Determinants of sound location selectivity in bat inferior colliculus: a combined dichotic and free-field stimulation study

Abstract

This study of the neural representation of sound location in the bat Pteronotus parnellii describes how the peripheral and central components of its auditory system shape the horizontal and vertical spatial selectivity of single neurons in the inferior colliculus. Pteronotus extracts spatial information from the echoes of an emitted pulse composed of four constant-frequency harmonics (30, 60, 90, and 120 kHz), each terminated by a downward frequency sweep. To quantify the intensity cues available in the echo, cochlear microphonic response thresholds were used to measure the directional selectivity of the ear and the interaural intensity level disparities (IIDs) created between ears at standardized speaker positions in the bat's frontal sound field, at frequencies in the pulse spectrum. Speaker positions where thresholds were lowest were termed the sensitive area (SA) of the ear. Positions where IID values were greater than 10 dB were termed the difference area (DA). Ear directionality exhibited a pronounced frequency dependence, both in terms of the degree of directional selectivity and the position of the SA. At the 30-kHz harmonic of the pulse, the ear was broadly directional; the SA covered most of the lower half of the ipsilateral field. The ear was highly directional at the 60- and 90-kHz harmonics. Also, the vertical position of the SA changed dramatically between 60 and 90 kHz, from the horizontal midline at 60 kHz to 40 degrees below the midline at 90 kHz. The positions of the DAs also showed a pronounced frequency dependence. The 30-kHz DA was restricted to the extreme lateral part of the frontal sound field. The 60- and 90-kHz DAs were located in the same positions as the equivalent SAs and exhibited the same difference in vertical position. The DAs of the pulse harmonics differ in both their horizontal and vertical positions; the ears thus generate pronounced binaural spectral cues, which provide two-dimensional spatial information. In the inferior colliculus, a combined paradigm of closed-field dichotic stimulation, followed by free-field stimulation, was used to document the frequency tuning and binaural response properties of single neurons and to correlate these properties with the neuron's horizontal and vertical spatial selectivity in the frontal sound field. Where a neuron responded to free-field stimulation at the lowest intensity is termed its SA. A neuron's frequency tuning primarily influenced its degree of spatial selectivity and its sensitivity in the vertical plane, reflecting the directional properties of the external ears at the neuron's best frequency.(ABSTRACT TRUNCATED AT 400 WORDS)