1968) Role of brainstem auditory structures in sound localization. II. Inferior colliculus and its brachium. J Neurophysiol 31: 96–108

    Google Scholar 

  • Masterton RB, Diamond IT (1967) The Medial Superior Olive and sound localization. Science 155: 1696–1697

    Google Scholar 

  • McFadden D, Pasanen EG (1976) Lateralisation at high frequencies based on interaural time differences. J Acoust Soc Am 59: 634–639

    Google Scholar 

  • Middlebrooks JC, Pettigrew JD (1981) Functional classes of neurons in primary Auditory Cortex of the cat distinguished by sensitivity to sound source location. J Neurosci 1: 107–120

    Google Scholar 

  • Moushegian G, Rupert A, Whitcombe MA (1964a) Brain stem neuronal response patterns to monaural and binaural tones. J Neurophysiol 27: 1174–1191

    Google Scholar 

  • Moushegian G, Rupert A, Whitcombe MA (1964b) Medial Superior Olivary unit response patterns to monaural and binaural clicks. J Acoust Soc Am 36: 196–202

    Google Scholar 

  • Moushegian G, Rupert AL, Langford TL (1967) Stimulus coding by medial Superior Olive neurons. J Neurophysiol 30: 1239–1261

    Google Scholar 

  • Moushegian G, Stillman RD, Rupert AL (1971) Characteristic delays in the Superior Olivary Complex and Inferior Colliculus. In: Sachs MB (ed) Physiology of the auditory system. National Educational Consultants, Baltimore, pp 245–254

    Google Scholar 

  • Moushegian G, Rupert AL, Gidda JS (1975) Functional characteristics of Superior Olivary neurons to binaural stimuli. J Neurophysiol 38: 1037–1048

    Google Scholar 

  • Moiseff A, Konishi M (1981) Neuronal and behavioural sensitivity to interaural time differences in the owl. J Neurosci 1: 40–48

    Google Scholar 

  • Papajewski W (1979) ‘Recognition’ of binaural patterns of tone intensity in the Superior Olivary Complex of the rat. Verh Dtsch Zool Ges 223: 61

    Google Scholar 

  • Rose JE, Gross NB, Geisler CD, Hind JE (1966) Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localisation of a sound source. J Neurophysiol 29: 288–314

    Google Scholar 

  • Thompson GC, Masterton RB (1978) Brain stem auditory pathways involved in reflexive head orientation to sound. J Neurophysiol 41: 1183–1202

    Google Scholar 

  • Tsuchitani C (1977) Functional organisation of lateral cell groups of cat Superior Olivary Complex. J Neurophysiol 40: 296–318

    Google Scholar 

  • Tsuchitani C, Boudreau JC (1964) Wave activity in the Superior Olivary Complex of the cat. J Neurophysiol 27: 814–827

    Google Scholar 

  • Tsuchitani C, Boudreau JC (1966) Single unit analysis of cat Superior Olive S-segment with tonal stimuli. J Neurophysiol 29: 684–697

    Google Scholar 

  • Tsuchitani C, Boudreau JC (1967) Encoding of stimulus frequency and intensity by cat Superior Olive S-segment cells. J Acoust Soc Am 42: 794–805

    Google Scholar 

  • Tsuchitani C, Boudreau JC (1969) Stimulus level of dichotically presented tones and cat Superior Olive S-segment cell discharge. J Acoust Soc Am 46: 979–988

    Google Scholar 

  • Warr WB (1966) Fiber degeneration following lesions in the anteroventral cochlear nucleus of the cat. Exp Neurol 14: 453–474

    Google Scholar 

  • Warr WB (1969) Fiber degeneration following lesions in the posteroventral cochlear nucleus of the cat. Exp Neurol 23: 140–155

    Google Scholar 

  • Warr WB (1972) Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat. Brain Res 40: 247–270

    Google Scholar 

  • Wiener FM, Pfeiffer RR, Backus ASN (1966) On the sound pressure transformation by the head and auditory meatus of the cat. Acta Otolaryngol 61: 255–269

    Google Scholar 

  • Woolf NK (1981) Precise extracellular marking in the auditory nerve with high impedance micropipettes. Hearing Res 4: 121–125

    Google Scholar 

  • Worden FG, Galambos R (eds) (1974) Auditory processing of biologically significant sounds. Neuroscience Research Program Bulletin 10. Neuroscience Research Program, Brookline, Mass

    Google Scholar 

  • Yost WA, Wightman FL, Green DM (1971) Lateralisation of filtered clicks. J Acoust Soc Am 50: 1526–1531

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by the Deutsche Forschungsgemeinschaft (SFB 45)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caird, D., Klinke, R. Processing of binaural stimuli by cat superior olivary complex neurons. Exp Brain Res 52, 385–399 (1983). https://doi.org/10.1007/BF00238032

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00238032

Key words

Navigation