Cortical evoked potentials to an auditory illusion: Binaural beats
Introduction
When two sinusoids with slightly different frequencies are superimposed, their interference results in periodic amplitude fluctuations whose frequency corresponds to the frequency difference between the sinusoids. When sound with slightly different frequencies is mixed in the same ear, the fluctuations in the intensity of the sound are perceived as beats, reflecting the acoustic properties of the stimulus and are thus called acoustic beats. When a tone of one frequency and steady intensity is presented to one ear and a slightly different frequency is presented to the other ear, a perception of beats is experienced, with a beat frequency corresponding to the frequency difference between the two ears. These beats do not reflect a physical property of the sound, but probably the convergence of neural activity from the two ears in the central binaural auditory pathways of the brain. The intensity changes in the perceived sound are therefore called “binaural beats”. Binaural beats are present when the disparate frequencies to the two ears are low, and beats are difficult to hear at frequencies above 1000 Hz (Licklider et al., 1950).
The most widely accepted physiological explanation for binaural beats suggests that discharges of neurons that preserve phase information of the sound in each ear according to the volley principle (Rose et al., 1968, Palmer and Russel, 1986, Goldberg and Brownell, 1973) converge on binaurally-activated neurons in the ascending auditory pathway (Kuwada et al., 1979, McAlpine et al., 1996, McAlpine et al., 1998, Spitzer and Semple, 1998) that, in turn, generate the neurophysiological correlate of binaural beats (Wernick and Starr, 1968) in the brainstem.
Normative human studies on binaural beats showed differences between the subjective rhythm perceived and the difference between the two frequencies, indicating a central effect (Fritze, 1985). Clinical studies of binaural beats in humans varied in their sensitivity to cortical damage. Some reported that binaural beats were not sensitive to cortical damage (Noffsinger, 1982) but others showed that binaural beats could not be perceived by patients with cortical lesions associated with severe aphasia (Barr et al., 1977). A detailed study of a single patient with Auditory Neuropathy reported that a marked impairment of binaural beats was observed in conjunction with impaired auditory perceptions dependent on temporal cues, such as lateralization of binaural clicks, change of binaural masked threshold with changes in signal phase, detection of paired monaural clicks, monaural detection of a silent gap in a sound, and monaural threshold elevation for short duration tones (Starr et al., 1991). Effects of binaural beats at the Beta EEG frequency on psychomotor performance, mood and arousal (Lane et al., 1998) have also been reported.
Thus, animal experiments indicate the auditory brainstem as the level of binaural beat formation, human studies agree that binaural beats are a central effect which is sensitive to temporal acoustic cues and which may interact with cortical function.
Although the psychoacoustic effect of binaural beats has been well-studied in normals and patients, only very few studies reported ERP correlates of binaural beats. Two studies recorded auditory steady-state responses to a binaural beat frequency of 40 Hz. In the first (Schwarz and Taylor, 2005), the right and left ears were stimulated with tones differing in frequency by 40 Hz, and binaural beat steady-state potentials were recorded. A 40-Hz binaural beat potential was evoked with a low base stimulus frequency (400 Hz) but became undetectable when base frequency was above 3 kHz. In another study (Karino et al., 2006), magnetic fields evoked by beats of 4.00 or 6.66 Hz in base frequencies of 240 and 480 Hz were described. The fields showed small but sufficient amplitudes to be distinguished from the noise in the recordings. Spectral analyses of the magnetic fields revealed that the responses contained a specific spectral component of the beat frequency. Source estimates suggested multiple sources in the left and right auditory cortices and in parietal and frontal cortices. The phase of the beat-evoked waveforms showed great variability, suggesting that the responses did not represent changing interaural phase differences but a cognitive process corresponding to subjective fluctuations of binaural beats. More recently, 40 Hz binaural beats of a 500 Hz base frequency were used to evoke steady-state magnetic fields which were also compared with the transient-evoked N1m (Draganova et al., 2008). The auditory steady-state sources were lateralized to the right hemisphere and were anterior, inferior, and medial compared with onset N1m sources.
Two of the three previous reports on electrophysiological correlates of binaural beats used a beat frequency of 40 Hz. This frequency is optimal for thalamic and primary cortical steady-state activity, but later cortical contributions associated with perception are markedly attenuated at this rate. Moreover, the filter properties of scalp and skull attenuate 40 Hz potentials relative to lower frequencies and this attenuation of a beat frequency of 40 Hz may impede the detection and characterization of the slower brain activity associated with the perception of binaural beats. There is disagreement among previous studies on the sources of the beat-evoked oscillations: One study found bilateral sources in temporal lobe (Karino et al., 2006) while in the other – sources were lateralized to the right (Draganova et al., 2008).
The purpose of this study was to define cortical auditory evoked potentials to binaural beats of 3 or 6 Hz in high- (1000 Hz) and low- (250 Hz) base frequency tones, and to estimate their intracranial sources. Potentials to the onset of the tones were also recorded for comparison.
Section snippets
Subjects
Eighteen (16 men and 2 women) 18 to 25 years old right handed normal hearing subjects participated in the study. Subjects were paid for their participation and all procedures were approved by the institutional review board for experiments involving human subjects (Helsinki Committee).
Stimuli
Binaural tone bursts of 2000 ms duration and 70 dBnHL intensity were presented through earphones (Sony MDR-CD770) with a flat frequency response (within 10 dB across the frequency range 100–10,000 Hz). Tones were
Results
All subjects reported perceiving beats in all four stimulus conditions (3 and 6 Hz beats in 250 and 1000 Hz base frequencies). The beats were described as faint to comfortable and as emanating from the center of the head. At onset, the binaural tones evoked components beginning with a P50, N100 and P200, followed by a positive peak labeled and a negativity termed N0, followed by repetitive negative/positive oscillations corresponding to the frequency difference between left and right ear.
The results of this study
In this study brain potentials associated with the auditory illusion of binaural beats were recorded and compared across two beat frequencies with tone bursts of two base frequencies. Beat-evoked oscillations were preceded by tone-onset components P50, N100 and P200, and were followed by tone-offset components. Sources of the beats-evoked oscillations across all stimulus conditions were mostly in the left lateral and inferior temporal lobe. This lateralized temporal activity is in line with
Conclusions
The results of this study confirm that brain activity corresponding to an auditory illusion can be recorded from the scalp. The oscillations associated with binaural beats were larger to low- than to high frequency sound, congruent with the involvement in this illusion of ‘volley principle’ neural encoding. The results are in line with the suggested mechanism of binaural beats: neural volleys with slightly different frequencies from left and right ear converge and interfere in the central
Acknowledgements
This study was partially supported by the US-Israel Binational Science Foundation, by Grant DC 02618 from the National Institutes of Health and by the Rappaport Family Institute for Research in the Medical Sciences.
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