A model was developed that simulates the binaural response properties of low-frequency inferior colliculus (IC) neurons in response to several types of stimuli. The model incorporates existing models for auditory-nerve fibers, bushy cells in the cochlear nucleus, and cells in medial superior olive (MSO). The IC model neuron receives two inputs, one excitatory from an ipsilateral MSO model cell and one inhibitory from a contralateral MSO model cell. The membrane potential of the IC model neuron (and the other model neurons) is described by Hodgkin–Huxley type equations. Responses of IC neurons are simulated for pure-tone stimuli, binaural beat stimuli, interaural phase-modulated tones, single binaural clicks, and pairs of binaural clicks. The simulation results show most of the observed properties of IC discharge patterns, including the bimodal and unimodal interaural time difference (ITD) functions, sensitivities to direction and rate of change of ITD, ITD-dependent echo suppression, and early and late inhibitions in response to clicks. This study demonstrates that these response properties can be generated by a simple model incorporating ITD-dependent excitation and inhibition from binaural neurons.

1.
Adams, J. C., and Mugnaini, E. (1984). “Dorsal neucleus of lateral lemniscus: A nucleus of GABAergic projection neurons,” Brain Res. Bull. 13, 585–590.
2.
Adams, J. C., and Wenthold, R. J. (1987). “Immunostaining of ascending auditory pathways with glycine antiserum,” Assoc. Res. Otolaryngol. 10, 63.
3.
Blauert, J. (1983). “The psychophysics of human sound localization,” in Spatical Hearing (MIT, Cambridge, MA), pp. 1–408.
4.
Boerger, G. (1965). “Über die Trägheit des Gehörs bei der Richtungsempfindung [On the persistence of the directional sensation in hearing],” Proceedings of the 5th International Congress on Acoustics, liége, B 27.
5.
Brugge
,
J. F.
,
Anderson
,
D. J.
, and
Aitkin
,
L. M.
(
1970
). “
Responses of neurons in the dorsal nucleus of lateral lemniscus of cat to binaural tonal stimulation
,”
J. Neurophysiol.
33
,
441
458
.
6.
Brughera
,
A. R.
,
Stutman
,
E. R.
,
Carney
,
L. H.
, and
Colburn
,
H. S.
(
1996
). “
A model with excitation and inhibition for cells in the medial superior olive
,”
Aud. Neurosci.
2
,
219
233
.
7.
Cai, H. (unpublished).
8.
Cai, H. (1997). “Models for the binaural response properties of inferior colliculus neurons,” dissertation, Boston University.
9.
Cai
,
H.
,
Carney
,
L. H.
, and
Colburn
,
H. S.
(
1998
). “
A model for binaural response properties of inferior colliculus neurons: II. A model with interaural time difference sensitive excitatory and inhibitory inputs and an adaptation mechanism
,”
J. Acoust. Soc. Am.
103
,
494
506
.
10.
Cant
,
N. B.
, and
Hyson
,
R. L.
(
1992
). “
Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil
,”
Hearing Res.
49
,
281
298
.
11.
Carney
,
L. H.
(
1993
). “
A model for the responses of low-frequency auditory-nerve fibers in cat
,”
J. Acoust. Soc. Am.
93
,
401
417
.
12.
Carney
,
L. H.
, and
Yin
,
T. C. T.
(
1989
). “
Responses of low-frequency cells in the inferior colliculus to interaural time differences of clicks: Excitatory and inhibitory components
,”
J. Neurophysiol.
62
,
144
161
.
13.
Colburn, H. S. (1996). “Computational models of binaural processing,” in Auditory Computation, edited by H. Hawkins and T. McMullen (Springer-Verlag, Berlin), pp. 332–400.
14.
Colburn
,
H. S.
, and
Ibrahim
,
H.
(
1993
). “
Modeling of precedence effect behavior in single neurons and in human listeners
,”
J. Acoust. Soc. Am.
93
,
2293
(A).
15.
Eccles, J. C. (1964). The Physiology of Synapses (Academic, New York).
16.
Finlayson
,
P. G.
, and
Caspary
,
D. M.
(
1989
). “
Synaptic potentials of chinchilla lateral superior olivary neurons
,”
Hearing Res.
38
,
221
228
.
17.
Fitzpatrick
,
D. C.
,
Kuwada
,
S.
,
Batra
,
R.
, and
Trahiotis
,
C.
(
1995
). “
Neural responses to simple simulated echoes in the auditory brain stem of the unanesthetized rabbit
,”
J. Neurophysiol.
74
,
2469
2486
.
18.
Glendenning
,
K. K.
,
Brunso-Bechtold
,
J. K.
,
Thompson
,
G. C.
, and
Masterton
,
R. B.
(
1981
). “
Ascending auditory afferents to the nuclei of the lateral lemniscus
,”
J. Comp. Neurol.
197
,
673
703
.
19.
Goldberg
,
J. M.
, and
Brown
,
P. B.
(
1969
). “
Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms for sound localization
,”
J. Neurophysiol.
32
,
613
636
.
20.
Guinan, Jr., J. J., Norris, B. E., and Guinan, S. S. (1972). “Single auditory units in the superior olivary complex. II. Locations of unit categories and tonotopic organization,” Int. J. Neurosci. 4, 147–166.
21.
Henkel
,
C. K.
, and
Spangler
,
K. M.
(
1983
). “
Organization of the efferent projections of the MSO nucleus in the cat as revealed by HRP and autoradiographic tracing methods
,”
J. Comp. Neurol.
221
,
416
428
.
22.
Hodgkin
,
A. L.
, and
Huxley
,
A. F.
(
1952
). “
A quantitative description of membrane current and its application to conduction and excitation in the nerve
,”
J. Physiol. (London)
117
,
500
544
.
23.
Johnson
,
D. H.
(
1980
). “
The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones
,”
J. Acoust. Soc. Am.
68
,
1115
1122
.
24.
Joris
,
P. X.
,
Carney
,
L. H.
,
Smith
,
P. H.
, and
Yin
,
T. C. T.
(
1994
). “
Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency
,”
J. Neurophysiol.
71
,
1022
1036
.
25.
Kuwada, S., Batra, R., and Fitzpatrick, D. C. (1997). “Neural processing of binaural temporal cues,” in Binaural and Spatial Hearing in Real and Virtual Environments, edited by R. H. Gilkey and T. R. Anderson (Erlbaum, Mahwah, NJ), pp. 399–426.
26.
Kuwada
,
S.
,
Batra
,
R.
, and
Stanford
,
T. R.
(
1989
). “
Monaural and binaural response properties of neurons in the inferior colliculus of the rabbit: Effects of sodium pentobarbital
,”
J. Neurophysiol.
61
,
269
282
.
27.
Kuwada
,
S.
,
Stanford
,
T. R.
, and
Batra
,
R.
(
1987
). “
Interaural phase-sensitive units in the inferior colliculus of the unanesthetized rabbit: Effects of changing frequency
,”
J. Neurophysiol.
57
,
1338
1360
.
28.
Kuwada
,
S.
, and
Yin
,
T. C. T.
(
1983
). “
Binaural interaction in low-frequency neurons in inferior colliculus of the cat. I. Effects of long interaural delays, intensity, and repetition rate on interaural delay function
,”
J. Neurophysiol.
50
,
981
999
.
29.
Kuwada
,
S.
,
Yin
,
T. C. T.
,
Syka
,
J.
,
Buunen
,
T. J. F.
, and
Wickesberg
,
R. E.
(
1984
). “
Binaural interaction in low-frequency neurons in inferior colliculus of the cat. IV. Comparison of monaural and binaural response properties
,”
J. Neurophysiol.
51
,
1306
1325
.
30.
Lindemann
,
W.
(
1986a
). “
Extension of a binaural cross-correlation model by contralateral inhibition. I. Simulation of lateralization for stationary signals
,”
J. Acoust. Soc. Am.
80
,
1608
1622
.
31.
Lindemann
,
W.
(
1986b
). “
Extension of a binaural cross-correlation model by contralateral inhibition. II. The law of the first wave front
,”
J. Acoust. Soc. Am.
80
,
1623
1630
.
32.
Litovsky R., and Yin, T. C. T. (1993). “Single-unit responses to stimuli that mimic the precedence effect in the inferior colliculus of the cat.” Assoc. Res. Otolaryngol. Abstr. 16, 128.
33.
Litovsky, R., and Yin, T. C. T. (1994). “Physiological correlates of the precedence effect: Free field recordings in the inferior colliculus of the cat,” Assoc. Res. Otolaryngol. Abstr. 17, 337.
34.
Manis
,
P. B.
, and
Marx
,
S. O.
(
1991
). “
Outward currents in isolated ventral cochlear nucleus neurons
,”
J. Neurosci.
11
,
2865
2880
.
35.
Mardia, K. V. (1972). Statistics of Directional Data (Academic, London).
36.
Oertel
,
D.
(
1983
). “
Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus
,”
J. Neurosci.
3
,
2043
2053
.
37.
Oertel
,
D.
(
1985
). “
Use of brain slices in the study of the auditory system: spatial and temporal summation of synaptic inputs in cells in the anteroventral cochlear nucleus of the mouse
,”
J. Acoust. Soc. Am.
78
,
328
333
.
38.
Oliver
,
D. L.
(
1987
). “
Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: possible substrates for binaural interaction
,”
J. Comp. Neurol.
264
,
24
46
.
39.
Oliver, D. L., and Huerta, M. F. (1992). “Inferior and superior colliculus,” in The Mammalian Auditory Pathway: Neuroanatomy, edited by D. B. Webster, A. N. Popper, and R. R. Fay (Springer-Verlag, Berlin), pp. 168–221.
40.
Oliver
,
D. L.
, and
Morest
,
D. K.
(
1984
). “
The central nucleus of the inferior colliculus in the cat
,”
J. Comp. Neurol.
222
,
237
264
.
41.
Peruzzi, D., and Oliver, D. L. (1995). “Intrinsic membrane properties and morphology of neurons in the rat inferior colliculus,” Assoc. Res. Otolaryngol. Abstr. 18, 515.
42.
Rose
,
J. E.
,
Gross
,
N. B.
,
Geisler
,
C. D.
, and
Hind
,
J. E.
(
1966
). “
Some neural mechanisms in the inferior colliculus of the cat which may be relevant to localization of a sound source
,”
J. Neurophysiol.
29
,
288
314
.
43.
Rothman
,
S. R.
,
Young
,
E. D.
, and
Manis
,
P. B.
(
1993
). “
Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model
,”
J. Neurophysiol.
70
,
2562
2583
.
44.
Shneiderman
,
A.
,
Chase
,
M. B.
,
Rockwood
,
J. M.
,
Benson
,
C. G.
, and
Potashner
,
S. J.
(
1993
). “
Evidence for a GABAergic projection from the dorsal nucleus of the lateral lemniscus to the inferior colliculus
,”
J. Neurochem.
60
,
72
82
.
45.
Shneiderman
,
A.
, and
Oliver
,
D. L.
(
1989
). “
EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus: A possible source of inhibitory inputs to the inferior colliculus
,”
J. Comp. Neurol.
286
,
28
47
.
46.
Shneiderman
,
A.
,
Oliver
,
D. L.
, and
Henkel
,
C. K.
(
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
.
47.
Smith
,
P. H.
(
1995
). “
Structural and functional differences distinguish principal from non-principal cells in the guinea pig MSO slice
,”
J. Neurophysiol.
73
,
1653
1667
.
48.
Smith
,
P. H.
,
Joris
,
P. X.
,
and
Carney
,
L. H.
(
1991
). “
Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of cat
,”
J. Comp. Neurol.
304
,
387
401
.
49.
Smith
,
P. H.
, and
Rhode
,
W. S.
(
1987
). “
Characterization of HRP-labeled globular bushy cells in the cat anteroventral cochlear nucleus
,”
J. Comp. Neurol.
266
,
360
375
.
50.
Spitzer
,
M. W.
, and
Semple
,
M. N.
(
1991
). “
Interaural phase coding in auditory midbrain: influence of dynamic stimulus features
,”
Science
254
,
721
724
.
51.
Spitzer, M. W., and Semple, M. N. (1992). “Responses to time-varying phase disparity in gerbil superior olive: evidence for hierarchical processing,” Soc. Neurosci. Abstr. 18, 149.
52.
Spitzer
,
M. W.
, and
Semple
,
M. N.
(
1993
). “
Responses of inferior colliculus neurons to time-varying interaural phase disparity: effects of shifting the locus of virtual motion
,”
J. Neurophysiol.
69
,
1245
1263
.
53.
Sujaku, Y., Kuwada, S., and Yin, T. C. T. (1981). “Binaural interaction in the cat inferior colliculus: comparison of the physiological data with a computer simulated model,” in Neuronal Mechanisms of Hearing, edited by J. Syka and L. Aitkin (Plenum, New York), pp. 233–238.
54.
Wu
,
S. H.
, and
Oertel
,
D.
(
1984
). “
Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus
,”
J. Neurosci.
4
,
1577
1588
.
55.
Yin, T. C. T. (personal communication).
56.
Yin
,
T. C. T.
(
1994
). “
Physiological correlates of the precedence effect and summing localization in the inferior colliculus of the cat
,”
J. Neurosci.
14
,
5170
5186
.
57.
Yin
,
T. C. T.
, and
Chan
,
J. C. K.
(
1990
). “
Interaural time sensitivity in medial superior olive of cat
,”
J. Neurophysiol.
64
,
465
488
.
58.
Yin
,
T. C. T.
,
Chan
,
J. C. K.
, and
Carney
,
L. H.
(
1987
). “
Effects of interaural time delays of noise stimuli on low-frequency cells in the cat’s inferior colliculus. III. Evidence for cross-correlation
,”
J. Neurophysiol.
58
,
562
583
.
59.
Yin
,
T. C. T.
,
Chan
,
J. C. K.
, and
Irvine
,
D. R. F.
(
1986
). “
Effects of interaural time delays of noise stimuli on low-frequency cells in the cat’s inferior colliculus. I. Responses to wideband noise
,”
J. Neurophysiol.
55
,
280
300
.
60.
Yin
,
T. C. T.
, and
Kuwada
,
S.
(
1983a
). “
Binaural interaction in low-frequency neurons in inferior colliculus of the cat. II. Effects of changing rate and direction of interaural phase
,”
J. Neurophysiol.
50
,
1000
1019
.
61.
Yin
,
T. C. T.
, and
Kuwada
,
S.
(
1983b
). “
Binaural interaction in low-frequency neurons in inferior colliculus of the cat. III. Effects of changing frequency
,”
J. Neurophysiol.
50
,
1020
1042
.
62.
Yin, T. C. T., and Kuwada, S. (1984). “Neuronal Mechanisms of Binaural Interaction,” in Dynamic Aspects of Neocortical Function, edited by G. M. Edelman, W. E. Gall, and W. M. Cowan (Wiley, New York), pp. 263–313.
This content is only available via PDF.
You do not currently have access to this content.