Abstract
Sensory systems have evolved to provide animals with information about their environments. Information relayed from sensory receptors is processed in the central nervous system to yield a perception of the environment. In the vertebrate auditory system, efferent neurons originate in the brainstem and send projections to the ear, which modify the ascending information before it reaches the brain. The overall role of efferent innervation in sensory perception is poorly understood, and the efferent system remains rather enigmatic. The present studies have examined the anatomy, auditory physiology, and peripheral effects of the efferent neurons in the relatively simple ear of a teleost fish, the sleeper goby (Dormitator latifrons). The anatomy of the auditory nuclei in the brainstem, including the efferent neurons, was studied with retrograde labeling and confocal microscopy. Multiple fluorophore tracers were used to retrogradely label each of the branches of the eighth nerve and lateral line nerves. The auditory physiology of octavolateral efferent neurons was studied using single-cell recording. Efferent neurons responded omnidirectionally to stimuli and had broadly-tuned, low-pass frequency responses. This suggests that they respond generally to the presence and intensity of sounds in the environment, with little directional or frequency selectivity. The effects of efferent activity on the signal-to-noise ratio (SNR) of the auditory system as a whole were studied by stimulating efferent neurons and quantifying the SNR of tone-evoked auditory responses (compound saccular nerve potentials) before and after efferent stimulation. Efferent stimulation decreased the SNR of the responses in quiet conditions, but increased it when tones were masked by broadband noise. This suggests that efferent neurons enhance the encoding of stimuli in difficult listening conditions, where signals are partially masked by noise. These data collectively suggest that the efferent neurons provide a general feedback to the ear, which increases the SNR of the auditory system when noise levels in the environment are high and signals are likely to be masked.