The effects of intense sound exposure on phase locking in the chick (Gallus domesticus) cochlear nerve Adam C. Furman, Michael Avissar and James C. Saunders Auditory Research Laboratory, Department of Otorhinolaryngology, Head and Neck Surgery, University of Pennsylvania, 5-Ravdin- ORL, 3400 Spruce Street, Philadelphia, PA 19104, USA Keywords: chick, intense sound exposure, phase locking, synchronization, vector strength Abstract Little is known about changes that occur to phase locking in the auditory nerve following exposure to intense and damaging levels of sound. The present study evaluated synchronization in the discharge patterns of cochlear nerve units collected from two groups of young chicks (Gallus domesticus), one shortly after removal from an exposure to a 120-dB, 900-Hz pure tone for 48 h and the other from a group of non-exposed control animals. Spontaneous activity, the characteristic frequency (CF), CF threshold and a phase- locked peri-stimulus time histogram were obtained for every unit in each group. Vector strength and temporal dispersion were calculated from these peri-stimulus time histograms, and plotted against the unit’s CF. All parameters of unit responses were then compared between control and exposed units. The results in exposed units revealed that CF thresholds were elevated by 30–35 dB whereas spontaneous activity declined by 24%. In both control and exposed units a high degree of synchronization was observed in the low frequencies. The level of synchronization above approximately 0.5 kHz then systematically declined. The vector strengths in units recorded shortly after removal from the exposure were identical to those seen in control chicks. The deterioration in discharge activity of exposed units, seen in CF threshold and spontaneous activity, contrasted with the total absence of any overstimulation effect on synchronization. This suggested that synchronization arises from mechanisms unscathed by the acoustic trauma induced by the exposure. Introduction Exposure to intense and damaging levels of sound in the chicken causes considerable disruption to structure and function in the peripheral auditory system. The greatest structural damage occurs to the basilar papilla within the confines of the so called ‘patch’ lesion (Cotanche, 1987a,b, 1999). The tectorial membrane in this lesion deteriorates entirely and is accompanied by substantial abneural hair cell loss. These hair cell losses are complemented by dramatic changes in the surface areas of supporting cells and surviving hair cells (Cotanche et al., 1987; Marsh et al., 1990; Saunders et al., 1992). Marginal cells of the tegmentum vasculosum are also injured by the exposure (Askew et al., 2006). In addition, various types of damage have been reported to the hair cell sensory hair bundle, including about a 48% loss in tip-links (Erulkar et al., 1996; Husbands et al., 1999; Kurian et al., 2003) Profound post-exposure changes have been reported in the activity of cochlear nerve (auditory nerve) units (Chen et al., 1996; Saunders et al., 1996b). Shortly after removal from the exposure, discharge activity reveals, among other things, a loss in threshold sensitivity, deterioration in frequency selectivity, a lessening of spontaneous activity and a narrowing of the dynamic range of rate-level functions (Saunders et al., 1996b; Plontke et al., 1999). There is also a 63% reduction in the endocochlear potential, and changes in stereocillia physiology have also been reported following both in vivo and in vitro overstimulation (Duncan & Saunders, 2000; Szymko et al., 1995). Phase locking, a property of sound-driven discharge activity, can be identified by responses synchronized in time to a particular phase angle of a sinusoidal stimulus. This phenomenon contributes to several aspects of hearing including binaural localization and is thought to play a role in speech recognition (Geisler, 1998). Indeed, binaural hearing relies on small differences in the time of arrival at brainstem auditory nuclei, arising from discharge activity originating in the auditory nerve from each ear (Goldberg & Brown, 1969; Carr & Konishi, 1988). In addition, the periodic representation of the stimulus plays an important role in the neural representation of pitch, either through phase locking in individual neurons or through periodic discharges in ensembles of neurons (i.e. neural volleying, Wever, 1949). Time resolution or synchrony in auditory neurons of various songbirds was first reported by Konishi (1969). His results suggested that birds were ‘clearly superior to typical mammals in time resolution.’ In more recent work with avian species such as the red- winged black bird, starling or pigeon, phase locking is maintained at frequencies as high as 4.0 kHz (Sachs et al., 1980; Gleich & Narins, 1988; Hill et al., 1989; Manley et al., 1997). Remarkably, the barn owl exhibits phase locking to 10.0 kHz (Ko ¨ppl, 1997). Phase locking has also been reported for the adult chicken and synchronization to approximately 2.0 kHz was noted (Salvi et al., 1992). The effects of sound exposure on phase locking in the discharge patterns of cochlear nerve units of the chick, or any avian species, remain to be described in detail. Given the profound structural and Correspondence: Adam Furman, as above. E-mail: acfurman@mail.med.upenn.edu Received 10 May 2006, revised 22 June 2006, accepted 25 July 2006 European Journal of Neuroscience, Vol. 24, pp. 2003–2010, 2006 doi:10.1111/j.1460-9568.2006.05068.x ª The Authors (2006). Journal Compilation ª Federation of European Neuroscience Societies and Blackwell Publishing Ltd