Abstract
Tinnitus or ringing of the ears is a subjective phantom sensation necessitating behavioral models that objectively demonstrate the existence and quality of the tinnitus sensation. The gap detection test uses the acoustic startle response elicited by loud noise pulses and its gating or suppression by preceding sub-startling prepulses. Gaps in noise bands serve as prepulses, assuming that ongoing tinnitus masks the gap and results in impaired gap detection. This test has shown its reliability in rats, mice, and gerbils. No data exists for the guinea pig so far, although gap detection is similar across mammals and the acoustic startle response is a well-established tool in guinea pig studies of psychiatric disorders and in pharmacological studies. Here we investigated the startle behavior and prepulse inhibition (PPI) of the guinea pig and showed that guinea pigs have a reliable startle response that can be suppressed by 15 ms gaps embedded in narrow noise bands preceding the startle noise pulse. After recovery of auditory brainstem response (ABR) thresholds from a unilateral noise over-exposure centered at 7 kHz, guinea pigs showed diminished gap-induced reduction of the startle response in frequency bands between 8 and 18 kHz. This suggests the development of tinnitus in frequency regions that showed a temporary threshold shift (TTS) after noise over-exposure. Changes in discharge rate and synchrony, two neuronal correlates of tinnitus, should be reflected in altered ABR waveforms, which would be useful to objectively detect tinnitus and its localization to auditory brainstem structures. Therefore, we analyzed latencies and amplitudes of the first five ABR waves at suprathreshold sound intensities and correlated ABR abnormalities with the results of the behavioral tinnitus testing. Early ABR wave amplitudes up to N3 were increased for animals with tinnitus possibly stemming from hyperactivity and hypersynchrony underlying the tinnitus percept. Animals that did not develop tinnitus after noise exposure showed the opposite effect, a decrease in wave amplitudes for the later waves P4–P5. Changes in latencies were only observed in tinnitus animals, which showed increased latencies. Thus, tinnitus-induced changes in the discharge activity of the auditory nerve and central auditory nuclei are represented in the ABR.
Highlights
Until recently, there were no reliable behavioral models to determine whether or not animals perceive the phantom sound known as tinnitus
We describe the basic features of the guinea pigs’ startle and gating and show that noise exposure results in gap-prepulse inhibition” (PPI) deficits comparable to that shown in rats
All procedures were performed in accordance with the National Institutes of Health (NIH) Guidelines for the Use and Care of Laboratory Animals (NIH publication no. 80-23) and guidelines provided by the University Committee on Use and Care of Animals of the University of Michigan
Summary
There were no reliable behavioral models to determine whether or not animals perceive the phantom sound known as tinnitus. The mammalian acoustic startle response, which is elicited by sudden, loud sound, is characterized by muscle contractions of the face, neck, limb, and back resulting in a crouching posture. Root neurons, and the lateral superior olive, which deliver startle stimulus information to the caudal pontine reticular nucleus that mediates the startle via its projections to relevant muscles (Koch, 1999). Preceding the startle stimulus 30–500 ms with a non-startle-eliciting sensory input diminishes the startle amplitude. This “prepulse inhibition” (PPI) of the startle is mediated by a gating pathway comprised of the cochlear nucleus, inferior colliculus (IC), superior colliculus, and pedunculopontine tegmental nucleus, which project to the caudal pontine reticular nucleus
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