Pupillary dilation response as an indicator of auditory discrimination in the barn owl

Abstract

The pupil of an awake, untrained, head-restrained barn owl was found to dilate in response to sounds with a latency of about 25 ms. The magnitude of the dilation scaled with signal-to-noise ratio. The dilation response habituated when a sound was repeated, but recovered when stimulus frequency or location was changed. The magnitude of the recovered response was related to the degree to which habituating and novel stimuli differed and was therefore exploited to measure frequency and spatial discrimination. Frequency discrimination was examined by habituating the response to a reference tone at 3 kHz or 6 kHz and determining the minimum change in frequency required to induce recovery. We observed frequency discrimination of 125 Hz at 3 kHz and 250 Hz at 6 kHz--values comparable to those reported by others using an operant task. Spatial discrimination was assessed by habituating the response to a stimulus from one location and determining the minimum horizontal speaker separation required for recovery. This yielded the first measure of the minimum audible angle in the barn owl: 3 degrees for broadband noise and 4.5 degrees for narrowband noise. The acoustically evoked pupillary dilation is thus a promising indicator of auditory discrimination requiring neither training nor aversive stimuli.

Stimulus-specific adaptation, habituation and change detection in the gaze control system

“…SSA in the auditory cortex or the thalamus has been reported to diminish at ISIs longer than 2 s (Ulanovsky et al 2003) or has only been studied at ISIs < 2 s (von der Behrens et al 2009;Antunes et al 2010). Therefore, we can conclude that the information about the standard is stored in memory for only about 2 s. This poses a major problem because many examples of behavioral habituation have been reported with ISIs of tens of seconds to minutes, even for short duration stimuli (Thompson and Spencer 1966;Weinberger et al 1975;Bala and Takahashi 2000;Zimmer 2006;Glanzman 2009;Dong and Clayton 2006;Valentinuzzi and Ferrari 1997). It is therefore necessary to identify a form of SSA that maintains a longer memory trace.…”

“…Behavioral habituation does not comply with the above-mentioned principle of comparable time scales. For example, in the barn owl, reflexive pupil dilation and eye movements to sequences of relatively short stimuli with ISIs of 10-13 s readily habituated and recovered when the stimulus was switched from one type to another (Bala and Takahashi 2000;Spitzer et al 2003;Netser et al 2011).…”

“…Perhaps not surprisingly, mechanisms have evolved to respond selectively to unexpected events and to trigger a series of autonomic reflexes that prepare the body for possible action (Sokolov 1963;Barry 2009). These include galvanic responses (Bradley 2009), changes in heart rate (Bradley 2009), and pupillary dilation (Bala and Takahashi 2000;Weinberger et al 1975). This wide repertoire of responses, which is remarkably preserved phylogenetically, has been termed by Pavlov as the "orienting response" (Sokolov 1963;Barry 2009).…”

“…The last stimulus is salient because just like the sound of the door knob, it represents a stimulus that is out of order in time; a tone is heard during the time in which a broadband noise is expected, therefore this type of saliency will be referred to here as temporal saliency. Both temporal and spatial saliency are perceptually privileged; they give rise to attentional capture (Tiitinen et al 1994;Posner 1980), enhanced autonomic responses (Weisbard and Graham 1971;Bala and Takahashi 2000), and enhanced neural responses (Ulanovsky et al 2003;Reches and Gutfreund 2008;Naatanen 1995;Gottlieb et al 1998). Given these similarities in the outcome, it is likely that the neural mechanisms for mapping spatial saliency overlap with the neural mechanisms for mapping temporal saliency.…”

Transient Pupil Response Is Modulated by Contrast-Based Saliency

“…Although tones are notoriously hard to localize, they are best localized at 0°azimuth and for frequencies less than ϳ1200 Hz for which the interaural time difference can be exploited (Middlebrooks and Green, 1991), even though frontback confusions likely occurred. Moreover, tonal signals have the advantage of high saliency against the white noise background of the lab environment, and have been used previously (Bala and Takahashi, 2000). Although the monkey fixated the central FP (0.5°diameter; 20 -23 cd/ m 2 ) for reward, on half the trials an auditory stimulus (100 ms pure tone at 1000 Hz generated by the Matlab software, MathWorks) was presented at 0°azimuth from a speaker located above the monitor.…”