Human auditory steady state responses to binaural and monaural beats
Introduction
Two simultaneous pure tone stimuli of frequencies within the same critical band (Fletcher, 1940, Greenwood, 1961a, Greenwood, 1961b, Moore, 2003) may be heard as one tone with a pitch at the mean frequency of both inputs, beating at a rate equal to the difference between both input frequencies (cf. Moore et al., 1998). Because both tones are summed before entering the cochlear filter, acoustic beating tones can be heard at pitches throughout the auditory frequency range. Beat stimuli are similar to amplitude-modulated (AM) tones that are commonly used in auditory steady-state response (ASSR) audiometry (Picton et al., 2003). An important difference is that, at supra-threshold intensities, the two-component beat stimulus may excite a narrower cochlear frequency band than an AM stimulus, which consists of three spectral components, spread over twice the frequency range at an identical pitch and envelope oscillation rate. Thus, the ASSR in response to beat stimuli (beat-ASSR) may, in special cases, offer improved frequency resolution in objective audiometry, justifying its exploration in human subjects.
A beating tone may also be heard when each sinusoidal component is presented, in isolation, to a different ear (Tobias, 1963). This binaural beat, a much fainter sensation, is restricted to relatively low component frequencies of a few hundred Hz (Licklider et al., 1950) that are temporally encoded as spike firing phase-locked to the sound wave (Rose et al., 1968). In the mammalian auditory system robust phase locking, to tone frequencies up to a few kHz, has been demonstrated in cochlear nerve fibers (Palmer and Russell, 1986) and in the spherical bushy cells of the antero-ventral cochlear nucleus (Goldberg and Brownell, 1973) whose axons project to the medial superior olivary (MSO) nucleus (Goldberg and Brown, 1969, Smith et al., 1993). MSO neurons receive the inputs from both ears separately, each at one of their two dendritic trees (Ramon and Cajal, 1909, Schwartz, 1977), where the sound waves are, presumably, replicated (Agmon-Snir et al., 1998). The membrane potential at the MSO neuron spike trigger zone, close to the soma, is thought to reflect a combination of the sound waves from both ears, and the output spike rate of MSO neurons is modulated at the envelope time pattern of the sum of both input waveforms (Yin and Chan, 1990). Thus, firing patterns of inferior colliculus neurons, the target of MSO axon projections, can reflect a binaural beat (Kuwada et al., 1979). In the tonotopic array of the MSO, each neuron is tuned to a narrow frequency band, similar to cochlear nerve fibers, and different tones in both ears may be combined only if they fall in the same critical frequency band. Thus, different tones in each ear can be heard as binaural beat only if they are separated in frequency by less than a critical band (like acoustic beats) and have frequencies sufficiently low to be temporally encoded (unlike acoustic beats). An EEG response to binaural beat stimuli will, therefore, functionally assess the temporal coding mechanisms in the lower auditory brainstem.
A binaural beat stimulus should, hypothetically, be able to evoke an ASSR, since it should cause firing rates in the MSO output, and thus in cortical afferents, to be modulated in a manner similar to the AM tones commonly used in ASSR audiometry. We did not doubt that we could record an acoustic beat ASSR from the human brain, since this response type had already been reported for non-human mammals (Dolphin et al., 1994). Our ability to detect a binaural beat ASSR was less certain, however, for several reasons. (1) The binaural beat usually is a faint sensation. Thus, a corresponding EEG signal could be small and difficult to separate from larger EEG oscillations. (2) Maximal steady state responses have been recorded at stimulus repetition- or amplitude modulation rates in the gamma range, close to 40 Hz (cf. Picton et al., 2003). The human auditory system may interpret a 40 Hz modulation rate as a distinct low pitch tone rather than a beat. (3) A human subject may have a choice to listen to two tones in different ears separately or combine them as one beating sound. Here, one perception could exclude the other, as in Edgar Rubin's famous picture showing mutually excluding contours of either two faces or a vase (cf. Kandel, 1991). During dichotic sound stimulation two mutually exclusive perceptions may also occur. For example, a dichotic presentation of the second of two noises, delayed between the ears, can cause either a noise sensation at a specific location in space or a musical pitch (Fourcin, 1970). A binaural beat ASSR could, therefore, depend upon a focus of attention on the beat sensation. Using a time domain analysis, we attempted to optimize a distinction of small steady state responses from the ongoing EEG and noise. Hink et al. (1980) reported a beating binaural frequency following response. Here we show that two pure tone stimuli in separate ears can evoke a binaural beat ASSR at a 40 Hz difference frequency in normal hearing subjects. The binaural beat ASSR differed qualitatively from a much more robust monaural, acoustic beat ASSR.
Section snippets
Subjects
Eighteen healthy subjects (11 females and 7 males, ages from 16 to 47 years) without otological or neurological disease in their histories and with normal pure tone audiometric thresholds were recruited for experiments. The subjects were paid to participate in the study, informed in writing about purpose and procedures and signed a consent form, according to procedures approved by the Human Ethics Committee of the University of British Columbia, in compliance with the Helsinki Convention.
Stimuli
Beat ASSR
Stimulation of the same (right or left) ear with two tones differing in frequency by 40 Hz, with a mean frequency of 400 Hz and presented 70 dB above individual component thresholds (40–400, 70 dB stimulus), produced a strong 40 Hz oscillation in the band pass filtered averaged EEG record. This acoustic beat ASSR, shown for the CZ electrode in the example of Fig. 1 (monaural), gradually grew in amplitude over the first 200 ms and was sustained throughout the remaining stimulus duration. After
Beat ASSR and beat sensation
Binaural beats originate, presumably, in the same neural circuits of the auditory brainstem that compute sound direction from an inter-aural time difference (Kuwada et al., 1979). If the tone presented to one ear differs in frequency from the tone in the other ear by less than ∼2 Hz the sound appears to move in the head from side to side. At greater frequency difference the perceived tone fluctuates in loudness instead (Moore, 2003), producing similar beating vibrato sensations during binaural
Acknowledgements
We thank three anonymous reviewers of this journal for suggestions that improved this paper. This study has been supported by the Canadian Institutes for Health Research, The Hearing Foundation of Canada and the Rotary Hearing Foundation, Vancouver.
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