A comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in Lemur catta and Nycticebus coucang

Abstract

Primates depend on acoustic signals and cues to avoid predators, locate food, and share information. Accordingly, the structure and function of acoustic stimuli have long been emphasized in studies of primate behavioral and cognitive ecology. Yet, few studies have addressed how well primates hear such stimuli; indeed, the auditory thresholds of most primate species are unknown. This empirical void is due in part to the logistic and economic challenges attendant on traditional behavioral testing methods. Technological advances have produced a safe and cost-effective alternative-the auditory brainstem response (ABR) method, which can be utilized in field conditions, on virtually any animal species, and without subject training. Here we used the ABR and four methods of threshold determination to construct audiograms for two strepsirrhine primates: the ring-tailed lemur (Lemur catta) and slow loris (Nycticebus coucang). Next, to verify the general efficacy of the ABR method, we compared our results to published behaviorally-derived audiograms. We found that the four ABR threshold detection methods produced similar results, including relatively elevated thresholds but similarly shaped audiograms compared to those derived behaviorally. The ABR and behavioral absolute thresholds were significantly correlated, and the frequencies of best sensitivity and high-frequency limits were comparable. However, at frequencies < or =2 kHz, ABR thresholds were especially elevated, resulting in decreased agreement with behavioral thresholds and, in Lemur, the ABR 10-dB range starting points were more than 2 octaves higher than the behavioral points. Finally, a comparison of ABR- and behaviorally-derived audiograms from various animal taxa demonstrates the widespread efficacy of the ABR for estimating frequency of best sensitivity, but otherwise suggests caution; factors such as stimulus properties and threshold definition affect results. We conclude that the ABR method is a promising technique for estimating primate hearing sensitivity, but that additional data are required to explore its efficacy for estimating low-frequency thresholds.

Social drive and the evolution of primate hearing

“…The ABR method is thus a viable alternative to traditional behavioural methods that require months of training in laboratory settings. Importantly, common parameters of auditory sensitivity such as the frequency of best sensitivity and the high-frequency limit are comparable between the two methods [29].…”

“…To estimate the hearing sensitivities of primates, we used the auditory brainstem response (ABR) method [29]. In this minimally invasive method, brief tones are used to evoke neural activity from the ascending auditory pathway that is recorded with sensory electrodes placed on the scalp [30,31].…”

“…The use of such anaesthetics during the ABR testing has been common across a wide variety of animals, and short-term exposure (i.e. 1 h) does not affect thresholds significantly [29]. The body temperatures of the animals were monitored and controlled with blankets and electric heating pads; after the procedure, all animals were returned to their enclosures unharmed and then monitored.…”

“…(b) Data analysis (i) Auditory brainstem response thresholds and parameters For each frequency, we used a linear regression method [29] to determine the auditory threshold (quietest detectable level). We set the criterion at 77 mV (average encephalographic background noise þ 40 mV); at this level, the ABR was consistently distinct above random fluctuations in background noise (see example of an ABR waveform series in electronic supplementary material, figure S2b).…”

“…We calculated the 60 dB high-frequency limits (table 2) mathematically on the basis of thresholds reported in the original sources. The 60 dB highfrequency limit is comparable between ABR-and behaviourally derived datasets [29]; however, at lower frequencies, absolute threshold levels may differ between methodologies [29]. We, therefore, omitted any consideration of absolute threshold level (i.e.…”