Suboptimal Use of Neural Information in a Mammalian Auditory System

Abstract

Establishing neural determinants of psychophysical performance requires both behavioral and neurophysiological metrics amenable to correlative analyses. It is often assumed that organisms use neural information optimally, such that any information available in a neural code that could improve behavioral performance is used. Studies have shown that detection of amplitudemodulated (AM) auditory tones by humans is correlated to neural synchrony thresholds, as recorded in rabbit at the level of the inferior colliculus, the first level of the ascending auditory pathway where neurons are tuned to AM stimuli. Behavioral thresholds in rabbit, however, are ϳ10 dB higher (i.e., 3 times less sensitive) than in humans, and are better correlated to rate-based than temporal coding schemes in the auditory midbrain. The behavioral and physiological results shown here illustrate an unexpected, suboptimal utilization of available neural information that could provide new insights into the mechanisms that link neuronal function to behavior.

Neural correlates of behavioral amplitude modulation sensitivity in the budgerigar midbrain

“…Behavioral sensitivity to AM tones has been studied previously in humans and rabbits (Carney et al 2014) Fig. 3.…”

“…The solid black line shows AM thresholds averaged across birds. Also shown are previously published (Carney et al 2014) average behavioral thresholds of humans (dotted black line) and rabbits (solid gray line) obtained with the same single-interval, 2-alternative behavioral task and similar stimulus parameters (carrier frequency: 5 kHz; level: 50 dB SPL; duration: 500 ms). Shaded gray regions show Ϯ1 SD from the mean.…”

“…The finding that behavioral thresholds for AM detection are ϳ10 dB more sensitive in the budgerigar than in the rabbit raises the question of how thresholds of the IC compare between these two species. Neural AM thresholds in the rabbit were recalculated from an existing dataset of IC single-unit and multiunit neural recordings (Carney et al 2014) using the same rate-and synchrony-based (VS PP ) analyses used here. In general, rate and synchrony thresholds were similar between budgerigar and rabbits for both carrier types, up to the maximum modulation frequency studied in the rabbit, 256 Hz (Fig.…”

“…The relationship between behavioral and IC sensitivity to AM in the same animal model has been examined previously in a single species-the rabbit-which has limited behavioral sensitivity to AM (Carney et al 2014). The rabbit study used receiver-operating characteristic (ROC) analyses (Egan 1975) to calculate thresholds for AM detection (i.e., minimum detectable modulation depths) across a population of IC neurons, based on both average discharge rate and envelope synchrony, for comparison with behavioral thresholds obtained with operant conditioning procedures.…”

“…However, the mechanisms underlying AM perception in species with more sensitive auditory perceptual abilities are unexplored. Human listeners may use envelope synchrony of IC responses to achieve greater AM sensitivity than rabbits (Carney et al 2014;Nelson and Carney 2007). Alternatively, rate-based AM thresholds in the human IC may be more sensitive than in the rabbit and therefore able to support superior behavioral performance.…”