Acta Oto-Laryngologica
ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20
Development of Auditory Evoked Potentials Jos J. Eggermont To cite this article: Jos J. Eggermont (1992) Development of Auditory Evoked Potentials, Acta Oto-Laryngologica, 112:2, 197-200, DOI: 10.1080/00016489.1992.11665403 To link to this article: http://dx.doi.org/10.1080/00016489.1992.11665403
Published online: 04 Jan 2016.
Submit your article to this journal
View related articles
Citing articles: 3 View citing articles
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ioto20 Download by: [Universität Osnabrueck]
Date: 18 March 2016, At: 21:15
Acta Otolaryngol (Stockh) 1992; 112: 197-200
Development of Auditory Evoked Potentials JOS J.EGGERMONT From the Department of Psychology, The University of Calgary, Canada
Downloaded by [Universität Osnabrueck] at 21:15 18 March 2016
Eggermont JJ. Development of auditory evoked potentials. Acta Otolaryngol (Stockh) 1992; 112: 197-200. The development and maturation of the human auditory system appears to occur in parallel at all levels from middle ear to cortex. The maturation of evoked potentials from auditory brainstem to auditory cortex can be described by equal percentage changes in equal time periods. This is essentially the exponential growth model with equal maturation rate for each station. The auditory nerve maturation occurs at a rate considerably faster than that for more central parts of the nervous system. Premature birth does not seem to affect the maturation rate and time to maturity of the auditory brainstem potentials, so that experience does not seem to affect physiological maturation. However, there is a clear difference in maturation rates for different frequency regions, suggesting that the time course of structural maturation has an effect. Behavioral changes in hearing threshold show maturation rates similar to the physiological ones for the central nervous system. Key words: maturation, evoked potentials. prematurity,
auditory brains/em response.
INTRODUCfiON Auditory evoked potentials (AEP) can be recorded from the entire auditory pathway. They originate in the auditory nerve (compound action potential, CAP, and waves I and II of the auditory brainstem response, ABR), the auditory brain stem (waves III to V of the ABR), the auditory midbrain and/or thalamus (waves VI and VII of the ABR) and the auditory cortex (middle latency responses, MLR, and slow vertex potentials, SVP). The more rostral the origin of the AEP the longer is its latency: thus for a 60 dB nHL click the CAP (and also wave I) has a latency of about 1.6 ms, wave V (probably originating in the lateral lemniscus) has a latency of 5.6 ms, the P. component's latency of the MLR is 25 ms, and that of the N 1 component of the SVP about 90 ms. A comprehensive survey of the use of the ABR in neonatology and pediatrics has been given by Picton et al. (I). Age has a profound effect on the latencies; neonates have longer latencies than adults. This age dependency of the AEPs has been explored extensively (most references to previous literature are omitted in this review but can be found in Eggermont (2, 3, 4) and this paper will deal with these changes and what they tell us about the maturation of the brain and the development of auditory function. LATENCY CHANGES DURING NORMAL DEVELOPMENT It is assumed (2, 3) that 1) the latency changes seen for the various evoked potential components reflect the maturation of structures (in the cochlea, auditory nerve, brain stem up to the auditory cortex) that are peripheral to the proposed generation site for that particular AEP. 2) The maturation ofthe auditory system structures is mainly the result of increased myelination (especially in auditory nerve and brain stem), increase in synaptic density (mainly in auditory cortex), and increase in synaptic efficacy (everywhere). 3) Each of these increases results in an exponential decrease in latency of the evoked potentials. 4) All maturational processes in the normal infant proceed independently and thus in parallel. Changes in wave I (the compound action potential of the auditory nerve) can hardly be observed in the full term infant suggesting that the cochlea is very close to maturity at the time
198 J. J. Eggermont 2.0
a
Acta Otolaryngol (Stockh) 112
a Starr o Uziel
a
+ Krumholtz
~
s.,"'
1.5
x Mochizuki m • Mochizuki f A Salamy • Eggermont
+ 1
u
r::
~
.... :,:; ~
1.0
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.:!
~
0.5
t~. ...
0.0
100
0
300
200
Downloaded by [Universität Osnabrueck] at 21:15 18 March 2016
Age (weeks CA)
b
4
Uzicl o Beiser + Krumholtz x Mochizuki m • Mochizuki f • Eggermont o Zimmennan D
-;;-
sg
3
e
~
~ 2
•
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g
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0 0
100
200
300
Fig. I. (a) Differences with adult latency for wave I as a function of conceptional age. Data are based on mean values from various publi· cations, indicated by first author (references in Eggermont, 1989), the additions m and f after Mochizuki represent male and female subjects. The Eggermont data refer to Egger· mont & Salamy (5); (b) Differences with adult latency for wave V as a function of conceptiona! age. Data again represent mean values at particular age groups from various publicalions. Exponential curve fits are drawn in.
Age (weeks CA)
of full term birth, and in order to study these changes we have to rely on preterms (5). To obtain an accurate impression of age dependent latency changes one should preferably compare studies from various institutions in order to avoid sample bias. One difficult aspect to deal with is that different clinics rarely do employ the same equipment or the same filter settings, the same headphones or same stimulus levels, etc. This problem can be circumvented by considering only the differences in the latency with mean adult values (determined in the same clinic and with the same equipment). These changes in latency difference will then only be due to the effect of maturation. In Fig. I a the latency differences with adult value from various sources (indicated by senior author's name; references in (4), all using click stimuli, are plotted as a function of conceptional age for wave I. One observes that the maturation is completed somewhere around the 45th week conceptional age and that from full term birth on there is only a small difference with adult values. It is therefore justified to say that the cochlea and auditory nerve are probably fully mature slightly after term birth. By using derived responses it was observed that the most basal part of the cochlea (frequencies above 8 kHz) takes much longer to mature than the middle and more apical parts (6). Changes in wave V latency are expected to follow in part the changes in wave I latency and in addition to reflect the maturation of the auditory brain stem structures. The latency differences with the adult values again compiled from various studies are plotted in Fig. I b. One observes that it takes approximately 3-5 years for this difference to become negligibly small. It appears that the data points can be approximated very well by the sum of two exponential functions. One of these exponential functions has, as expected, the same time constant as that for the wave I changes. The other exponential with a much longer time constant, and therefore representing a much slower process, is assumed to reflect the brain
Development of auditory evoked potentials
Acta Otolaryngol (Stockh) 112
250 • •
200
Pa (Roneveel) N2(8amelt) P2(Bamell) •••• I·V
.. .•
Downloaded by [Universität Osnabrueck] at 21:15 18 March 2016
•.
Fig. 2. Differences with adult
so
0
-,....~~----·----~----·----------·----------.-ro W 100 IW 140 40
value for ABR, MLR and SVP data. The exponential curvefits (drawn in) suggest that the SVP components mature with the same rate as the P, component of the MLR and the 1-V of the ABR.
Age (weeks CA)
stem related changes. By using the derived response technique (6) and focussing on the 1-V interval we found that the middle frequencies mature considerably faster and earlier than both the high (above 8 kHz) and the low (below I kHz) frequencies. Comparison of various ABR studies reveals that there is a surprisingly good correspondence between the results obtained. Part of the reason for the good correspondence is that only differences with adult latencies obtained in the same laboratory are compared and this to a large extent eliminates idiosyncratic effects of stimulus and equipment. On other occasions (2) I have selected data from other publications, only some of which are included in the present study. Changes in the MLR components in infancy and childhood have been somewhat controversial, some investigators could not find reliable latency changes while others claim that consistent latency changes could be recorded, however, not in all subjects (7, 8). Suzuki & Hirabayashi's (8) data indicated that the P1 component of the ABR has barely reached maturity in the 12-14-year-old; however, because their youngest age group was 4-7-year-old his data are not included in our graphical survey (Fig. 2). Changes in the SVP components, N2 and P 2, can be shown on basis of the data of Barnett et al. (9) covering the time span of 3 days after birth to 3 years of age (Fig. 2). When replotted on semilogarithmic coordinates the exponential curves become straight lines that almost run parallel and thus the rate of change for N 2 and P 2 is about the same as for the ABR wave V (2, 3, 4) thus we can definitely rule out that the maturation of these SVPs is governed by a slower process than that for the ABR.
199
Downloaded by [Universität Osnabrueck] at 21:15 18 March 2016
200 J. J. Eggermont
Acta Otolaryngol (Stockh) 112
EFFECTS OF PREMATURITY Recently we (5) investigated the maturation of the ABR for a group of full terms (n=465) and a group of healthy preterms (n= 178). The preterm population comprised subjects with birthweights equal to or below I 500 g (mean= 1 097, SD=223.94) and gestational ages ranging from 25-35 weeks (mean 29.3, SD=2.3). All subjects were enrolled in the Pediatric Follow-up Program at UCSF. Infants with chromosomal abnormalities or major congenital anomalies, significant neurological involvement or hearing loss (determined retrospectively) were excluded from ABR analyses. The study was mixed longitudinal and cross sectional (total number of ABRs: 1164) and learned us that the 1-111, 111-V, and 1-V delay changed in the same way in preterms as in full terms and that the actual value of these delays was determined by the conceptional age and was independent of gestational age. Furthermore the rate of change appeared to be the same for all three inter-peak intervals. Thus prematurity had in itself no adverse effect on the maturation of the ABR parameters, nor did the earlier exposure to environmental sounds advance the maturation of the ABR. BEHAVIORAL AND PHYSIOLOGICAL MATURATION COMPARED Exponential changes in hearing threshold in listeners 6.5 months to 20.5 years were reported recently by Schneider et at. (I 0). These data showed that the rate of behavioral maturation was very close to the rate for the physiological maturation of the 1-V, MLR and SVP components reported here. This suggests that behavioral thresholds are not only determined by the maturational status of cochlea and the auditory nerve but also by the slower maturating central nervous system. ACKNOWLEDGEMENTS This manuscript was prepared under grant support from the Alberta Heritage Foundation for Medical Research and the Natural Sciences and Engineering Research Council.
REFERENCES I. Picton TW, Taylor MJ, Durieux-Smith A, Edwards CG. Brainstem auditory evoked potentials in pediatrics. In: AminofT MJ, ed. Electrodiagnosis in clinical neurology, 2nd ed. New York: Churchill Livingstone, 1986: 505-34. 2. Eggermont JJ. Physiology of the developing auditory system. In: Trehub SE, Schneider B, eds. Auditory development in infancy. New York: Plenum Press, 1985: 21-45. 3. Eggermont JJ. On the rate of maturation of sensory evoked potentials. Electroencephalogy Oin Neurophysiol 1988; 70: 293-305. 4. Eggermont JJ. The onset and development of auditory function: contributions of evoked potential studies. J Speech Language Pathol Audiol 1989; 13: 5-16. 5. Eggermont JJ, Salamy A. Maturational time course for the ABR in preterm and full term infants. Hear Res 1988; 33: 35-48. 6. Eggermont JJ, Ponton CW, Coupland SG, Winkelaar R. Frequency dependent maturation of the cochlea and brainstem evoked potentials. Acta Otolaryngol (Stockh) 1991; Ill: 220-4. 7. Rotteveel JJ, Colon EJ, Stegeman OF, Visco YM. The maturation of the central auditory conduction in preterm infants until three months post term. I. Composite group averages of brain stem (ABR) and middle latency (MLR) auditory evoked responses. Hear Res 1987; 26: 11-20. 8. Suzuki T, Hirabayashi M. Age-related morphological changes in auditory middle-latency response. Audiology 1987; 26: 312-02. 9. Barnett AB, Ohlrich ES, Weiss IP, Shanks B. Auditory evoked potentials during sleep in normal children from ten days to three years of age. Electroencephalogy Clin Neurophysiol 1975; 39: 29-41. 10. Schneider BA, Trehub SE, Morrongiello BA, Thorpe LA. Developmental changes in masked thresholds. J Acoust Soc Am 1989; 86: 1733-42. Address for correspondence: J os J. Eggermont, Department of Psychology, The University of Calgary, 2500 University Drive, Calgary, Alberta, Canada T2N IN4
ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20
Development of Auditory Evoked Potentials Jos J. Eggermont To cite this article: Jos J. Eggermont (1992) Development of Auditory Evoked Potentials, Acta Oto-Laryngologica, 112:2, 197-200, DOI: 10.1080/00016489.1992.11665403 To link to this article: http://dx.doi.org/10.1080/00016489.1992.11665403
Published online: 04 Jan 2016.
Submit your article to this journal
View related articles
Citing articles: 3 View citing articles
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ioto20 Download by: [Universität Osnabrueck]
Date: 18 March 2016, At: 21:15
Acta Otolaryngol (Stockh) 1992; 112: 197-200
Development of Auditory Evoked Potentials JOS J.EGGERMONT From the Department of Psychology, The University of Calgary, Canada
Downloaded by [Universität Osnabrueck] at 21:15 18 March 2016
Eggermont JJ. Development of auditory evoked potentials. Acta Otolaryngol (Stockh) 1992; 112: 197-200. The development and maturation of the human auditory system appears to occur in parallel at all levels from middle ear to cortex. The maturation of evoked potentials from auditory brainstem to auditory cortex can be described by equal percentage changes in equal time periods. This is essentially the exponential growth model with equal maturation rate for each station. The auditory nerve maturation occurs at a rate considerably faster than that for more central parts of the nervous system. Premature birth does not seem to affect the maturation rate and time to maturity of the auditory brainstem potentials, so that experience does not seem to affect physiological maturation. However, there is a clear difference in maturation rates for different frequency regions, suggesting that the time course of structural maturation has an effect. Behavioral changes in hearing threshold show maturation rates similar to the physiological ones for the central nervous system. Key words: maturation, evoked potentials. prematurity,
auditory brains/em response.
INTRODUCfiON Auditory evoked potentials (AEP) can be recorded from the entire auditory pathway. They originate in the auditory nerve (compound action potential, CAP, and waves I and II of the auditory brainstem response, ABR), the auditory brain stem (waves III to V of the ABR), the auditory midbrain and/or thalamus (waves VI and VII of the ABR) and the auditory cortex (middle latency responses, MLR, and slow vertex potentials, SVP). The more rostral the origin of the AEP the longer is its latency: thus for a 60 dB nHL click the CAP (and also wave I) has a latency of about 1.6 ms, wave V (probably originating in the lateral lemniscus) has a latency of 5.6 ms, the P. component's latency of the MLR is 25 ms, and that of the N 1 component of the SVP about 90 ms. A comprehensive survey of the use of the ABR in neonatology and pediatrics has been given by Picton et al. (I). Age has a profound effect on the latencies; neonates have longer latencies than adults. This age dependency of the AEPs has been explored extensively (most references to previous literature are omitted in this review but can be found in Eggermont (2, 3, 4) and this paper will deal with these changes and what they tell us about the maturation of the brain and the development of auditory function. LATENCY CHANGES DURING NORMAL DEVELOPMENT It is assumed (2, 3) that 1) the latency changes seen for the various evoked potential components reflect the maturation of structures (in the cochlea, auditory nerve, brain stem up to the auditory cortex) that are peripheral to the proposed generation site for that particular AEP. 2) The maturation ofthe auditory system structures is mainly the result of increased myelination (especially in auditory nerve and brain stem), increase in synaptic density (mainly in auditory cortex), and increase in synaptic efficacy (everywhere). 3) Each of these increases results in an exponential decrease in latency of the evoked potentials. 4) All maturational processes in the normal infant proceed independently and thus in parallel. Changes in wave I (the compound action potential of the auditory nerve) can hardly be observed in the full term infant suggesting that the cochlea is very close to maturity at the time
198 J. J. Eggermont 2.0
a
Acta Otolaryngol (Stockh) 112
a Starr o Uziel
a
+ Krumholtz
~
s.,"'
1.5
x Mochizuki m • Mochizuki f A Salamy • Eggermont
+ 1
u
r::
~
.... :,:; ~
1.0
>.
g !l
.:!
~
0.5
t~. ...
0.0
100
0
300
200
Downloaded by [Universität Osnabrueck] at 21:15 18 March 2016
Age (weeks CA)
b
4
Uzicl o Beiser + Krumholtz x Mochizuki m • Mochizuki f • Eggermont o Zimmennan D
-;;-
sg
3
e
~
~ 2
•
>.
g
3
I
0 0
100
200
300
Fig. I. (a) Differences with adult latency for wave I as a function of conceptional age. Data are based on mean values from various publi· cations, indicated by first author (references in Eggermont, 1989), the additions m and f after Mochizuki represent male and female subjects. The Eggermont data refer to Egger· mont & Salamy (5); (b) Differences with adult latency for wave V as a function of conceptiona! age. Data again represent mean values at particular age groups from various publicalions. Exponential curve fits are drawn in.
Age (weeks CA)
of full term birth, and in order to study these changes we have to rely on preterms (5). To obtain an accurate impression of age dependent latency changes one should preferably compare studies from various institutions in order to avoid sample bias. One difficult aspect to deal with is that different clinics rarely do employ the same equipment or the same filter settings, the same headphones or same stimulus levels, etc. This problem can be circumvented by considering only the differences in the latency with mean adult values (determined in the same clinic and with the same equipment). These changes in latency difference will then only be due to the effect of maturation. In Fig. I a the latency differences with adult value from various sources (indicated by senior author's name; references in (4), all using click stimuli, are plotted as a function of conceptional age for wave I. One observes that the maturation is completed somewhere around the 45th week conceptional age and that from full term birth on there is only a small difference with adult values. It is therefore justified to say that the cochlea and auditory nerve are probably fully mature slightly after term birth. By using derived responses it was observed that the most basal part of the cochlea (frequencies above 8 kHz) takes much longer to mature than the middle and more apical parts (6). Changes in wave V latency are expected to follow in part the changes in wave I latency and in addition to reflect the maturation of the auditory brain stem structures. The latency differences with the adult values again compiled from various studies are plotted in Fig. I b. One observes that it takes approximately 3-5 years for this difference to become negligibly small. It appears that the data points can be approximated very well by the sum of two exponential functions. One of these exponential functions has, as expected, the same time constant as that for the wave I changes. The other exponential with a much longer time constant, and therefore representing a much slower process, is assumed to reflect the brain
Development of auditory evoked potentials
Acta Otolaryngol (Stockh) 112
250 • •
200
Pa (Roneveel) N2(8amelt) P2(Bamell) •••• I·V
.. .•
Downloaded by [Universität Osnabrueck] at 21:15 18 March 2016
•.
Fig. 2. Differences with adult
so
0
-,....~~----·----~----·----------·----------.-ro W 100 IW 140 40
value for ABR, MLR and SVP data. The exponential curvefits (drawn in) suggest that the SVP components mature with the same rate as the P, component of the MLR and the 1-V of the ABR.
Age (weeks CA)
stem related changes. By using the derived response technique (6) and focussing on the 1-V interval we found that the middle frequencies mature considerably faster and earlier than both the high (above 8 kHz) and the low (below I kHz) frequencies. Comparison of various ABR studies reveals that there is a surprisingly good correspondence between the results obtained. Part of the reason for the good correspondence is that only differences with adult latencies obtained in the same laboratory are compared and this to a large extent eliminates idiosyncratic effects of stimulus and equipment. On other occasions (2) I have selected data from other publications, only some of which are included in the present study. Changes in the MLR components in infancy and childhood have been somewhat controversial, some investigators could not find reliable latency changes while others claim that consistent latency changes could be recorded, however, not in all subjects (7, 8). Suzuki & Hirabayashi's (8) data indicated that the P1 component of the ABR has barely reached maturity in the 12-14-year-old; however, because their youngest age group was 4-7-year-old his data are not included in our graphical survey (Fig. 2). Changes in the SVP components, N2 and P 2, can be shown on basis of the data of Barnett et al. (9) covering the time span of 3 days after birth to 3 years of age (Fig. 2). When replotted on semilogarithmic coordinates the exponential curves become straight lines that almost run parallel and thus the rate of change for N 2 and P 2 is about the same as for the ABR wave V (2, 3, 4) thus we can definitely rule out that the maturation of these SVPs is governed by a slower process than that for the ABR.
199
Downloaded by [Universität Osnabrueck] at 21:15 18 March 2016
200 J. J. Eggermont
Acta Otolaryngol (Stockh) 112
EFFECTS OF PREMATURITY Recently we (5) investigated the maturation of the ABR for a group of full terms (n=465) and a group of healthy preterms (n= 178). The preterm population comprised subjects with birthweights equal to or below I 500 g (mean= 1 097, SD=223.94) and gestational ages ranging from 25-35 weeks (mean 29.3, SD=2.3). All subjects were enrolled in the Pediatric Follow-up Program at UCSF. Infants with chromosomal abnormalities or major congenital anomalies, significant neurological involvement or hearing loss (determined retrospectively) were excluded from ABR analyses. The study was mixed longitudinal and cross sectional (total number of ABRs: 1164) and learned us that the 1-111, 111-V, and 1-V delay changed in the same way in preterms as in full terms and that the actual value of these delays was determined by the conceptional age and was independent of gestational age. Furthermore the rate of change appeared to be the same for all three inter-peak intervals. Thus prematurity had in itself no adverse effect on the maturation of the ABR parameters, nor did the earlier exposure to environmental sounds advance the maturation of the ABR. BEHAVIORAL AND PHYSIOLOGICAL MATURATION COMPARED Exponential changes in hearing threshold in listeners 6.5 months to 20.5 years were reported recently by Schneider et at. (I 0). These data showed that the rate of behavioral maturation was very close to the rate for the physiological maturation of the 1-V, MLR and SVP components reported here. This suggests that behavioral thresholds are not only determined by the maturational status of cochlea and the auditory nerve but also by the slower maturating central nervous system. ACKNOWLEDGEMENTS This manuscript was prepared under grant support from the Alberta Heritage Foundation for Medical Research and the Natural Sciences and Engineering Research Council.
REFERENCES I. Picton TW, Taylor MJ, Durieux-Smith A, Edwards CG. Brainstem auditory evoked potentials in pediatrics. In: AminofT MJ, ed. Electrodiagnosis in clinical neurology, 2nd ed. New York: Churchill Livingstone, 1986: 505-34. 2. Eggermont JJ. Physiology of the developing auditory system. In: Trehub SE, Schneider B, eds. Auditory development in infancy. New York: Plenum Press, 1985: 21-45. 3. Eggermont JJ. On the rate of maturation of sensory evoked potentials. Electroencephalogy Oin Neurophysiol 1988; 70: 293-305. 4. Eggermont JJ. The onset and development of auditory function: contributions of evoked potential studies. J Speech Language Pathol Audiol 1989; 13: 5-16. 5. Eggermont JJ, Salamy A. Maturational time course for the ABR in preterm and full term infants. Hear Res 1988; 33: 35-48. 6. Eggermont JJ, Ponton CW, Coupland SG, Winkelaar R. Frequency dependent maturation of the cochlea and brainstem evoked potentials. Acta Otolaryngol (Stockh) 1991; Ill: 220-4. 7. Rotteveel JJ, Colon EJ, Stegeman OF, Visco YM. The maturation of the central auditory conduction in preterm infants until three months post term. I. Composite group averages of brain stem (ABR) and middle latency (MLR) auditory evoked responses. Hear Res 1987; 26: 11-20. 8. Suzuki T, Hirabayashi M. Age-related morphological changes in auditory middle-latency response. Audiology 1987; 26: 312-02. 9. Barnett AB, Ohlrich ES, Weiss IP, Shanks B. Auditory evoked potentials during sleep in normal children from ten days to three years of age. Electroencephalogy Clin Neurophysiol 1975; 39: 29-41. 10. Schneider BA, Trehub SE, Morrongiello BA, Thorpe LA. Developmental changes in masked thresholds. J Acoust Soc Am 1989; 86: 1733-42. Address for correspondence: J os J. Eggermont, Department of Psychology, The University of Calgary, 2500 University Drive, Calgary, Alberta, Canada T2N IN4
