The earliest vertebrate ears likely subserved a gravistatic function for orientation in the aquatic environment. However, in addition to detecting acceleration created by the animal's own movements, the otolithic end organs that detect linear acceleration would have responded to particle movement created by external sources. The potential to identify and localize these external sources may have been a major selection force in the evolution of the early vertebrate ear and in the processing of sound in the central nervous system. The intrinsic physiological polarization of sensory hair cells on the otolith organs confers sensitivity to the direction of stimulation, including the direction of particle motion at auditory frequencies. In extant fishes, afferents from otolithic end organs encode the axis of particle motion, which is conveyed to the dorsal regions of first-order octaval nuclei. This directional information is further enhanced by bilateral computations in the medulla and the auditory midbrain. We propose that similar direction-sensitive neurons were present in the early aquatic tetrapods and that selection for sound localization in air acted upon preexisting brain stem circuits like those in fishes. With movement onto land, the early tetrapods may have retained some sensitivity to particle motion, transduced by bone conduction, and later acquired new auditory papillae and tympanic hearing. Tympanic hearing arose in parallel within each of the major tetrapod lineages and would have led to increased sensitivity to a broader frequency range and to modification of the preexisting circuitry for sound source localization.

Responses of cells in the toadfish medulla (descending octaval nucleus: DON) and midbrain (torus semicircularis: TS) were studied to investigate binaural interaction and processing. Normally, the two ears of fish cannot be stimulated independently. A method was developed to temporarily inactivate one ear by slightly displacing the saccular otolith on one side (tipping) to change its orientation in space and, therefore, alter the responsiveness of the hair cells. Brain cells were evaluated for directional characteristics and frequency response (1) before otolith tipping, (2) with the otolith tipped, and (3) post-tipping. For DON cells (n=14), contralateral saccular otolith tipping most often resulted in subtle effects consisting of an overall change in responsiveness (±spikes/sec); significant changes in the preferred direction were rare. In the TS (n=20), most cells exhibited changes in responsiveness and in directionality. These experiments demonstrate the existence of excitatory and inhibitory binaural interactions in the medulla and midbrain and show rather complex and unexpected binaural effects on the responsiveness and directional properties of auditory brain cells. [Work supported by the NIH/NIDCD.]