490
Brain Research, 92 (1975) 490-498 ci2~Elsevier Scientific Pubhshmg Company, Amsterdam - Printed m The Netherlands
The effect of sound pressure waveform on human brain stem auditory evoked responses
EDWARD M. ORNITZ AND DONALD O WALTER Department o f Psychtato' and Brain Research Instttute, U C L.A Centel Jor the Health Scwnces, Los Angeles, Calif. 90024 ( U S.A.)
(Accepted Aprd 8th, 1975)
Neural responses from the auditory pathway in the human brain stem recorded from the skin of the head were first reported in 19672s,3a. Yoshie e t al. 33 recorded from a needle electrode in the external auditory meatus referenced to the earlobe, whereas Sohmer and Feinmesser 2s recorded from the earlobe referenced to the nose. These studies (along with those conducted independently m France and reported in the same year, using a promontory recording 24) formed the basis of modern nonsurgical electrocochleography, the subsequent development of which has been reviewed by Eggermont and Odenthal 4. Using the earlobe to nose recording, and averaging techniques, Sohmer and Feinmesser 2s identified 4 successive waves occurring at approximately 1 msec intervals following a click stimulus. The first two waves were identified as the N~ and N2 components of the cochlear action potential, familiar to electrocochleography 5,19. Sohmer and Feinmesser 28 suggested that the succeeding peaks might be due either to repetitive firing of auditory nerve fibers, or to discharge of neurons in brain stem auditory nuclei, and that all components of this very-short-latency response (occurring within 6 msec of the arrival of the stimulus) reached the recording electrodes by volume conduction. In a subsequent study, Sohmer and Feinmesser 29 were able to record the same set of waves with the recording dipole shifted from an earlobe-nose to an earlobe-vertex placement. These results were subsequently replicated by other investigators using various electrode combinations 1°, 11,17,22,23. The responses have been recorded in neonates 1'~ and young children 8,15, they are unaffected by varying states of attention 21 and remain stable during several stages of sleep 1. Both Jewett 9 and Lev and Sohmer 14, by recording directly from brain stem sites in cats, confirmed the earlier suggestion of Sohmer and Feinmesser 2s that the series of successive vertex positive (relative to, e.g., earlobe) waves recordable from the human scalp represented activity from the auditory nerve, the cochlear nucleus, the superior olive, and the inferior colliculus respectively Using the nomenclature of Picton e t al 22 vertex positive waves 1 (latency 1.5 msec) and II (latency 2.6 msec) can be considered equivalent to waves N1 and N2 described in electrocochleography. It seems reasonably certain that these waves are
491
Rarefaction and Condensation Sound Waves
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Fig. 1. The oscilloscope photographs show the effect of reversing the input (lower tracings) to the audio-amplifier (upper tracings) on the sound pressure wave (middle tracings). The audio-amplifier was connected to the earphone so that a positive pulse caused the diaphragm to 'pull' back (rarefaction) and a negatwe pulse caused the diaphragm to 'push' forward (condensation). The resulting sound pressure waves had identical frequency characteristics (measured with a Briiel and Kjaer audiofrequency spectrometer) which are displayed m the graph.
492 generated by the auditory nerve fibers and the cochlear nucleus. The specific source of wave III (latency 3.8 msec), wave IV (latency 5 0 msec), and wave V (5.8 msec) is less definite. Topographic analysis z2 tends to support the interpretation that the later waves are composites of mulUple generators, perhaps representing act~wty from the superior ohve (wave III) and the inferior colliculus (waves IV and V) combined with repetitive firings from the more peripheral sites 10. In these investigations of the very-short-latency evoked responses, little attention has been paid to the physical parameters of the stimulus (usually clicks) and their effects on the waveform of the response. Most reports simply specify the wzdth of the pulse used as input to the audioamplifying system, without regard to polarity or waveform of the output or of the resultant soundwave. Other reports indicate activation of the audioamphfier with alternating positive and negative pulses, but only show the averaged response to all pulses combined. We have obtained short-latency click-evoked responses from 20 normal adults (20-31 years) and chddren (2-12 years) and 8 autistic children, using vertex-tomastoid placement of silver-silver chloride disc electrodes. Chcks were produced from square wave pulses (0.2 msec) delivered monaurally at a rate of 10/sec, after amphfication to 68 dB (HL), to a T D H 39 earphone. The resultant sound pressure waves (measured with a Brfiel and Kjaer audiofrequency spectrometer, Type 2112, through a Brfiel and Kjaer artificial ear, Type 4152) to positive pulses (rarefaction) and negatwe pulses (condensation) are shown in Fig. 1. Responses were amplified on one channel of a Grass 78 electroencephalograph with the sensitivity at 1 and the band pass of 30-3000 Hz (half-amplitude values), and were then subjected to additional high pass filtering (half-amplitude at 500 Hz) before averaging; 1024 responses to rarefaction clicks and 1024 responses to condensation clicks were separately summed on-hne by a FabriTek 1062 signal average~ using the first quarter (12.5 msec) of the full memory. Figs. 2 and 3 show typical responses to rarefaction and condensation clicks in a normal adult and an autistic child respectively. Attention is directed to the close similarity between the response to the rarefaction and condensation chcks m the adult subject. In the autistic chdd, however, it can be seen that the peaks of the responses to the two types of chcks are almost completely out of phase. When these two responses are added together, the resulting amphtudes are smaller than those of either response (the scaling has been halved to compensate for the doubled number of responses). Differing responses to rarefaction and condensation chcks were not confined to the autistic children, but also occurred in the responses of normal subjects; occurrence or non-occurrence of this d~fferentml response was remarkably stable for each subject. Twelve subjects were recorded on 2 or more days, 3 of these subjects returning for 3 or more recording days over periods of many weeks. Of these 12 subjects, the 9 who showed the differential response always showed it, and the 3 who d~d not show it, never showed it. For all subjects who showed the differential response, the peak latencies were always shorter in response to rarefaction clicks. The most impressive differences were observed in the latencies of vertex positive peak 4 (mean latency 4.8 msec) : the peak response to rarefaction clicks preceded the peak response to condensation clicks by 0.4-0.8 msec.
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Fig. 2. Normal adult. The upper left and right quadrants show 3 averaged auditory evoked responses (AERs) to rarefaction and condensation chcks respectwely. The lower left quadrant compares one of the AERs to rarefaction clicks with one of the AERs to condensation clicks. The lower right quadrant shows three AERs, each of which is the sum of responses to an equal number of rarefaction and condensation clicks. In this and the next figure, the numbers below the successive peaks identify vertex positive (downward deflection) waves m accordance with the usage of Picton et aL~L The appearance of the stimulus artifact is due to overflow in the D - A converter. No attempt is made to suppress it in order to demonstrate its large amplitude andbrief duration.
494
"
Brain Research, 92 (1975) 490-498 ci2~Elsevier Scientific Pubhshmg Company, Amsterdam - Printed m The Netherlands
The effect of sound pressure waveform on human brain stem auditory evoked responses
EDWARD M. ORNITZ AND DONALD O WALTER Department o f Psychtato' and Brain Research Instttute, U C L.A Centel Jor the Health Scwnces, Los Angeles, Calif. 90024 ( U S.A.)
(Accepted Aprd 8th, 1975)
Neural responses from the auditory pathway in the human brain stem recorded from the skin of the head were first reported in 19672s,3a. Yoshie e t al. 33 recorded from a needle electrode in the external auditory meatus referenced to the earlobe, whereas Sohmer and Feinmesser 2s recorded from the earlobe referenced to the nose. These studies (along with those conducted independently m France and reported in the same year, using a promontory recording 24) formed the basis of modern nonsurgical electrocochleography, the subsequent development of which has been reviewed by Eggermont and Odenthal 4. Using the earlobe to nose recording, and averaging techniques, Sohmer and Feinmesser 2s identified 4 successive waves occurring at approximately 1 msec intervals following a click stimulus. The first two waves were identified as the N~ and N2 components of the cochlear action potential, familiar to electrocochleography 5,19. Sohmer and Feinmesser 28 suggested that the succeeding peaks might be due either to repetitive firing of auditory nerve fibers, or to discharge of neurons in brain stem auditory nuclei, and that all components of this very-short-latency response (occurring within 6 msec of the arrival of the stimulus) reached the recording electrodes by volume conduction. In a subsequent study, Sohmer and Feinmesser 29 were able to record the same set of waves with the recording dipole shifted from an earlobe-nose to an earlobe-vertex placement. These results were subsequently replicated by other investigators using various electrode combinations 1°, 11,17,22,23. The responses have been recorded in neonates 1'~ and young children 8,15, they are unaffected by varying states of attention 21 and remain stable during several stages of sleep 1. Both Jewett 9 and Lev and Sohmer 14, by recording directly from brain stem sites in cats, confirmed the earlier suggestion of Sohmer and Feinmesser 2s that the series of successive vertex positive (relative to, e.g., earlobe) waves recordable from the human scalp represented activity from the auditory nerve, the cochlear nucleus, the superior olive, and the inferior colliculus respectively Using the nomenclature of Picton e t al 22 vertex positive waves 1 (latency 1.5 msec) and II (latency 2.6 msec) can be considered equivalent to waves N1 and N2 described in electrocochleography. It seems reasonably certain that these waves are
491
Rarefaction and Condensation Sound Waves
Ou'l'pul" O! A u d i o A m p l i I
Sound
Rarefaction
,2msec
Ou'l'puf
-}- S q u a r e
of
Audio
Condensation
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Fig. 1. The oscilloscope photographs show the effect of reversing the input (lower tracings) to the audio-amplifier (upper tracings) on the sound pressure wave (middle tracings). The audio-amplifier was connected to the earphone so that a positive pulse caused the diaphragm to 'pull' back (rarefaction) and a negatwe pulse caused the diaphragm to 'push' forward (condensation). The resulting sound pressure waves had identical frequency characteristics (measured with a Briiel and Kjaer audiofrequency spectrometer) which are displayed m the graph.
492 generated by the auditory nerve fibers and the cochlear nucleus. The specific source of wave III (latency 3.8 msec), wave IV (latency 5 0 msec), and wave V (5.8 msec) is less definite. Topographic analysis z2 tends to support the interpretation that the later waves are composites of mulUple generators, perhaps representing act~wty from the superior ohve (wave III) and the inferior colliculus (waves IV and V) combined with repetitive firings from the more peripheral sites 10. In these investigations of the very-short-latency evoked responses, little attention has been paid to the physical parameters of the stimulus (usually clicks) and their effects on the waveform of the response. Most reports simply specify the wzdth of the pulse used as input to the audioamplifying system, without regard to polarity or waveform of the output or of the resultant soundwave. Other reports indicate activation of the audioamphfier with alternating positive and negative pulses, but only show the averaged response to all pulses combined. We have obtained short-latency click-evoked responses from 20 normal adults (20-31 years) and chddren (2-12 years) and 8 autistic children, using vertex-tomastoid placement of silver-silver chloride disc electrodes. Chcks were produced from square wave pulses (0.2 msec) delivered monaurally at a rate of 10/sec, after amphfication to 68 dB (HL), to a T D H 39 earphone. The resultant sound pressure waves (measured with a Brfiel and Kjaer audiofrequency spectrometer, Type 2112, through a Brfiel and Kjaer artificial ear, Type 4152) to positive pulses (rarefaction) and negatwe pulses (condensation) are shown in Fig. 1. Responses were amplified on one channel of a Grass 78 electroencephalograph with the sensitivity at 1 and the band pass of 30-3000 Hz (half-amplitude values), and were then subjected to additional high pass filtering (half-amplitude at 500 Hz) before averaging; 1024 responses to rarefaction clicks and 1024 responses to condensation clicks were separately summed on-hne by a FabriTek 1062 signal average~ using the first quarter (12.5 msec) of the full memory. Figs. 2 and 3 show typical responses to rarefaction and condensation clicks in a normal adult and an autistic child respectively. Attention is directed to the close similarity between the response to the rarefaction and condensation chcks m the adult subject. In the autistic chdd, however, it can be seen that the peaks of the responses to the two types of chcks are almost completely out of phase. When these two responses are added together, the resulting amphtudes are smaller than those of either response (the scaling has been halved to compensate for the doubled number of responses). Differing responses to rarefaction and condensation chcks were not confined to the autistic children, but also occurred in the responses of normal subjects; occurrence or non-occurrence of this d~fferentml response was remarkably stable for each subject. Twelve subjects were recorded on 2 or more days, 3 of these subjects returning for 3 or more recording days over periods of many weeks. Of these 12 subjects, the 9 who showed the differential response always showed it, and the 3 who d~d not show it, never showed it. For all subjects who showed the differential response, the peak latencies were always shorter in response to rarefaction clicks. The most impressive differences were observed in the latencies of vertex positive peak 4 (mean latency 4.8 msec) : the peak response to rarefaction clicks preceded the peak response to condensation clicks by 0.4-0.8 msec.
r~
g,
w a:
e
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m
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cJ tJ -J -r al "o
o
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Fig. 2. Normal adult. The upper left and right quadrants show 3 averaged auditory evoked responses (AERs) to rarefaction and condensation chcks respectwely. The lower left quadrant compares one of the AERs to rarefaction clicks with one of the AERs to condensation clicks. The lower right quadrant shows three AERs, each of which is the sum of responses to an equal number of rarefaction and condensation clicks. In this and the next figure, the numbers below the successive peaks identify vertex positive (downward deflection) waves m accordance with the usage of Picton et aL~L The appearance of the stimulus artifact is due to overflow in the D - A converter. No attempt is made to suppress it in order to demonstrate its large amplitude andbrief duration.
494
"
