Auditory receptor neurons exhibit sensory habituation; their responses decline with repeated stimulation. We studied the effects of sensory habituation on the neural encoding of sound localization cues using crickets as a model system. In crickets, Teleogryllus oceanicus, sound localization is based on binaural comparison of stimulus intensity. There are two potential codes at the receptor-neuron level for interaural intensity difference: interaural difference in response strength, i.e. spike rate and/or count, and interaural difference in response latency. These are affected differently by sensory habituation. When crickets are stimulated with cricket-song-like trains of sound pulses, response strength declines for successive pulses in the train, and the decrease becomes more pronounced as the stimulus intensity increases. Response decrement is thus greater for receptors serving the ear ipsilateral to the sound source, where intensity is higher, resulting in a decrease in the interaural difference in response strength. Sensory habituation also affects response latency, which increases for responses to successive sound pulses in the stimulus train. The change in latency is independent of intensity, and thus is similar for receptors serving both ears. As a result, interaural latency difference is unaffected by sensory habituation and may be a more reliable cue for sound localization.

REFERENCES

Alexander
R. D.
(
1961
).
Aggressiveness, territoriality and sexual behavior in field crickets (Orthoptera; Gryllidae)
.
Behaviour
17
,
130
–.
Balakrishnan
R.
,
Pollack
G. S.
(
1996
).
Recognition of courtship song in the field cricket, Teleogryllus oceanicus
.
Anim. Behav
51
,
353
–.
Balakrishnan
R.
,
Pollack
G. S.
(
1997
).
The role of antennal sensory cues in female responses to courting males in the cricket Teleogryllus oceanicus
.
J. Exp. Biol
200
,
511
–.
Böhm
H.
,
Schildberger
K.
,
Huber
F.
(
1991
).
Visual and acoustic course control in the cricket Gryllus bimaculatus
.
J. Exp. Biol
159
,
235
–.
Carr
C. E.
(
1993
).
Processing of temporal information in the brain
.
Annu. Rev. Neurosci
16
,
223
–.
Clague
H.
,
Theunissen
F.
,
Miller
J. P.
(
1997
).
Effects of adaptation on neural coding by primary sensory interneurons in the cricket cercal system
.
J. Neurophysiol
77
,
207
–.
Coro
F.
,
Perez
M.
,
Mora
E.
,
Boada
D.
,
Conner
W. E.
,
Sandeford
M. V.
,
Avila
H.
(
1998
).
Receptor cell habituation in the A1 auditory receptor of four noctuoid moths
.
J. Exp. Biol
201
,
2879
–.
Eggermont
J. J.
(
1985
).
Peripheral auditory adaptation and fatigue: a model oriented review
.
Hearing Res
18
,
57
–.
Eggermont
J. J.
(
1998
).
Azimuth coding in primary auditory cortex of the cat. II. Relative latency and interspike interval representation
.
J. Neurophysiol
80
,
2151
–.
Eggermont
J. J.
,
Spoor
A.
(
1973
).
Cochlear adaptation in guinea pigs: a quantitative description
.
Audiology
12
,
193
–.
Eggermont
J. J.
,
Spoor
A.
(
1973
).
Masking of action potentials in the guinea pig cochlea, its relation to adaptation
.
Audiology
12
,
221
–.
Epping
W. J. M.
(
1990
).
Influence of adaptation on neural sensitivity to temporal characteristics of sound in the dorsal medullary nucleus and torus semicircularis of the grassfrog
.
Hearing Res
45
,
1
–.
French
A. S.
(
1989
).
Ouabain selectively affects the slow component of sensory adaptation in an insect mechanoreceptor
.
BrainRes
504
,
112
–.
French
A. S.
(
1989
).
Two components of rapid sensory adaptation in a cockroach mechanoreceptor neuron
.
J. Neurophysiol
62
,
768
–.
Gerhardt
H. C.
(
1991
).
Female mate choice in treefrogs: static and dynamic acoustic criteria
.
Anim. Behav
42
,
615
–.
Imaizumi
K.
,
Pollack
G. S.
(
1999
).
Neural coding of sound frequency by cricket auditory receptors
.
J. Neurosci
19
,
1508
–.
Laughlin
S. B.
(
1989
).
The role of sensory adaptation in insect compound eyes
.
J. Exp. Biol
146
,
39
–.
Miles
R. N.
,
Robert
D.
,
Hoy
R. R.
(
1995
).
Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea
.
J. Acoust. Soc. Am
98
,
1
–.
Mörchen
A.
,
Rheinlaender
J.
,
Schwartzkopf
J.
(
1978
).
Latency shift in insect auditory nerve fibers
.
Naturwissenschaften
65
,
656
–.
Pasztor
V. M.
,
Bush
B. M. H.
(
1983
).
Graded potentials and spiking in single units of the oval organ, a mechanoreceptor in the lobster ventilatory system. III. Sensory habituation to repetitive stimulation
.
J. Exp. Biol
107
,
465
–.
Pollack
G. S.
(
1988
).
Selective attention in an insect auditory neuron
.
J. Neurosci
8
,
2635
–.
Pollack
G. S.
(
1997
).
SWEEPS: a program for the acquisition andanalysis of neurophysiological data
.
Comput. Methods Programs Biomed
53
,
163
–.
Pollak
G. D.
(
1988
).
Time is traded for intensity in the bat's auditory system
.
Hearing Res
36
,
107
–.
Rheinlaender
J.
,
Mörchen
A.
(
1979
).
‘Time—intensity trading’ in locust auditory interneurons
.
Nature
281
,
672
–.
Smith
R. L.
,
Brachman
M. L.
,
Goodman
D. A.
(
1983
).
Adaptation in the auditory periphery
.
Ann. N.Y. Acad. Sci
405
,
79
–.
Sokolove
P. G.
,
Cooke
I. M.
(
1971
).
Inhibition of impulse activity in a sensory neuron by an electrogenic pump
.
J. Gen. Physiol
57
,
125
–.
Wickesberg
R. E.
,
Stevens
H. E.
(
1998
).
Responses of auditory nerve fibers to trains of clicks
.
J. Acoust. Soc. Am
103
,
1990
–.
Yin
T. C. T.
,
Chan
J. C. K.
(
1990
).
Interaural time sensitivity in medial superior olive of cat
.
J. Neurophysiol
64
,
1577
–.
Yin
T. C. T.
,
Hirsch
J. A.
,
Chan
J. C. K.
(
1985
).
Responses of neurons in the cat's superior colliculus to acoustic stimuli. II. A model of interaural intensity sensitivity
.
J. Neurophysiol
53
,
746
–.
This content is only available via PDF.