G. Ter Haar, DVM, DECVS
Dr. Purves described the auditory system as one of the engineering masterpieces of the human body with an array of miniature acoustical detectors packed into a space no larger than a pea1. Although humans are highly visual creatures, much of the human communication is mediated by the auditory system and indeed, deafness can be more debilitating than blindness. It is much more difficult to establish the effect and impact of hearing loss or even deafness in dogs. Just extrapolating what is known for men to dogs, probably does not do justice to the incredible sensitivity and specificity of the canine cochlea. Judging hearing in humans can be relatively straightforward with behavioral tests or more objectively with electrophysiological tests. People can describe their own sensation of hearing or the lack of it. Judging hearing in dogs is much more complicated, even though objective hearing assessment is possible nowadays. These techniques however only allow for verification of morphologic integrity of the auditory system, but sound awareness cannot be appreciated with these methods. It has to be kept in mind that hearing itself is a much more complex phenomenon then can be appreciated from hearing assessment tests used in animals. Clinically relevant information can be obtained however with the methods described later on.
Anatomy & Physiology
The external ear and the middle ear form collectively, a mechanical transmission system that converts sound, or air pressure waves, into fluid waves in the inner ear1,2. The external ear, the pinna, in dogs can easily be moved towards the origin of a sound and gathers the sound energy and focuses it on the eardrum. The major function of the middle ear is to match relatively low impedance airborne sounds to the higher impedance fluid of the inner ear. The sensory transduction occurs in the organ of Corti, which is situated in the scala media en separated from the scala vestibuli and the scala tympani by reissner's membrane and the basilar membrane respectively. It is here where the hair cells interact with supporting elements to convert fluid waves into the bending of hair bundles and resultant ion influxes. The release of neurotransmitter from the basal portions of stimulated hair cells leads to neural impulses, action potentials. Once the nerve impulse is generated in the cochlea, the signal travels along the acoustic nerve to the cochlear nuclei. From here, many projections lead to the olivary nuclei at the same level. The axons of the olivary neurons project via the lateral lemniscus to the inferior colliculi, where they synapse on neurons that project to the primary auditory cortex1,2.
When people speak of sound, they are usually referring to pressure waves generated by vibrating air molecules. Sound waves propagate in three dimensions, creating spherical shells of alternating compression and rarefaction. Like all wave phenomena, sound waves have four major features: waveform, phase, amplitude and frequency1,2. These four determine our perception of sound, especially the frequency and amplitude of the waves. Sounds composed of single sine waves are however extremely rare in nature, most sounds consist of acoustically complex waveforms.
The frequency of a sound, expressed in cycles per second or Hertz roughly corresponds to the pitch of a sound, whereas the amplitude, usually expressed in decibels, determines the loudness of a sound. By changing the frequency and/or amplitude of a sound, a different stimulation of the ear and thus perception, will occur. The receptors, the hair cells, act like miniature amplifiers, each tuned mechanically by shape and function to provide a maximal electrical response when vibrated at a particular frequency by the fluid waves of the inner ear. Along the cochlea, all small groups of hair cells have their own specific frequency by which they are stimulated maximally. The hair cells are thus a set of frequency filters, ordered spatially within the cochlea; those with high-pass frequencies occupy the base and those with low-pass frequencies occupy the apex1,2.
Therefore, a sound with a high frequency will cause maximal displacement of a portion of the basilar membrane at the base of the cochlea. The greater the displacement of the basilar membrane, the more sensory receptor and neurons that are stimulated, leading to increased sound intensity. A sound wave with a higher amplitude leads to a greater basilar membrane displacement. A sound with a low frequency causes displacement of a more apical situated portion of the cochlea.
Several methods have been employed to test hearing ability in dogs, ranging from behavioural studies to measurement of electrical responses after auditory stimulation, using impedance audiometry (tympanometry, acoustic reflex testing), evoked response audiometry (brainstem (BAER) and middle latency (MLAER) auditory evoked responses), and cochlear microphony3,4,5,6. The brain responds to auditory stimuli by consistent changes in electrical activity and these changes can be recorded from scalp electrodes. It is generally agreed that the recorded brainstem evoked potentials represent the passage of auditory input from the inner ear through the various structures of the brainstem towards the auditory cortex3.
The specific type of recording depends on the length of time that is averaged after the stimulus has been given. The time between stimulus onset and response is called latency. For the early latency components, meaning the responses recorded between 0 en 10 milliseconds after the stimulus, generators are thought to arise almost totally within the brainstem. Therefore, this series of waves is referred to as the brainstem auditory evoked responses. Jewett and Williston were the first to describe the series of 7 peaks following auditory stimulation in the early seventies, hence they are now referred to as the "Jewett bumps"3,7.
The last two decades, brainstem auditory evoked responses have been used increasingly to test hearing ability in veterinary medicine3,4. The acoustic signal usually consisted of a click stimulus, which stimulates a large part of the cochlea. Brainstem evoked response audiometry using clicks will suffice for differentiating neurologic from conduction deafness and is of use in assessing some brainstem pathologic changes. Frequency-specific information, however, is needed in assessing the extent of neurologic deafness, e.g., noise-induced deafness, deafness caused by ototoxicity and presbycusis, which can all be partial and frequency-specific6.
Aim of the Study6
A method was developed to deliver tone bursts ranging in frequency from 1-32 kHz for frequency-specific assessment of the canine cochlea. Our aim was to collect reference values for BAER wave (peak) latencies, interpeak latencies, amplitudes, amplitude-ratio's and thresholds in response to both click and tone burst stimulation for a more complete assessment of thresholds of hearing in dogs.
Animals, Materials & Methods6
Brainstem auditory evoked responses (early latency responses, 0-10 ms) to a click (CS) and to 1, 2, 4, 8, 12, 16, 24, and 32 kHz tone burst stimulations (TS) were compared at 80 dB sound pressure level stimulus intensity in 10 clinically-healthy dogs, 3.5 to 7.0 years of age (mean, 5.7 years) weighing 12.5 to 21.3 kg (mean, 17.8 kg). The responses were obtained with the animals under a light plane of anaesthesia.
All stimulations yielded a 5-7 positive wave pattern, with the exception of the 1 kHz TS, which evoked a frequency-following response. Thresholds were lowest for CS, 12, and 16 kHz TS. All individual peak latencies for TS were significantly (P < 0.05) longer than for CS. Peak I latencies were significantly (P < 0.05) shorter for 12 and 16 kHz TS than for other TS. Interpeak latencies I-V were significantly (P < 0.05) longer for 4-32 kHz TS than for CS. Differences in interpeak latencies I-III were not significant. Amplitudes of waves I and V were significantly (P < 0.05) lower for TS than for CS, except for higher wave V amplitude (P < 0.05) at 2 and 32 kHz TS. Peak I-Peak V amplitude ratios were significantly (P < 0.05) higher for 2, 4, 16, 24, and 32 kHz TS and lower for 8 and 12 kHz TS, compared to CS.
It is concluded that specific tone burst stimulation of the canine cochlea using low to high frequencies yields reproducible results and that results are in agreement with results of behavioral studies on frequency thresholds and hearing sensitivity in dogs. For testing hearing in terms of sound intensity (dB) in dogs, CS is sufficient. In addition, to determine the extent of neurological damage due to ototoxic drugs, presbycusis, or noise, frequency-specific assessment should be done. Our report provides a normative database for parameters necessary to evaluate frequency-specific hearing losses in dogs, but does not, however, give any information on sound perception in dogs, which is impossible to judge. These results do show however that dogs are capable of hearing a much wider range of frequencies then humans, thus it is clear that their perception of sounds must be very different from our own perception.
From a cultural perspective, the human auditory system is essential not only to language, but also to music. Whether or not dogs appreciate our music, we don't know, but we do know that dogs have an even more developed auditory system then humans.
1. Purves D. The auditory system. In: Purves D, Augustine GJ, Fitzpatrick D, et al, ed. Neuroscience. Sunderland, MA: Sinauer Associates; 1997:223-243.
2. Møller AR. Hearing; It's physiology and pathophysiology, California (2000), pp. 1-93.
3. Sims MH. Electrodiagnostic Evaluation of auditory function. Vet Clin North Am Small Anim Pract 1988;18:913-944.
4. Venker-van Haagen AJ, Siemelink RJG and Smoorenburg GF. Auditory brainstem responses in the normal beagle. Vet Quart 1989;11:129-137.
5. Heffner HE. Hearing in Large and Small Dogs: Absolute Thresholds and Size of the Tympanic Membrane. Behav Neurosci 1983;97:310-318.
6. Ter Haar G, Venker-van Haagen AJ, de Groot HNM and van den Brom WE. Click and Low-, Middle-, and High-Frequency Toneburst Stimulation of the Canine Cochlea. J Vet Intern Med 2002;16:274-280.
7. Jewett DL and Williston JS. Auditory-evoked far field averaged from the scalp of humans. Brain 1971;94:681-696.