Hierarchical differences in the encoding of sound and choice in the subcortical auditory system.

Detection of sounds is a fundamental function of the auditory system. Although studies of auditory cortex have gained substantial insight into detection performance using behaving animals, previous subcortical studies have mostly taken place under anesthesia, in passively listening animals, or have not measured performance at threshold. These limitations preclude direct comparisons between neuronal responses and behavior. To address this, we simultaneously measured auditory detection performance and single-unit activity in the inferior colliculus (IC) and cochlear nucleus (CN) in macaques. The spontaneous activity and response variability of CN neurons were higher than those observed for IC neurons. Signal detection theoretic methods revealed that the magnitude of responses of IC neurons provided more reliable estimates of psychometric threshold and slope compared with the responses of single CN neurons. However, pooling small populations of CN neurons provided reliable estimates of psychometric threshold and slope, suggesting sufficient information in CN population activity. Trial-by-trial correlations between spike count and behavioral response emerged 50-75 ms after sound onset for most IC neurons, but for few neurons in the CN. These results highlight hierarchical differences between neurometric-psychometric correlations in CN and IC and have important implications for how subcortical information could be decoded.NEW & NOTEWORTHY The cerebral cortex is widely recognized to play a role in sensory processing and decision-making. Accounts of the neural basis of auditory perception and its dysfunction are based on this idea. However, significantly less attention has been paid to midbrain and brainstem structures in this regard. Here, we find that subcortical auditory neurons represent stimulus information sufficient for detection and predict behavioral choice on a trial-by-trial basis.

Frequency selectivity in macaque monkeys measured using a notched-noise method.

The auditory system is thought to process complex sounds through overlapping bandpass filters. Frequency selectivity as estimated by auditory filters has been well quantified in humans and other mammalian species using behavioral and physiological methodologies, but little work has been done to examine frequency selectivity in nonhuman primates. In particular, knowledge of macaque frequency selectivity would help address the recent controversy over the sharpness of cochlear tuning in humans relative to other animal species. The purpose of our study was to investigate the frequency selectivity of macaque monkeys using a notched-noise paradigm. Four macaques were trained to detect tones in noises that were spectrally notched symmetrically and asymmetrically around the tone frequency. Masked tone thresholds decreased with increasing notch width. Auditory filter shapes were estimated using a rounded exponential function. Macaque auditory filters were symmetric at low noise levels and broader and more asymmetric at higher noise levels with broader low-frequency and steeper high-frequency tails. Macaque filter bandwidths (BW3dB) increased with increasing center frequency, similar to humans and other species. Estimates of equivalent rectangular bandwidth (ERB) and filter quality factor (QERB) suggest macaque filters are broader than human filters. These data shed further light on frequency selectivity across species and serve as a baseline for studies of neuronal frequency selectivity and frequency selectivity in subjects with hearing loss.

Spatial and temporal disparity in signals and maskers affects signal detection in non-human primates.

Detection thresholds for auditory stimuli (signals) increase in the presence of maskers. Natural environments contain maskers/distractors that can have a wide range of spatiotemporal properties relative to the signal. While these parameters have been well explored psychophysically in humans, they have not been well explored in animal models, and their neuronal underpinnings are not well understood. As a precursor to the neuronal measurements, we report the effects of systematically varying the spatial and temporal relationship between signals and noise in macaque monkeys (Macaca mulatta and Macaca radiata). Macaques detected tones masked by noise in a Go/No-Go task in which the spatiotemporal relationships between the tone and noise were systematically varied. Masked thresholds were higher when the masker was continuous or gated on and off simultaneously with the signal, and lower when the continuous masker was turned off during the signal. A burst of noise caused higher masked thresholds if it completely temporally overlapped with the signal, whereas partial overlap resulted in lower thresholds. Noise durations needed to be at least 100 ms before significant masking could be observed. Thresholds for short duration tones were significantly higher when the onsets of signal and masker coincided compared to when the signal was presented during the steady state portion of the noise (overshoot). When signal and masker were separated in space, masked signal detection thresholds decreased relative to when the masker and signal were co-located (spatial release from masking). Masking release was larger for azimuthal separations than for elevation separations. These results in macaques are similar to those observed in humans, suggesting that the specific spatiotemporal relationship between signal and masker determine threshold in natural environments for macaques in a manner similar to humans. These results form the basis for future investigations of neuronal correlates and mechanisms of masking.

Detection of modulated tones in modulated noise by non-human primates.

In natural environments, many sounds are amplitude-modulated. Amplitude modulation is thought to be a signal that aids auditory object formation. A previous study of the detection of signals in noise found that when tones or noise were amplitude-modulated, the noise was a less effective masker, and detection thresholds for tones in noise were lowered. These results suggest that the detection of modulated signals in modulated noise would be enhanced. This paper describes the results of experiments investigating how detection is modified when both signal and noise were amplitude-modulated. Two monkeys (Macaca mulatta) were trained to detect amplitude-modulated tones in continuous, amplitude-modulated broadband noise. When the phase difference of otherwise similarly amplitude-modulated tones and noise were varied, detection thresholds were highest when the modulations were in phase and lowest when the modulations were anti-phase. When the depth of the modulation of tones or noise was varied, detection thresholds decreased if the modulations were anti-phase. When the modulations were in phase, increasing the depth of tone modulation caused an increase in tone detection thresholds, but increasing depth of noise modulations did not affect tone detection thresholds. Changing the modulation frequency of tone or noise caused changes in threshold that saturated at modulation frequencies higher than 20 Hz; thresholds decreased when the tone and noise modulations were in phase and decreased when they were anti-phase. The relationship between reaction times and tone level were not modified by manipulations to the nature of temporal variations in the signal or noise. The changes in behavioral threshold were consistent with a model where the brain subtracted noise from signal. These results suggest that the parameters of the modulation of signals and maskers heavily influence detection in very predictable ways. These results are consistent with some results in humans and avians and form the baseline for neurophysiological studies of mechanisms of detection in noise.

Detection of tones and their modification by noise in nonhuman primates.

A fundamental function of the auditory system is to detect important sounds in the presence of other competing environmental sounds. This paper describes behavioral performance in a tone detection task by nonhuman primates (Macaca mulatta) and the modification of the performance by continuous background noise and by sinusoidally amplitude modulating signals or noise. Two monkeys were trained to report detection of tones in a reaction time Go/No-Go task using the method of constant stimuli. The tones spanned a wide range of frequencies and sound levels, and were presented alone or in continuous broadband noise (40 kHz bandwidth). Signal detection theoretic analysis revealed that thresholds to tones were lowest between 8 and 16 kHz, and were higher outside this range. At each frequency, reaction times decreased with increases in tone sound pressure level. The slope of this relationship was higher at frequencies below 1 kHz and was lower for higher frequencies. In continuous broadband noise, tone thresholds increased at the rate of 1 dB/dB of noise for frequencies above 1 kHz. Noise did not change either the reaction times for a given tone sound pressure level or the slopes of the reaction time vs. tone level relationship. Amplitude modulation of tones resulted in reduced threshold for nearly all the frequencies tested. Amplitude modulation of the tone caused thresholds for detection in continuous broadband noise to be changed by smaller amounts relative to the detection of steady-state tones in noise. Amplitude modulation of background noise resulted in reduction of detection thresholds of steady-state tones by an average of 11 dB relative to thresholds in steady-state noise of equivalent mean amplitude. In all cases, the slopes of the reaction time vs. sound level relationship were not modified. These results show that macaques have hearing functions similar to those measured in humans. These studies form the basis for ongoing studies of neural mechanisms of hearing in noisy backgrounds.