377
4 Do Modifi cations of Inner Ear Morphology Relate
to Hearing Improvements?
From a functional perspective, one might ask for the physiological meaning of the
“invention” of horizontal orientation groups of ciliary bundles on the macula sacculi. The combination of vertical and horizontal groups was explained as an adaptation for localizing sound sources, independently achieved by ciliary bundles that
follow the curvature of the macula in non-teleost actinopterygians and lungfi shes or
the “invention” of true horizontal groups in teleosts (Platt and Popper 1981a ; Popper
and Northcutt 1983 ). Experimental data indicate that differently oriented ciliary
bundles are stimulated to different degrees depending on the location of the sound
source, i.e. the angle between ciliary bundle orientation and the direction of the
acoustic stimuli (Lu et al. 1998 ).
But how do otophysans and mormyrids that possess only vertical groups on the
macula sacculi infer directional clues? A study on the goldfi sh indicated that also
the macula lagenae and the macula utriculi detect directional information (Fay
1984 ). This was confi rmed by detailed investigations of the non-otophysan
Dormitator latifrons (Gobiiformes) which revealed a strong relationship between
the orientation patterns of ciliary bundles on the macula lagenae and macula utriculi
with the preferred best response axes of the afferent fi bers of the lagena and the
utricle (Lu et al. 2003 , 2004 ). Large lagenae in otophysans (and possibly also in
mormyrids) may thus have evolved for sound source localization, whereas the saccule is specialized to detect low-pressure sounds indicating a division of labor
between these two end organs (Popper and Platt 1983 ). Several non-otophysans
with ancillary auditory structures show a remarkable complex structuring of the
macula into several distinct regions which are completely separated (see the tripartite macula utriculi in clupeiform fi sh, Fig. 4c ) or interconnected by thin epithelial
bridges (e.g., the trilobate macula sacculi in Chitala chitala , Fig. 5a or the bilobate
macula sacculi in Antimora rostrata , Fig. 5b ) in 2D or through a distinct 3D shape
in which certain regions are out-of plane compared to the remaining macula (e.g.,
macula sacculi in Bairdiella chrysoura , Fig. 5d ). It is tempting to speculate whether
this structuring might refl ect division of labor within the macula which accounts for
stimulation via particle motion originating directly from the sound source vs. reradiated particle motion from the swim bladder. Future studies may tackle the questions of how and when these “separated” macula regions develop during ontogeny
and whether these maculae show specialized innervation patterns. Modeling of the
stimulation of the different macula regions may shed light on this distinct macula
structuring.
Certain modifi ed orientation patterns—mainly on the macula sacculi—may have
evolved to enhance hearing together with ancillary auditory structures. Apparently,
species with ancillary auditory structures, which mostly correlate with improved
hearing (Ladich and Popper 2004 ; Braun and Grande 2008 ; Ladich and Fay 2013 ;
Ladich 2014a ), often display modifi ed orientation patterns on the maculae, mainly
on the macula sacculi (Platt and Popper 1981a ). This is evident in the vertical pattern
Diversity of Inner Ears in Fishes: Possible Contribution Towards Hearing…
4 Do Modifi cations of Inner Ear Morphology Relate
to Hearing Improvements?
From a functional perspective, one might ask for the physiological meaning of the
“invention” of horizontal orientation groups of ciliary bundles on the macula sacculi. The combination of vertical and horizontal groups was explained as an adaptation for localizing sound sources, independently achieved by ciliary bundles that
follow the curvature of the macula in non-teleost actinopterygians and lungfi shes or
the “invention” of true horizontal groups in teleosts (Platt and Popper 1981a ; Popper
and Northcutt 1983 ). Experimental data indicate that differently oriented ciliary
bundles are stimulated to different degrees depending on the location of the sound
source, i.e. the angle between ciliary bundle orientation and the direction of the
acoustic stimuli (Lu et al. 1998 ).
But how do otophysans and mormyrids that possess only vertical groups on the
macula sacculi infer directional clues? A study on the goldfi sh indicated that also
the macula lagenae and the macula utriculi detect directional information (Fay
1984 ). This was confi rmed by detailed investigations of the non-otophysan
Dormitator latifrons (Gobiiformes) which revealed a strong relationship between
the orientation patterns of ciliary bundles on the macula lagenae and macula utriculi
with the preferred best response axes of the afferent fi bers of the lagena and the
utricle (Lu et al. 2003 , 2004 ). Large lagenae in otophysans (and possibly also in
mormyrids) may thus have evolved for sound source localization, whereas the saccule is specialized to detect low-pressure sounds indicating a division of labor
between these two end organs (Popper and Platt 1983 ). Several non-otophysans
with ancillary auditory structures show a remarkable complex structuring of the
macula into several distinct regions which are completely separated (see the tripartite macula utriculi in clupeiform fi sh, Fig. 4c ) or interconnected by thin epithelial
bridges (e.g., the trilobate macula sacculi in Chitala chitala , Fig. 5a or the bilobate
macula sacculi in Antimora rostrata , Fig. 5b ) in 2D or through a distinct 3D shape
in which certain regions are out-of plane compared to the remaining macula (e.g.,
macula sacculi in Bairdiella chrysoura , Fig. 5d ). It is tempting to speculate whether
this structuring might refl ect division of labor within the macula which accounts for
stimulation via particle motion originating directly from the sound source vs. reradiated particle motion from the swim bladder. Future studies may tackle the questions of how and when these “separated” macula regions develop during ontogeny
and whether these maculae show specialized innervation patterns. Modeling of the
stimulation of the different macula regions may shed light on this distinct macula
structuring.
Certain modifi ed orientation patterns—mainly on the macula sacculi—may have
evolved to enhance hearing together with ancillary auditory structures. Apparently,
species with ancillary auditory structures, which mostly correlate with improved
hearing (Ladich and Popper 2004 ; Braun and Grande 2008 ; Ladich and Fay 2013 ;
Ladich 2014a ), often display modifi ed orientation patterns on the maculae, mainly
on the macula sacculi (Platt and Popper 1981a ). This is evident in the vertical pattern
Diversity of Inner Ears in Fishes: Possible Contribution Towards Hearing…