Ontogenetic changes in the response properties of individual, primary auditory afferents in the vocal plainfin midshipman fish Porichthys notatus Girard
1 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY
14853, USA
2 Department of Psychology, University of Washington, Seattle, WA 98195,
USA
* Author for correspondence (e-mail: sisneros{at}u.washington.edu)
Accepted 8 June 2005
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Summary |
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Key words: midshipman fish, Porichthys notatus, hearing, saccule, auditory neuron, vocalization, ontogeny
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Introduction |
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Previous developmental studies of auditory function in fishes have reported
either increases, decreases or no change in auditory sensitivity with age and
growth. Based on multiunit recordings from an in vitro preparation of
the macula neglecta, a nonotolithic end organ of the inner ear in the skate
Raja clavata, Corwin
(1983) was the first to
establish an ontogenetic increase in threshold sensitivity in response to
vibrational stimuli. Among teleosts, age/size-related increases in behavioral
auditory threshold sensitivity have been reported using behavioral
conditioning techniques for two distantly related species of hearing
generalists, a damselfish (Pomacentrus spp.) and the Red Sea bream
Pagrus major (Kenyon,
1996
; Iwashita et al.,
1999
). Wysocki and Ladich
(2001
) used the evoked
auditory brainstem recording (ABR) technique to show that auditory sensitivity
increases prior to the ability to vocalize and communicate acoustically in a
hearing specialist, the croaking gourami Trichopsis vittata. In
contrast to these studies, a recent ABR study shows that auditory threshold
sensitivity decreases with an increase in fish size for another species of
damselfish, the sergeant major Abudefduf saxatilis
(Egner and Mann, 2005
). A
final ontogenetic pattern has been identified among ostariophysines that are
hearing specialists; Popper
(1971
) reports no shifts in
behavioral auditory threshold sensitivity between two subadult groups of
goldfish Carassius auratus that differed in size (5 cm vs 10
cm total length); while Higgs et al.
(2002
,
2003
) used the ABR technique
to show that the bandwidth of detectable frequencies, but not auditory
threshold sensitivity, increased with age and size in zebrafish Danio
rerio.
The major goal of the present study was to determine age/size related
shifts in the discharge properties and the frequency response dynamics of
afferent neurons from the saccule of the plainfin midshipman fish
Porichthys notatus Girard. We focused on saccular afferents of
midshipman fish for several reasons. First, lesion experiments provide strong
support for the hypothesis that the saccule is their main organ of hearing
(Cohen and Winn, 1967).
Second, we have extensively studied the response properties of primary
saccular afferents in adults (McKibben and Bass,
1999
,
2001
;
Sisneros and Bass, 2003
;
Sisneros et al., 2004a
).
Third, no study has yet demonstrated how, or if, auditory mechanisms are
transformed during ontogeny in a hearing generalist. Fourth, it is unknown how
auditory sensitivity in a hearing generalist might change concurrently with
the ability to vocalize. Studies of vocal teleosts provide the advantage of
identifying the significance of changing auditory mechanisms in the context of
a well-defined, behaviourally relevant stimulus, namely vocalizations (see
Bass and McKibben, 2003
;
Lu, 2004
;
Bass and Lu, in press
). Fifth,
it remains essential to characterize the response dynamics of single-unit
auditory neurons if we are to integrate the results of previous ontogenetic
studies using ABR and behavioral conditioning techniques with the relative
abundance of single-unit recording studies of adults for both hearing
specialists and generalists, and other vertebrates in general. Lastly, we were
particularly interested in possible shifts in peripheral encoding mechanisms
during non-adult stages, given our recent demonstration of steroid-dependent
seasonal plasticity in peripheral frequency encoding among adults
(Sisneros et al., 2004a
).
To our knowledge, this study represents the first in vivo analysis of age- and size-related changes in the encoding properties of individual auditory neurons for any fish species. In contrast to our previous work showing changes in frequency encoding that are dependent on adult reproductive state, we now show that the resting discharge properties and auditory threshold sensitivity, but not the frequency response properties, of peripheral auditory neurons change with size (age) among pre-adult midshipman fish.
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Materials and methods |
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Although previous reports describe the response properties of eighth nerve
afferents in adult midshipman (see Introduction), we include some of that data
in this report to provide a more complete portrayal of age/size related
changes in response properties. Midshipman have two classes of adult males,
known as types I and II, which follow divergent reproductive and vocal tactics
(for a review, see Bass, 1996).
All of the new male data in this study are type I. Only type I males produce
advertisement calls to attract gravid females laden with ripe eggs to their
nest. We recently showed that elevation of plasma steroid levels of
testosterone and 17ß-estradiol to levels comparable to those found in
gravid females affect auditory saccular afferents in females via an
induced upward shift in best frequency and in the phase-locking precision at
higher frequencies >140 Hz (Sisneros et
al., 2004a
). Thus, in order to avoid any influences of naturally
cycling gonadal steroids on the response properties of the peripheral auditory
system we used only adult animals collected by otter trawl during the
non-reproductive season (see above). More specifically, we compare the
juvenile data to resting discharge data from 15 non-reproductive females and
frequency response data from 24 non-reproductive females that were part of a
previous study of seasonal changes in the adult peripheral auditory system
(Sisneros and Bass, 2003
).
Additional, unreported resting discharge data are included from six
non-reproductive females, and both resting discharge and frequency response
data from four non-reproductive males. An earlier report used a higher
stimulus intensity to characterize most auditory afferents in type I males
that were not classified as either reproductive or non-reproductive
(McKibben and Bass, 1999
), and
so we collected new data from a representative set of non-reproductive males
using the same stimulus intensity employed in this study and the previous one
of females (Sisneros and Bass,
2003
). Adult status (female SL >9.5 cm; male
SL >11.5 cm) was based on the previously reported dimorphic size
ranges for males and females (e.g. Bass et
al., 1996
; Brantley et al.,
1993a
; Foran and Bass,
1998
; Grober et al.,
1994
).
All animals were maintained in saltwater aquaria at 1215°C. Juveniles were fed brine shrimp every 23 days, whereas adults were fed goldfish and brine shrimp every 34 days.
Neurophysiology experiments
Standard electrophysiology techniques and recording methods were used to
characterize eighth nerve auditory afferents in the midshipman fish
(McKibben and Bass, 1999;
Sisneros and Bass, 2003
).
Animals were anesthetized by immersion in a seawater bath of 0.025% p-amino
benzoate (benzocaine; Sigma, St Louis, MO, USA) and then given an
intramuscular injection of pancuronium bromide (
0.5 mg
kg1) and fentanyl (
1 mg kg1) for
immobilization and analgesia, respectively. Eighth nerve auditory afferents of
the saccule were then exposed by dorsal craniotomy
(Fig. 1). The cranial cavity
was filled with an inert fluid (Fluorinert FC75, 3M, St Paul, MN, USA) to
enhance clarity and prevent drying. A 2 cm dam of denture cream was built up
around the cranial cavity, which then allowed the animal to be lowered just
below the water surface. Fish were then positioned such that the saccule was
10 cm above the surface of the underwater loudspeaker that was embedded
in sand on the bottom of a 30 cm diameter, 24 cm high Nalgene tank (similar in
design to that used by Fay,
1990
). The tank was housed inside an acoustic isolation chamber
(Industrial Acoustics, New York, NY, USA) on a vibration isolation table, and
all recording and stimulus generation equipment were located outside the
chamber. Fish were perfused continuously with fresh seawater at
1415°C through the mouth and over the gills during the experiments
and the condition of the animal was monitored by watching the blood flow in
the dorsal vasculature of the brain. All experimental procedures in this study
were conducted under the guidelines of the National Institutes of Health for
the care and use of animals and were approved by the Cornell University
Institutional Animal Care and Use Committee.
|
Stimulus generation
Acoustic stimuli were synthesized and generated using CASSIE software
package on a Macintosh Centris with a 12-bit DA board, attenuated (PA4,
Tucker-Davis Technology, Gainesville, FL, USA) and amplified (NAD 3020A, NAD
Electronics, Boston, MA, USA) before being played through an underwater
loudspeaker (UW-30, Telex Communications, Burnsville, MN, USA). The frequency
response of the underwater loudspeaker was measured using a minihydrophone
(Bruel and Kjaer 8103) in the position normally occupied by the head of the
fish. Relative sound pressure measurements were then made using a spectrum
analyzer (Stanford Research Systems SR780), calibrated by peak-to-peak voltage
measurements on an oscilloscope, and then adjusted with CASSIE software so
that the sound pressures at all frequencies (60400 Hz) used were of
equal amplitude within ±2 dB. Although the midshipman ear may be
primarily sensitive to the particle motion component of a sound wave, the
determination of sound level in terms of pressure provides a valid
characterization of the sound stimuli used here (for an extended discussion,
see McKibben and Bass, 1999;
also for recent review of underwater sound fields, see
Bass and Clark, 2003
).
Basic auditory stimuli consisted of eight repetitions of single tones 500
ms in duration, with fall and rise times of 50 ms. Each repetition was
presented at a rate of one every 1.5 s. Iso-intensity responses were measured
using pure tones presented at 10 or 20 Hz increments from 60 to 400 Hz at a
sound pressure of 130 dB re 1 µPa. This sound intensity is consistent with
known sound intensity levels for midshipman sounds recorded near the nests
(Bass and Clark, 2003).
Data analysis
Resting discharge activity was measured for eight repetitions of the
stimulus interval in the absence of an auditory stimulus and then used to
generate interspike interval histograms with 1 ms bins.
On isolation of single units showing an auditory response to the search
stimulus, the iso-intensity responses were measured for the vector strength of
synchronization (VS), which is a metric of the synchronization (i.e. degree of
phase locking) of the saccular afferent discharge to the auditory stimulus.
Spike train responses of auditory afferents to individual tones were
quantified for VS and were calculated from spike train data acquired over the
entire stimulus duration. VS is equivalent to the mean vector length for the
circular distribution of spikes over the period of the stimulus and was
calculated according to Goldberg and Brown
(1969) using 2 ms bins. VS
varies from 0 for either a random or uniform distribution to 1 for perfect
synchronization if all spikes fall in the same bin. A Rayleigh Z test
was performed to determine whether synchronization to pure tones was
significantly different from random (P<0.05)
(Batschelet, 1981
). Only
significant VS values were used to generate iso-intensity response curves. We
used the VS metric rather than averaged evoked spike rate because VS is known
to be less variable than the evoked spike rate (McKibben and Bass,
1999
,
2001
) and is a more consistent
measure for frequency encoding among teleost fishes (Fay,
1978
,
1982
,
1994
), including the
midshipman fish (McKibben and Bass,
1999
; Sisneros and Bass,
2003
).
The best frequency (BF) of a unit was determined as the frequency that evoked the highest VS to the individual tones.
Statistical analysis
The effect of life history stage (small juvenile, large juvenile, and
adult) on resting discharge, BF and auditory threshold at BF were determined
by one-way ANOVA followed by the NewmanKuels method for pairwise
multiple comparisons. In cases where data sets failed tests of equal variance
and a parametric ANOVA or a t-test could not be used, data were
analyzed using the non-parametric KruskalWallis one-way ANOVA followed
by the Dunn's test for pairwise multiple comparisons or the MannWhitney
U-test, respectively. The non-parametric Wilcoxon paired-sampled test
was used to test for differences in the iso-intensity profiles of VS median
values from nonreproductive adult type I males and adult females. For all
tests, was set at 0.05. An analysis of the slopes for the relationship
of VS at BF and resting discharge rate was determined by an analysis of
covariance (ANCOVA). Associations between resting discharge rate and
SL, auditory threshold at BF and SL, and VS at BF and
resting discharge rate were determined using Pearson's correlation and linear
regression. Differences in phase-locking precision at BF between silent and
spontaneously active units were determined by a Student's test. Values are
reported as means ± S.D. unless otherwise
stated.
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Results |
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Auditory neurons that did not display resting discharges were classified as silent units and comprised 15.8%, 16.1% and 7.2% of the total saccular afferent population in the small juvenile, large juvenile and adult size classes, respectively. Resting discharge rates ranged from 0 to 51.6 spikes s1 for small juveniles (N=38 units), 0 to 62.8 spikes s1 for large juveniles (N=31 units) and 0 to 100.4 spikes s1 for adults (N=69 units) (Fig. 2). Mean resting discharge rates increased with size from small juvenile to adults and were positively correlated with standard fish length (Fig. 3; r=0.59, H0: ß=0, t=3.33, P<0.005). Although there was no difference in resting discharge rates between large juveniles (mean= 17.4±18.1 spikes s1, median=9.6 spikes s1, N=31) and adults (mean=27.2±24.1 spikes s1, median=20.9 spikes s1, N=69), the median resting discharge rate for adults was 5.6 times greater than that for small juveniles (mean= 8.1±10.4 spikes s1, median=3.7 spikes s1, N=38) (Kruskal-Wallis one-way ANOVA, Dunn's test, H=23.6, d.f.=2, P<0.01). Thus, there is an approximate sixfold increase in resting discharge rate during development from the small juvenile to the adult size class.
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|
Frequency sensitivity of saccular afferents to auditory stimuli
Responses to single tone stimuli at 130 dB re 1 µPa were recorded for
163 auditory saccular afferent neurons in 54 midshipman fish: 27 units in 12
small juveniles (mean SL=3.9±0.6 cm), 35 units in 14 large
juveniles (mean SL=8.0±1.5 cm), and 101 units in 29 adults
(mean SL=13.7±2.2 cm). Because there was no significant
difference in the iso-intensity profiles of median VS values from the five
nonreproductive adult type I males (N=13 units) recorded for this
study and those collected from the non-reproductive adult females (SL
>9.5 cm; N=88 units) in our previous study
(Sisneros and Bass, 2003)
(Wilcoxon paired-sampled test, P=0.16), data were pooled and then
used for comparison to juveniles. Iso-intensity responses measured for spike
synchronization revealed similar shapes of the iso-intensity response curves
and BFs for the three size classes. Median VS declined gradually from 60 Hz to
400 Hz in all three size class (Fig.
4). The BFs ranged from 60 Hz to 200 Hz for all three size classes
(Fig. 5) and there was no
difference in mean BF among the three study groups (one-way ANOVA,
F=1.41, d.f.=2, 160, P=0.25).
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|
Auditory threshold at BF was determined for 16 saccular primary afferents from 12 fish (four units in three small juveniles, two units in two large juveniles, and ten units in seven adults). The auditory threshold at BF increased with size from small juvenile to adults and was negatively correlated with standard fish length (Fig. 6; r=0.65, H0: ß=0, t=3.19, P<0.01). Although there was no difference in threshold at BF between large juveniles (104±5 dB re 1 µPa, N=2) and adults (102±5 dB re 1 µPa, N=10), the mean sound pressure at the auditory threshold at BF for small juveniles (118±11 dB re 1 µPa, N=4) was approximately 56 times higher than that for large juveniles and adults, respectively (one-way ANOVA, NewmanKuels method, F=7.84, d.f.=2, 13, P<0.01). Thus, auditory sensitivity at BF increases during ontogeny from the small juvenile to the adult size class.
|
Relationship between VS at BF and resting discharge rate
A weak but significant linear relationship was discovered between
phase-locking precision at BF and resting discharge rate for a subsample of
auditory saccular afferents that were analyzed for both resting discharge rate
and VS at BF. The VS of synchronization at BF was negatively correlated with
the resting discharge rate for small juveniles (r=0.55,
H0: ß=0, t=2.58, P<0.05),
large juveniles (r=0.50, H0: ß=0,
t=2.74, P<0.05) and adults
(r=0.42, H0: ß=0,
t=3.48, P<0.01). Because the slopes of these
regressions did not differ among the three size classes (ANCOVA,
F=0.14, d.f.=2, 100, P=0.86), the data were pooled, and the
linear relationship for VS at BF and resting discharge rate was plotted
(Fig.
7)(r=0.48, H0: ß=0,
t=5.51, P<0.001). In addition, an analysis of
phase-locking precision at BF on the basis of discharge type (silent
vs spontaneous units) revealed that the mean VS at BF was higher for
silent units (0.94±0.08, N=12) than for spontaneously active
units (0.84+0.12, N=92) (t-test, t=2.68, d.f.=102,
P<0.01). Thus, these results show that VS at BF decreases with
increasing resting discharge rate and that silent units have higher
phase-locking precision at BF than spontaneously active units.
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Discussion |
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Resting discharge activity
The auditory primary afferent neurons in the saccular nerve of midshipman
and in many other teleost fishes form a relatively heterogeneous population of
spontaneously active units. The resting discharge rates were highly variable
and skewed in their distribution (the majority were <25 spikes
s1) for all three size classes of the midshipman fish. The
range (Fig. 2) and rate
(Fig. 3) of the resting
discharge activity increased with fish size. The high variability of resting
discharge rates for saccular afferents is common in other teleost fishes and
can vary from 0200 spikes s1 for sculpin Cottus
scorpius (Enger, 1963),
0250 spikes s1 for the Atlantic cod Gadus
morhua (Horner et al.,
1981
), 0184 spikes s1 for catfish
Ictalurus punctatus (Moeng and
Popper, 1984
), 0310 spikes s1 for
goldfish Carassius auratus (Fay,
1981
), 0180 spikes s1 for toadfish
Opsanus tau (Fay and Edds-Walton,
1997
), and 0162 spikes s1 for sleeper
goby Dormitator latifrons (Lu et
al., 1998
). Such differences in the resting discharge rates among
the various teleost species may be due to a wide range of factors that include
species differences in the discharge properties of the peripheral auditory
system and/or the number of hair cells that are innervated by individual
primary afferent neurons. However, some of this variability is most likely due
to the influence of temperature on neuronal response properties. Temperature
is known to have a significant influence on the thresholds for membrane
depolarization and spike initiation of neurons
(Carpenter, 1981
). The
previous studies were conducted using both tropical and temperate fish species
at their respective ambient temperatures.
The mean resting discharge rate for adult midshipman fish (29.4 spikes
s1) was higher than that reported for most species of adult
teleost fishes, except for the Atlantic cod G. morhua, which had a
rate as high as 94 spikes s1
(Horner et al., 1981). Mean
rates for other adult teleosts range from 16 spikes s1 in
the sleeper goby (Lu et al.,
1998
) to 1322 spikes s1 in the goldfish
(Fay and Ream, 1986
). In
contrast to mean spike rates, the percent occurrence of silent units recorded
for juvenile (about 16%), and adult (7.2%) midshipman was much lower than that
previously reported for other teleosts, again with the exception of the
Atlantic cod (6%; Horner et al.,
1981
). The percent occurrence of silent units reported for other
teleosts range from about 3045%
(Enger, 1963
;
Fay, 1978
;
Moeng and Popper, 1984
).
Resting discharge rates of adult midshipman were approximately six times
those of small juveniles. This ontogenetic increase in resting discharge rate
likely facilitates an increase in the sampling and encoding of frequency
information as well as auditory threshold sensitivity. Previous work on
mammals indicates that auditory sensitivity (i.e. auditory intensity
thresholds) of primary afferent neurons is inversely correlated with resting
discharge rate (Liberman,
1978; Geisler et al.,
1985
). The intensity thresholds of primary auditory afferents in
adult cats with low resting discharge rates (<0.5 spikes
s1) are, on average, at least 20 dB higher than those with
high resting discharge rates (>18 spikes s1) at any
particular characteristic frequency
(Liberman, 1978
). A similar
relationship between auditory threshold sensitivity and resting discharge rate
was found for midshipman saccular afferents across the different ontogenetic
stages studied here.
An age-related change in the morphology of the saccular afferents is one
possible means that could alter the response properties of the saccule. For
example, changes in the saccular afferent diameter could alter the saccular
afferent discharge properties and auditory threshold sensitivity. Variations
in afferent diameter could affect the space constants for excitatory
potentials generated by the hair-cell neurotransmitter and influence the
thresholds for membrane depolarization and afferent discharge behavior
(Liberman, 1982;
Geisler et al., 1985
).
Alternatively, age-related increases in the number of saccular hair cells and
an increase in the convergence ratio of hair cells to saccular afferent
neurons could also contribute to changes in the response properties and
threshold sensitivity of the saccule. Future studies that examine the
relationships of resting discharge rate, auditory threshold sensitivity,
saccular hair cell numbers and afferent morphology, and the functional role of
silent units will provide valuable insight into the mechanisms responsible for
the ontogenetic changes in the encoding properties of the midshipman
peripheral auditory system.
Auditory response properties of midshipman saccular afferents and functional significance of the ontogenetic changes
Our results indicate that the auditory saccular afferents of midshipman are
broadly tuned to relatively low-frequency auditory stimuli throughout
ontogeny. We show that the peripheral frequency sensitivity of adults is
similar to that of both small and large juveniles. Adult females show a
seasonal, reproductive-state dependent plasticity of peripheral frequency
encoding (Sisneros and Bass,
2003) that is dependent on seasonal shifts in circulating plasma
levels of testosterone and estradiol
(Sisneros et al., 2004a
).
Non-reproductive adults (Sisneros et al.,
2004b
), like juveniles
(Brantley et al., 1993b
; R.
Knapp and A. H. Bass, unpublished observations), have basal levels of gonadal
steroids. The similarity in the frequency response properties of saccular
afferents between juvenile and non-reproductive adult midshipman (also for
non-reproductive type I males; see
McKibben and Bass, 1999
), is
consistent with their shared steroid hormone profiles and the role of elevated
levels of circulating steroids in the induction of upward shifts in frequency
encoding.
In contrast to the maintenance of a similar pattern of frequency encoding
for saccular afferents from small juvenile to non-reproductive adult status,
we showed that auditory threshold sensitivity at BF increased with fish size
(age). Auditory threshold sensitivity at BF of large juveniles and adults was
approximately 56 times that of small juveniles. We were unable to
demonstrate a significant increase in auditory threshold sensitivity from
large juveniles (104 dB re 1 µPa) to adults (102 dB re 1 µPa), but this
may be due to the relatively low sample size of the large juvenile size class
for which we were only able to obtain two recordings of auditory threshold
sensitivity at BF for this size class. An increase in auditory threshold
sensitivity with size is known to occur in other hearing generalists, as
demonstrated via behavioral conditioning experiments
(Kenyon, 1996,
Iwashita et al., 1999
), but
increases in physiologically measured, auditory threshold sensitivity have
only been demonstrated in one non-teleostean fish, the elasmobranch skate
(Corwin, 1983
). In contrast, a
recent study of a hearing generalist, the sergeant major damselfish
Abudefduf saxatilis, indicated a decreased ABR-measured auditory
threshold sensitivity with an increase in fish size from post-settlement
juvenile to adult (Egner and Mann,
2005
). Studies of hearing specialists indicate either a lack of
increased auditory threshold sensitivity with size (age) using behavioral
(Popper, 1971
) and ABR (Higgs
et al., 2002
,
2003
) methods, or a small
increase in auditory sensitivity over a restricted range using ABR
(Wysocki and Ladich, 2001
).
Differences in physiologically determined levels of auditory sensitivity among
the fish species so far tested may yet be due to the differences in either the
recording technique, for example, multi-unit eighth nerve recordings
(Corwin, 1983
) vs ABR
(Higgs et al., 2002
,
2003
;
Egner and Mann, 2005
)
vs single-unit eighth nerve recordings (this study) and/or the
presence of accessory hearing structures among hearing specialists that may
influence the development of auditory sensitivity in fishes (also see
Higgs et al., 2003
). Further
study using all of the above methods in both a hearing generalist and a
hearing specialist would help to resolve these different hypotheses.
The phase-locking precision at BF was negatively correlated with resting
discharge rate for midshipman saccular afferents for all three size classes of
midshipman fish, as previously reported for adult females
(Sisneros and Bass, 2003) and
mammalian auditory afferents (Johnson,
1980
; Palmer and Russell,
1986
). The maintenance of this relationship throughout different
stages of ontogeny may describe the limits to which a synchronized response
can be represented in the discharge pattern of auditory saccular afferent
neurons.
Plainfin midshipman fish generate three types of vocal communication
signals during the adult life history stage
(Ibarra et al., 1983,
Brantley and Bass, 1994
, Bass
et al., 1999). Both male reproductive morphs and females produce broadband,
short duration (50200 ms) `grunts', important for agonistic encounters
(Fig. 8A). However, only
nesting males are known to produce `grunt trains', which are a rapid
succession of single grunts used to fend off potential intruders into their
nests. The pulse repetition rate of the grunt ranges from 97110 Hz. A
second type of agonistic signal known as a `growl' is also produced by nesting
type I males in agonistic encounters. Growls
(Fig. 8C) are multiharmonic and
relatively long in duration (>1 s). Growls have an initial grunt-like
signal followed immediately by a multi-harmonic component with a fundamental
frequency (F0) of 59116 Hz that gradually changes
throughout the call. Nesting males also produce a third type of vocal signal
known as the `hum', which is a long duration (>1 min) multiharmonic
advertisement call (Fig. 8E).
Hums have F0 values similar to that grunts and growls that
range from 90100 Hz, contain several prominent harmonics ranging up to
400 Hz that typically contain as much or more spectral energy than the
F0, and are produced by nesting males during the breeding
season to attract gravid females for spawning.
|
The results of this study indicate that the saccular afferents of
juveniles, like those of non-reproductive adults, are best adapted to
temporally encode the low frequency components (100 Hz) of midshipman
vocalizations. The saccule of reproductive females shows enhanced temporal
encoding of the higher harmonics of the hum
(Sisneros and Bass, 2003
;
Sisneros et al., 2004a
) and
the growl (Fig. 8C,D), thereby
likely improving the receiver's probability of conspecific detection,
identification and localization during the summer breeding season (for further
discussion, see Sisneros et al.,
2004a
; Bass and Clark,
2003
; peripheral encoding in reproductive males has yet to be
studied). It is currently unknown if juveniles are sonic, but we expect them
only to make isolated grunts like females and type II males (see
Brantley and Bass, 1994
),
especially given the similarities in the morpho-physiological properties of
their vocal motor systems (Bass,
1995
; Bass et al.,
1996
). Field measurements of transmission distance show that the
F0 of midshipman-like calls falls off rapidly with
increasing distance from the sound source
(Fine and Lenhardt, 1983
; also
see Bass and Clark, 2003
),
which in this case would be a conspecific. Given this, the auditory system of
juveniles seems best adapted for the detection of calling conspecifics at
close range.
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Acknowledgments |
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References |
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