443
1998 , 2001a ; Zeddies et al. 2010 ; Zeddies et al. 2012 ). Because nocturnally active
reproductive females were known to rely on their auditory sense to locate mates,
Sisneros and Bass ( 2003 ) posited that the animal’s seasonal reproductive state infl uenced female auditory sensitivity and thus proceeded to test the hypothesis that
female reproductive state (gravid vs. non-gravid) modulated the frequency response
properties and sensitivity of the peripheral auditory system. Sisneros and Bass
( 2003 ) showed that summer reproductive females were more sensitive than winter
non-reproductive females to higher frequencies within the species’ hearing range.
Specifi cally, the auditory saccular afferents of reproductive females had greater
phase-locking accuracy than that of non-reproductive females to frequencies of
120–400 Hz, which corresponded to the dominant higher harmonic components of
the male’s advertisement call. Similarly, Sisneros ( 2009a ) showed that the hair cells
in the saccule, the main organ of hearing in midshipman, from reproductive females
were 2.5–4.5× more sensitive than that of non-reproductive females to frequencies
of 75–385 Hz, which also corresponds to the frequencies of the advertisement call
that contain the majority of the energy in the call.
Recently, Rohmann et al. ( 2013 ) showed that the pore-forming alpha-subunit slo
1 gene and its transcripts, slo 1a and slo 1b , both of which are expressed in the saccular epithelium (Rohmann et al. 2009 ), are upregulated during the summer reproductive season, which is consistent with higher BK channel expression and enhanced
higher frequency encoding in females (Rohmann et al. 2013 ). Higher BK channel
expression in the saccule of reproductive females is signifi cant because in nonmammalian vertebrates, hair cells with greater expression of calcium-activated
potassium (BK) channels are capable of higher resonant frequencies, and thus are
better at encoding higher frequency sounds (Fettiplace and Fuchs 1999 ). Together
these studies provide evidence that the peripheral auditory sensitivity of female
midshipman is modulated by the female’s reproductive cycle such that reproductive
females are better adapted than non-reproductive females to detect and encode the
dominant harmonic frequencies in the male’s advertisement call. This enhanced
sensitivity may represent an adaptation of the teleost auditory system to increase the
probability of mate localization and enable females to acquire acoustic information
needed for mate choice decisions.
The seasonal enhancement of hearing in female midshipman for the detection of
the higher frequency harmonics in the male social acoustic signals is likely adaptive for the shallow water acoustic environment where midshipman court and
socially interact during the breeding season. Sound propagation of low frequency
sounds in shallow water environments are greatly affected by water depth and substrate composition (Rogers and Cox 1988 ). The higher frequency harmonics of the
male’s advertisement call have been proposed to provide greater signal detection of
the male’s social acoustic signal for females because the advertisement call’s dominant harmonics (200–400 Hz) will propagate farther than the lower fundamental
frequency (~80–100 Hz) in shallow water environments due to an inverse relationship between the cutoff frequency of sound transmission and water depth (Fine and
Lenhardt 1983 ; Rogers and Cox 1988 ; Sisneros and Bass 2003 ). Substrate composition of the shallow water environment is also an important factor that affects
Neuroanatomical Evidence for Catecholamines as Modulators of Audition…
1998 , 2001a ; Zeddies et al. 2010 ; Zeddies et al. 2012 ). Because nocturnally active
reproductive females were known to rely on their auditory sense to locate mates,
Sisneros and Bass ( 2003 ) posited that the animal’s seasonal reproductive state infl uenced female auditory sensitivity and thus proceeded to test the hypothesis that
female reproductive state (gravid vs. non-gravid) modulated the frequency response
properties and sensitivity of the peripheral auditory system. Sisneros and Bass
( 2003 ) showed that summer reproductive females were more sensitive than winter
non-reproductive females to higher frequencies within the species’ hearing range.
Specifi cally, the auditory saccular afferents of reproductive females had greater
phase-locking accuracy than that of non-reproductive females to frequencies of
120–400 Hz, which corresponded to the dominant higher harmonic components of
the male’s advertisement call. Similarly, Sisneros ( 2009a ) showed that the hair cells
in the saccule, the main organ of hearing in midshipman, from reproductive females
were 2.5–4.5× more sensitive than that of non-reproductive females to frequencies
of 75–385 Hz, which also corresponds to the frequencies of the advertisement call
that contain the majority of the energy in the call.
Recently, Rohmann et al. ( 2013 ) showed that the pore-forming alpha-subunit slo
1 gene and its transcripts, slo 1a and slo 1b , both of which are expressed in the saccular epithelium (Rohmann et al. 2009 ), are upregulated during the summer reproductive season, which is consistent with higher BK channel expression and enhanced
higher frequency encoding in females (Rohmann et al. 2013 ). Higher BK channel
expression in the saccule of reproductive females is signifi cant because in nonmammalian vertebrates, hair cells with greater expression of calcium-activated
potassium (BK) channels are capable of higher resonant frequencies, and thus are
better at encoding higher frequency sounds (Fettiplace and Fuchs 1999 ). Together
these studies provide evidence that the peripheral auditory sensitivity of female
midshipman is modulated by the female’s reproductive cycle such that reproductive
females are better adapted than non-reproductive females to detect and encode the
dominant harmonic frequencies in the male’s advertisement call. This enhanced
sensitivity may represent an adaptation of the teleost auditory system to increase the
probability of mate localization and enable females to acquire acoustic information
needed for mate choice decisions.
The seasonal enhancement of hearing in female midshipman for the detection of
the higher frequency harmonics in the male social acoustic signals is likely adaptive for the shallow water acoustic environment where midshipman court and
socially interact during the breeding season. Sound propagation of low frequency
sounds in shallow water environments are greatly affected by water depth and substrate composition (Rogers and Cox 1988 ). The higher frequency harmonics of the
male’s advertisement call have been proposed to provide greater signal detection of
the male’s social acoustic signal for females because the advertisement call’s dominant harmonics (200–400 Hz) will propagate farther than the lower fundamental
frequency (~80–100 Hz) in shallow water environments due to an inverse relationship between the cutoff frequency of sound transmission and water depth (Fine and
Lenhardt 1983 ; Rogers and Cox 1988 ; Sisneros and Bass 2003 ). Substrate composition of the shallow water environment is also an important factor that affects
Neuroanatomical Evidence for Catecholamines as Modulators of Audition…