Behavioral/Systems/CognitiveSpectral Edge Sensitivity in Neural Circuits of the DorsalCochlear NucleusLina A. J. Reiss and Eric D. YoungCenter for Hearing Sciences and Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205One possible function of the dorsal cochlear nucleus (DCN) is discrimination of head-related transfer functions (HRTFs), spectral cuesused for vertical sound localization. Recent psychophysical and physiological studies suggest that steep, rising spectral edges may be thefeatures used to identify HRTFs. Here we showed, using notch noise and noise band stimuli presented over a range of frequencies, that asubclass of DCN type IV neurons responded with a response peak when the rising spectral edge of a notch or band was aligned near bestfrequency (BF). This edge sensitivity was correlated with weak or inhibited responses to broadband noise and inhibition in receptivefields at frequencies below BF. Some aspects of the inhibition shaping the response peak, namely inhibition to rising edges below BF andto falling edges at BF, could be explained by the properties of type II interneurons with BFs below those of the type IV neurons. However,many type IV neurons also showed inhibitory responses with the rising spectral edge just above BF, and these responses could not bereproduced by current models of DCN circuitry. Therefore, a new component of the DCN circuit is needed to fully explain the responsesto rising spectral edges. This shaping of edge sensitivity by inhibition to rising spectral edges both below and above BF suggests thespecialization of DCN for spectral edge coding along the tonotopic gradient.Key words: dorsal cochlear nucleus; spectral edges; spectral notches; sound localization; head-related transfer functions; DCNIntroductionSpectral sound localization cues are created by the acoustic filter-ing properties of the outer ear; the frequency-specific changes ingain from the free field to a point near the eardrum are describedby head-related transfer functions (HRTFs) (Blauert, 1969; He-brank and Wright, 1974). In cats, HRTFs are characterized by amidfrequency notch, which shifts systematically in frequencywith sound source azimuth and elevation (Musicant et al., 1990;Rice et al., 1992). This notch produces a sharp minimum in thesound spectrum at the eardrum, which is an important cue forvertical sound localization in cats (Huang and May, 1996; Tollinand Yin, 2003). Spectral notch processing has been associatedwith the dorsal cochlear nucleus (DCN) (Young and Davis, 2002;Oertel and Young, 2004) and interruption of the output axons ofthe DCN impairs the ability of behaving cats to orient to soundsources in the vertical plane (Sutherland et al., 1998; May, 2000).Recent studies raise the question of whether it is the frequencyof the notch itself or the frequency of the upper edge of the notchthat is encoded. Psychophysical experiments in human observersshow that steeply rising spectral edges can influence perceivedvertical location (Middlebrooks, 1992; Macpherson and Middle-brooks, 1999). Moreover, rising spectral edges are strongly en-coded by type O neurons in the inferior colliculus (ICC) (Davis etal., 2003). Type O neurons receive a dominant excitatory inputfrom type IV neurons in the DCN (Davis, 2001), and the edgesensitivity seen in the ICC could be derived from the DCN. TypeIV neurons receive inhibitory inputs from type II interneuronswith lower best frequencies (BFs) than the excitatory inputs totype IVs from the auditory nerve (AN) (Voigt and Young, 1990;Spirou and Young, 1991), an arrangement that could producespectral edge sensitivity.The goal of this study was to test whether DCN type IV neu-rons encode rising spectral edges and, if so, to determine whetherthe known circuitry of the DCN suffices to account for suchencoding. Previous studies explored a different hypothesis, thatspectral notches are encoded by inhibitory responses to the ab-sence of energy in the notch, based on the finding that most typeIV neurons are excited by broadband noise (BBN) but inhibitedby notches centered on BF (Spirou and Young, 1991; Nelken andYoung, 1994). These studies mainly examined the responses ofDCN type IV neurons to notch noise with the notch centered onBF, which gives no information about encoding of notches withspectral edges at BF.The data reported here show that the majority of DCN type IVneurons respond with a peak of discharge rate when a risingspectral edge is aligned near BF. This edge sensitivity is correlatedwith weak or inhibited responses to BBN and with inhibition inreceptive fields at frequencies just below BF. Some aspects of theinhibition can be explained by the properties of known DCNinhibitory circuits; however, important aspects of the responsescannot be reproduced by the current model of the DCN (Han-Received Dec. 6, 2004; revised Feb. 16, 2005; accepted Feb. 19, 2005.This work wassupported by National Institutes of Health Grants DC00115 and DC00441. Israel Nelken and KevinDavis provided archival data, which was helpful for guiding the experimental protocol, as well as one onset-C unitshown in this paper. Ian Bruce provided the auditory nerve model used for dorsal cochlear nucleus simulations. Wethank Sharba Bandyopadhyay, Steven Chase, Bradford May, and Israel Nelken for helpful comments on thismanuscript.Correspondence should be addressed to Eric D. Young, Department of Biomedical Engineering, Johns HopkinsUniversity School of Medicine, 505 Traylor Building, 720 Rutland Avenue, Baltimore, MD 21205. E-mail:[email protected]:10.1523/JNEUROSCI.4963-04.2005Copyright © 2005 Society for Neuroscience 0270-6474/05/253680-12$15.00/03680 • The Journal of Neuroscience, April 6, 2005 • 25(14):3680–3691cock and Voigt, 1999). Therefore, a new inhibitory component ofthe DCN circuit is needed to fully explain the responses to risingspectral edges.Materials and MethodsSurgical procedures. Experiments were conducted on 22 adult cats (3– 4kg) with infection-free ears and clear tympanic membranes. Animal useprotocols were approved by the Johns Hopkins Animal Care and UseCommittee. A detailed description of the surgical procedures is providedby Nelken and Young (1994). Briefly, cats were tranquilized with xylazine(2 mg, i.m.) and anesthetized with ketamine (40 mg/kg, i.m.; supplemen-tal dose, 15 mg/kg, i.m.). Atropine (0.1 mg, i.m.) was given to controlmucous secretion. Cats were decerebrated