Tympanic-membrane and malleus-incus-complex co-adaptations for high-frequency hearing in mammals

The development of the unique capacity for high-frequency hearing in many mammals was due in part to changes in the middle ear, such as the evolution of three distinct middle-ear bones and distinct radial and circumferential collagen fiber layers in the eardrum. Ossicular moment(s) of inertia (MOI) and principal rotational axes, as well as eardrum surface areas, were calculated from micro-CT-based 3-D reconstructions of human, cat, chinchilla, and guinea pig temporal bones. For guinea pig and chinchilla, the fused malleus-incus complex rotates about an anterior-posterior axis, due to the relatively lightweight ossicles and bilateral symmetry of the eardrum. For human and cat, however, the MOI calculated for the unfused malleus are 5-6 times smaller for rotations about an inferior-superior axis than for rotations about the other two orthogonal axes. It is argued that these preferred motions, along with the presence of a mobile malleus-incus joint and asymmetric eardrum, enable efficient high-frequency sound transmission in spite of the relatively large ossicular masses of these species. This work argues that the upper-frequency hearing limit of a given mammalian species can in part be understood in terms of morphological co-adaptations of the eardrum and ossicular chain.