Human Auditory Detection and Discrimination Measured with the Pupil Dilation Response
Avinash D S Bala, Elizabeth A Whitchurch, Terry T Takahashi, Avinash D S Bala, Elizabeth A Whitchurch, Terry T Takahashi
Abstract
In the standard Hughson-Westlake hearing tests (Carhart and Jerger 1959), patient responses like a button press, raised hand, or verbal response are used to assess detection of brief test signals such as tones of varying pitch and level. Because of its reliance on voluntary responses, Hughson-Westlake audiometry is not suitable for patients who cannot follow instructions reliably, such as pre-lingual infants (Northern and Downs 2002). As an alternative approach, we explored the use of the pupillary dilation response (PDR), a short-latency component of the orienting response evoked by novel stimuli, as an indicator of sound detection. The pupils of 31 adult participants (median age 24 years) were monitored with an infrared video camera during a standard hearing test in which they indicated by button press whether or not they heard narrowband noises centered at 1, 2, 4, and 8 kHz. Tests were conducted in a quiet, carpeted office. Pupil size was summed over the first 1750 ms after stimulus delivery, excluding later dilations linked to expenditure of cognitive effort (Kahneman and Beatty 1966; Kahneman et al. 1969). The PDR yielded thresholds comparable to the standard test at all center frequencies tested, suggesting that the PDR is as sensitive as traditional methods of assessing detection. We also tested the effects of repeating a stimulus on the habituation of the PDR. Results showed that habituation can be minimized by operating at near-threshold stimulus levels. At sound levels well above threshold, the PDR habituated but could be recovered by changing the frequency or sound level, suggesting that the PDR can also be used to test stimulus discrimination. Given these features, the PDR may be useful as an audiometric tool or as a means of assessing auditory discrimination in those who cannot produce a reliable voluntary response.
Keywords: audiometry; auditory detection; auditory discrimination; habituation; human; involuntary response; oddball; oddball paradigm; orienting; orienting reflex; orienting response; pupil dilation; pupillometry; recovery.
Conflict of interest statement
The authors declare that they have no conflict of interest.
Figures
References
- Bala ADS, Takahashi TT. Pupillary dilation response as an indicator of auditory discrimination in the barn owl. J Comp Physiol [A] 2000;186:425–434. doi: 10.1007/s003590050442.
- Bala ADS, Spitzer MW, Takahashi TT. Prediction of auditory spatial acuity from neural images on the owl’s auditory space map. Nature. 2003;424:771–774. doi: 10.1038/nature01835.
- Bala ADS, Spitzer MW, Takahashi TT. Auditory spatial acuity approximates the resolving power of space-specific neurons. PLoS One. 2007;2:e675. doi: 10.1371/journal.pone.0000675.
- Bala ADS, Keller CH, Takahashi TT (2018) Infant hearing assessed using the Pupil Dilation Response. In: Assoc. Res. Otolaryngol. Abs, p 353
- Britten KH, Shadlen MN, Newsome WT, Movshon JA. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci. 1992;12:4745–4765. doi: 10.1523/JNEUROSCI.12-12-04745.1992.
- Carhart R, Jerger J. Preferred method for clinical determination of pure-tone thresholds. J Speech Hear Disord. 1959;24:330–345. doi: 10.1044/jshd.2404.330.
- Coombs Clyde H. Adaptation of the galvanic response to auditory stimuli. Journal of Experimental Psychology. 1938;22(3):244–268. doi: 10.1037/h0063313.
- Egan JP (1975) Signal detection theory and ROC-analysis. Academic Press, NY
- Einhäuser W, Stout J, Koch C, Carter O. Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry. Proc Natl Acad Sci U S A. 2008;105:1704–1709. doi: 10.1073/pnas.0707727105.
- Geer JH. Effect of interstimulus intervals and rest-period length upon habituation of the orienting response. J Exp Psychol. 1966;72:647–619. doi: 10.1037/h0023760.
- Granholm E, Morris SK, Sarkin AJ, et al. Pupillary responses index overload of working memory resources in schizophrenia. J Abnorm Psychol. 1997;106:458–467. doi: 10.1037/0021-843X.106.3.458.
- Gutschalk A, Micheyl C, Oxenham AJ. Neural correlates of auditory perceptual awareness under informational masking. PLoS Biol. 2008;6:1156–1165. doi: 10.1371/journal.pbio.0060138.
- Hakerem G, Sutton S. Pupillary response at visual threshold. Nature. 1966;212:485–448. doi: 10.1038/212485a0.
- Hartmann Matthias, Fischer Martin H. Pupillometry: The Eyes Shed Fresh Light on the Mind. Current Biology. 2014;24(7):R281–R282. doi: 10.1016/j.cub.2014.02.028.
- Hicks CB, Tharpe AM, Ashmead DH. Behavioral auditory assessment of young infants: methodological limitations or natural lack of auditory responsiveness? Am J Audiol. 2000;9:124–130. doi: 10.1044/1059-0889(2000/015.
- Hochmann J-R, Papeo L. The invariance problem in infancy. Psychol Sci. 2014;25:2038–2046. doi: 10.1177/0956797614547918.
- Jackson JC. Amplitude and habituation of the orienting reflex as a function of stimulus intensity. Psychophysiology. 1974;11:647–659. doi: 10.1111/j.1469-8986.1974.tb01133.x.
- Johnson DA. Pupillary responses during a short-term memory task: cognitive processing, arousal, or both? J Exp Psychol. 1971;90:311–318. doi: 10.1037/h0031562.
- Kahneman D. A perspective on judgment and choice: mapping bounded rationality. Am Psychol. 2003;58:697–720. doi: 10.1037/0003-066X.58.9.697.
- Kahneman D, Beatty J. Pupil diameter and load on memory. Science 80- 1966;154:1583–1585. doi: 10.1126/science.154.3756.1583.
- Kahneman D, Tursky B, Shapiro D, Crider A. Pupillary, heart rate, and skin resistance changes during a mental task. J Exp Psychol. 1969;79:164–167. doi: 10.1037/h0026952.
- Koelewijn T, Zekveld AA, Festen JM, Kramer SE. Pupil dilation uncovers extra listening effort in the presence of a single-talker masker. Ear Hear. 2012;33:291–300. doi: 10.1097/AUD.0b013e3182310019.
- Koelewijn T, Shinn-Cunningham BG, Zekveld AA, Kramer SE. The pupil response is sensitive to divided attention during speech processing. Hear Res. 2014;312:114–120. doi: 10.1016/j.heares.2014.03.010.
- Levine FM, Whitney N. Absolute auditory threshold and threshold of unpleasantness of chronic schizophrenic patients and normal controls. J Abnorm Psychol. 1970;75:74–77. doi: 10.1037/h0028809.
- Liberman AE, et al. Some new data on the pupillary component in man. In: Voronin LG, Leontiev AN, Luria AR, et al., editors. Orienting reflex and exploratory behavior. Moscow: The Academy of Pedagogical Sciences of the RSFSR; 1958. pp. 187–194.
- McLaren JW, Erie JC, Brubaker RF (1992) Computerized analysis of pupillograms in studies of alertness. Investig Ophthalmol Vis Sci 33:671-676
- Northern J, Downs M. Hearing in children. 5. Philadelphia: Lippincott Williams & Wilkins; 2002.
- O’Gorman JG. The orienting reflex: novelty or significance detector? Psychophysiology. 1979;16:253–262. doi: 10.1111/j.1469-8986.1979.tb02988.x.
- Olsho LW, Koch EG, Halpin CF, Carter EA. An observer-based psychoacoustic procedure for use with young infants. Dev Psychol. 1987;23:627–640. doi: 10.1037/0012-1649.23.5.627.
- Raisig S, Welke T, Hagendorf H, van der Meer E. I spy with my little eye: detection of temporal violations in event sequences and the pupillary response. Int J Psychophysiol. 2010;76:1–8. doi: 10.1016/j.ijpsycho.2010.01.006.
- Richer F, Silverman C, Beatty J. Response selection and initiation in speeded reactions: a pupillometric analysis. J Exp Psychol Hum Percept Perform. 1983;9:360–370. doi: 10.1037/0096-1523.9.3.360.
- Shakhar GB, Lieblich I, Kugelmass S. Detection of information and GSR habituation: an attempt to derive detection efficiency from two habituation curves. Psychophysiology. 1975;12:283–288. doi: 10.1111/j.1469-8986.1975.tb01291.x.
- Simon EB. Primacy effect in orienting responses to auditory stimuli of tones and music. Percept Mot Ski. 1976;42:919–928. doi: 10.2466/pms.1976.42.3.919.
- Sokolov EN, et al. The orienting reflex, its structure and mechanisms. In: Voronin LG, Leontiev AN, Luria AR, et al., editors. Orienting reflex and exploratory behavior. Moscow: Publishing House of The Academy of Pedagogical Sciences of RSFR; 1958. pp. 141–153.
- Sokolov EN. Higher nervous functions: the orienting reflex. Annu Rev Physiol. 1963;25:545–580. doi: 10.1146/annurev.ph.25.030163.002553.
- Spitzer MW, Bala ADS, Takahashi TT. Auditory spatial discrimination by barn owls in simulated echoic conditions. J Acoust Soc Am. 2003;113:1631–1645. doi: 10.1121/1.1548152.
- Steel Morrison M., Papsin Blake C., Gordon Karen A. Binaural Fusion and Listening Effort in Children Who Use Bilateral Cochlear Implants: A Psychoacoustic and Pupillometric Study. PLOS ONE. 2015;10(2):e0117611. doi: 10.1371/journal.pone.0117611.
- Unsworth N, Robison MK. Individual differences in the allocation of attention to items in working memory: evidence from pupillometry. Psychon Bull Rev. 2015;22:757–765. doi: 10.3758/s13423-014-0747-6.
- van Olst E. The orienting reflex. The Hague: Mouton & Co.; 1971.
- Winn MB, Edwards JR, Litovsky RY. The impact of auditory spectral resolution on listening effort revealed by pupil dilation. Ear Hear. 2015;36:e153–e165. doi: 10.1097/AUD.0000000000000145.
- Zekveld AA, Heslenfeld DJ, Johnsrude IS, et al. The eye as a window to the listening brain: neural correlates of pupil size as a measure of cognitive listening load. Neuroimage. 2014;101:76–86. doi: 10.1016/j.neuroimage.2014.06.069.
Source: PubMed