Behavioral/Systems/CognitiveA Physiologically Based Model of Interaural Time DifferenceDiscriminationKenneth E. Hancock1and Bertrand Delgutte1,21Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts 02114, and2Research Laboratory of Electronics, MassachusettsInstitute of Technology, Cambridge, Massachusetts 02143Interaural time difference (ITD) is a cue to the location of sounds containing low frequencies and is represented in the inferior colliculus(IC) by cells that respond maximally at a particular best delay (BD). Previous studies have demonstrated that single ITD-sensitive cellscontain sufficient information in their discharge patterns to account for ITD acuity on the midline (ITD ⫽ 0). If ITD discrimination werebased on the activity of the most sensitive cell available (“lower envelope hypothesis”), then ITD acuity should be relatively constant as afunction of ITD. In response to broadband noise, however, the ITD acuity of human listeners degrades as ITD increases. To account forthese results, we hypothesize that pooling of information across neurons is an essential component of ITD discrimination. This reportdescribes a neural pooling model of ITD discrimination based on the response properties of ITD-sensitive cells in the IC of anesthetizedcats.Rate versus ITD curves were fit with a cross-correlation model of ITD sensitivity, and the parameters were used to constrain apopulation model of ITD discrimination. The model accurately predicts ITD acuity as a function of ITD for broadband noise stimuli whenresponses are pooled across best frequency (BF). Furthermore, ITD tuning based solely on a system of internal delays is not sufficient topredict ITD acuity in response to 500 Hz tones, suggesting that acuity is likely refined by additional mechanisms. The physiological dataconfirms evidence from the guinea pig that BD varies systematically with BF, generalizing the observation across species.Key words: auditory; binaural; hearing; inferior colliculus; localization; psychophysicsIntroductionA fundamental question in neuroscience concerns the num-ber of neurons used by the CNS to make sensory judgments(Parker and Newsome, 1998). Comparisons of neural responseproperties to psychophysical performance have led to two generalmodels of neural coding. The lower envelope hypothesis applieswhen the firing pattern of a single neuron accounts for sensoryjudgments related to a particular stimulus (Parker and Newsome,1998). For example, vibration detection thresholds for humansubjects are quantitatively similar to the lowest response thresh-olds exhibited by primary somatosensory afferents over a widerange of stimulus frequencies (Mountcastle et al., 1972). In othercases, a neural pooling model better accounts for psychophysicalperformance. For example, the smallest discriminable change ininterocular disparity, on which depth perception is based, in-creases with the base disparity at which it is measured (Badcockand Schor, 1985). This is inconsistent with the use of the mostsensitive neurons in cortical areas V1 and V2 because these neu-rons are highly sensitive to changes in disparity regardless of thebase disparity to which they are tuned (Poggio and Fischer, 1977).Interocular disparity discrimination is more consistent with amodel in which psychophysical judgments are based on thepooled responses of neurons tuned to many different base dis-parities (Lehky and Sejnowski, 1990).Neural pooling is also an issue in the context of the discrimi-nation of interaural time difference (ITD), a dominant cue to thelocation of sounds containing low-frequency components(Wightman and Kistler, 1992; Macpherson and Middlebrooks,2002). In response to 500 Hz tones, the just noticeable difference(JND) in ITD is nearly constant at 10␮sec as a function of ITD(Domnitz and Colburn, 1977). For broadband noise, however,the JND is three to four times larger and systematically increasesas ITD increases (Mossop and Culling, 1998).Previous studies have shown that ITD acuity near the midlineis consistent with the responses of single ITD-sensitive inferiorcolliculus (IC) neurons (Skottun et al., 2001; Shackleton et al.,2003). Because IC neurons are tuned to a wide range of ITDs,application of the lower envelope hypothesis to ITD discrimina-tion predicts uniform acuity for all ITDs. However, this contra-dicts the observation that ITD JNDs in response to broadbandnoise systematically increase with ITD (Mossop and Culling,1998). We hypothesized that a neural pooling model might betteraccount for ITD acuity in general and developed such a modelbased on the physiological response properties of ITD-sensitivecells in the cat IC. We first developed a version of the cross-correlator model (Colburn, 1973) that can be fit efficiently toReceived March 2, 2004; revised June 22, 2004; accepted June 23, 2004.ThisworkwassupportedbyNationalInstituteonDeafnessandOtherCommunicationDisordersGrantsDC00119,DC02258, and DC05295. We thank Leslie Liberman and Connie Miller for surgical support and the two anonymousreviewers for their helpful comments.Correspondence shouldbeaddressedtoKennethE. Hancock,Eaton-PeabodyLaboratory,MassachusettsEyeandEar Infirmary, 243 Charles Street, Boston, MA 02114. E-mail: [email protected]:10.1523/JNEUROSCI.0762-04.2004Copyright © 2004 Society for Neuroscience 0270-6474/04/247110-08$15.00/07110 • The Journal of Neuroscience, August 11, 2004 • 24(32):7110 –7117single-unit rate–ITD curves. The parameters derived from thedata were then used to constrain a population model of ITDdiscrimination. The population model accurately predicts ITDacuity as a function of ITD for broadband noise when responsesare first pooled across best frequency (BF). It appears that theauditory system places a premium on the consistency of ITDinformation across frequency (Stern et al., 1988) at the expense ofITD acuity on the periphery.Materials and MethodsPhysiological methods. Adult cats were anesthetized with intraperitonealinjections of dial-in urethane (diallylbarbituric acid; 75 mg/kg; Sigma, St.Louis, MO) and secured on a stereotaxic apparatus inside an electricallyshielded, double-walled sound-attenuating chamber. The inferior col-liculi were visualized by opening the posterior fossa and partially aspirat-ing the cerebellum. Single units were isolated using parylene-insulatedtungsten microelectrodes (Micro Probe, Potomac, MD).Acoustic stimuli were generated at a sampling