International Journal of Pediatric Otorhinolaryngology, 10 (1985) 221-228
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Elsevier POR 00339
Hearing assessment in developmentally impaired infants" classical conditioning as a supplement to brainstem-evoked response audiometry (BERA) Giulio E. Lancioni 1, Gerrit A. Hoogland 1, Paul M. Smeets 2, Graziano Brozzi 3.4, Mario V. Scoponi 3.4, Luigi Piattella 3 and Nelia Zamponi 3 I Unioersity of Nijmegen and -" Unioersity of Leiden (Holland); and "~Salesi Children's Hospital and 4 Lega F. D'Oro Research Center (Italy)
(Received June 3rd, 1985) (Accepted September 1st, 1985)
Key words: brainstem-evoked response audiometry (BERA) - classical conditioning - conditioned re-
sponse - conditioned stimulus - developmentally impaired infants - hearing assessment unconditioned response - unconditioned stimulus
Summary T h e b r a i n s t e m - e v o k e d r e s p o n s e a u d i o m e t r y ( B E R A ) is p r o b a b l y the most c o m m o n a p p r o a c h to h e a r i n g assessment in high-risk a n d d e v e l o p m e n t a l l y h a n d i c a p p e d infants. It is u s u a l l y suggested, however, that B E R A s h o u l d not be the sole a s s e s s m e n t m e t h o d . In a n a t t e m p t to d e t e r m i n e an effective s u p p l e m e n t to B E R A , the p r e s e n t s t u d y e v a l u a t e d a classical c o n d i t i o n i n g p r o c e d u r e with d e v e l o p m e n t a l l y i m p a i r e d babies. W i t h i n this p r o c e d u r e , different tones served as c o n d i t i o n e d stimuli while an a i r - p u f f was used as the u n c o n d i t i o n e d stimulus. Results i n d i c a t e that this p r o c e d u r e c o u l d b e successfully a p p l i e d with a l m o s t all of the babies.
Introduction T h e i m p o r t a n c e o f h e a r i n g a s s e s s m e n t in high-risk or d e v e l o p m e n t a l l y i m p a i r e d i n f a n t s a n d y o u n g c h i l d r e n as well as the difficulties e n c o u n t e r e d in this a r e a have b e e n widely d e b a t e d [10,14,16,29]. T o alleviate a s s e s s m e n t p r o b l e m s , a new tech-
Correspondence: G.E. Lancioni, Institute of Orthopedagogics, University of Nijmegen, Erasmusplein 1, 6500 HD Nijmegen, Holland.
0165-5876/85/$03.30 © 1985 Elsevier Science Publishers B.V. (Biomedical Division)
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nique has been introduced in the last decade, the (BERA) brainstem-evoked response audiometry [9,11,20,21]. This technique has been considered a breakthrough in the field for two reasons. First, without being invasive, it allows evaluation with virtually all subjects. Second, it is assumed that the electric response threshold obtainable through this technique is a reliable indicator of the hearing threshold of the subject. Despite these advantages, caution has been expressed with regard to the use of BERA as the sole assessment method. One major point of concern is that the results of BERA reflect the electrophysiological events taking place in the peripheral auditory pathway. Thus, a positive answer concerning the subject's hearing ability should be given with the reservation of possible impairment of higher auditory structures [14,15,24,29,30]. This reservation could be seen as rather serious in individuals with severe (neurological) developmental disorders. Therefore, particularly in these cases, BERA should be supplemented with additional measures. At present, electrophysiological methods may not be considered suitable to provide those supplementary measures [2,7,18,26]. Behavioral methods which might serve for such purpose (although in need of closer investigation) are: assessment of orienting responses, and conditioning to sound cues [19,23,28]. Orienting responses seem to be rather primitive forms of reaction, when compared with conditioned responses [1,5,17]. Moreover, low-functioning infants may often fail to show clearly observable orienting responses such as head turning [3,8,25,28]. Conditioned responses may be considered fairly comprehensive measures of hearing functioning. They involve (a) association of sound with a subsequent event, and thus (b) anticipation of the event on the basis of the sound signal [17,19,27]. Conditioned responses to sound have been established with normal infants [4,22] and a variety of retarded subjects [8,13]. Procedures were usually based on operant conditioning with visual or tangible/edible reinforcement. The same procedures could prove difficult or unsatisfactory with infants affected by severe developmental disorders. In fact, these infants may frequently show limited or variable interest for environmental appetitive reinforcers. A possibility to overcome these difficulties could be offered by classical conditioning since it need not rely on the aforementioned forms of reinforcement. The purpose of the present study was to investigate whether a classical conditioning procedure similar to that reported by Lancioni and Hoogland [12] could be effectively used with developmentally impaired babies. Conditioning (implemented in combination with BERA) involved tones of 1000, 2000 and 4000 Hz.
Materials and Methods
Subjecls Forty-two subjects ranging from 5.7 to 19.1 months of age (X = 10.1 months) were selected for the study. All babies (recruited at the Salesi Children's Hospital, Italy) presented neurological problems coupled with developmental delays. Their behavioral functioning was estimated to be between 2 and 8 months with a mode of 4-5 months. Their medical histories included, among others, prenatal infections,
223 perinatal traumas, hydrocephalus, progressive degenerative diseases, genetic anomalies. Prior to or concomitant with the conditioning, babies were exposed (without sedation) to BERA. This test was carried out with an Amplaid MK 4. Ag/AgCI disc electrodes were placed on the left and right earlobes and at the vertex of the skull. Alternating clicks (21/s) were used. For each intensity level, 2048 responses were averaged using filter settings of 200-2000 Hz. Both ears were tested separately, until a level of 40 dB SPL. The results of BERA were in no case known to the experimenter and observers involved in the conditioning procedure.
Apparatus for the conditioningprocedure The apparatus used in this study was similar to that described by Lancioni and Hoogland [12]. It consisted of an electronic control device connected to an Amplaid 300 audiometer equipped with T D H 39 headphones, and to a cylinder filled with compressed air. The electronic device controlled (a) the onset and duration of the tones, (b) the onset and duration of air-puffs obtained from the cylinder, (c) the intertrial and interstimulus intervals (the latter intervals consisted of the time intercurring between the onset of the tone and the onset of an air-puff), (d) the visual display indicating the number of trials performed within a session. The air-puffs, channelled through a plastic tube of 2.5 mm in diameter, hit the corner of the infant's eye or inflated a balloon held at the side of the infant's eye. An air-puff of 0.5 s used against the corner of the eye could have a volume of.about 1 / 9 - 1 / 2 of a liter. An air-puff of the same length used to inflate a balloon could reach higher volumes.
Experimenter, observers and reliability One experimenter carried out the conditioning procedure with all babies. Two observers (one at a time) assisted in the application of the procedure.'That is, they cooperated (with mothers) in maintaining the babies quiet, and meanwhile recorded the babies' responses during test trials. To this end, the observer had a recording sheet that reported trial numbers and empty boxes divided into two columns. At each test trial, she (a) recorded (in the box next to the trial number) whether the subject had responded or had failed to do so, (b) looked to the experimenter who signalled a score, then (c) recorded that score in the box adjacent to the one she had used. If the test trial was called off by the experimenter (e.g., the baby was engaging in gross movement, fussing, having eyes semiclosed), the observer crossed the boxes corresponding to that trial. The reliability was computed over the positive responses, or (if a baby failed to condition) over all test trials. The formula was agreements divided by agreements plus disagreements, times 100.
Experimental conditions The study was carried out in a quiet room of the hospital where the babies had been recruited. Initially, there were baseline trials. Then, conditioning (training and test trials) took place. A learning control strategy was also planned. Babies were on their mothers' lap or on a baby chair. To minimize fussing behavior, different soothing events (e.g., toys, vibrotactile stimulation, liquids) could be used at any stage of the study.
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Baseline trials. Within the initial trials, at least 3 tones (representing intensityfrequency levels applied for conditioning) were presented. The aim was to ensure that they were not followed by any (or any recurrent) defensive reactions (e.g., blinking). They were presented through one headphone held close to the infant's ear. The headphone set was not employed to avoid bothering/irritating the baby. A second group of trials served to decide how the air-puff had to be used (i.e., against the corner of the eye or channelled into a balloon). At first, puffs of air were presented on legs and arms, eventually on the corner of the eye. If the subject showed irritability, the balloon was employed. The intensity of the puff was regulated to obtain a fairly strong defensive reaction (unconditioned response), that is, total closure of the eyes or repeated blinking, possibly accompanied by turning of head. During conditioning, re-adjustments of the puff (and also the elimination of the balloon) were possible. Conditioning. Sessions were divided by intervals ranging from 10 rain to several hours. Every session contained a maximum of 16 trials implemented at variable intervals. The average intertrial interval was 20 s, but it could extend to 30 s while test trials were presented. The headphone was held in the same position as in baseline. The tube to deliver the air-puff or the balloon were held approximately 10-15 cm to the side of the baby (the same side as the ear used for presenting the tones). Training trials were conducted according to a delayed paradigm. That is, a 0.5-s air-puff (unconditioned stimulus) overlapped with the final portion of the 1.5-s tone (conditioned stimulus). Testing occurred by means of trials in which the unconditioned stimulus was omitted (i.e., only the tone was presented). At the beginning, the subjects were exposed to training with a tone of 2000 Hz and 75-80 dB HL. A maximum of 90 trials could be provided. Test trials were at first sporadic (usually after every 4 - 8 training trials). As soon as the baby had shown the first conditioned response (i.e., defensive reaction within a test trial), test and training trials were presented in ratios of 1:1 to 1:2. These ratios could momentarily be changed in 1 : 3 to 1 : 5 if the subjects failed to respond on the subsequent (two) test trial(s). Once the subjects had reached test criterion (i.e., 3 conditioned responses on 3 consecutive test trials, or 4 conditioned responses on 5 consecutive test trials, without responding between trials), the conditioned stimulus was changed. That is, a tone of the same intensity, but at the frequency of 4000 Hz (in a few cases of 1000 Hz) was presented. A maximum of 45 training trials were now available. Subjects received the first test trial after 1 - 4 training trials. The achievement of test criterion was followed by the use of a third conditioned stimulus, normally a tone of 1000 Hz (in a few cases of 4000 Hz) and 75-80 dB. For a small group of babies, the procedure comprised only the aforementioned 3 tones. For most subjects, however, conditioning continued with a tone of 2000 Hz and 65-70 dB. Several of these subjects (after achieving test criterion) were presented with the same tone on the contralateral ear, that is, the ear never used during previous conditioning. Learning control strategy. This strategy applied for subjects who failed to reach test criterion on the first tone used (i.e., 2000 Hz and 75-80 dB) within the 90 training trials available. The learning control strategy involved training and test
225 trials with the presentation of a visual stimulus (a red square) as conditioned stimulus. If the subjects failed to achieve test criterion with this strategy (i.e., 5 conditioned responses over 6 test trials) within 90 training trials, the procedure was terminated. If the subjects succeeded to achieve test criterion, conditioning with the tone was reinstated for at least 25 trials.
Results Of the 42 babies selected for the study, 3 were dropped because of high levels of irritability or difficulty to obtain a clear and consistent unconditioned response. The percentages of experimenter-observer agreement in recording the responses of the remaining 39 babies were comprised between 72 and 100 (principally, in the range 80-100). With regard to these babies, 34 showed successful acquisition of conditioned responses to sound, 5 exhibited failures. The performance of the former infants is summarized in Table I. The number of training trials the 34 babies needed to reach test criterion on the first tone (i.e., 2000 Hz at 75±80 dB) varied between 10 and 83 with a mean of 36. The training trials to reach test criterion on both the following tones (i.e., 4000 and 1000 Hz at 75-80 dB) totalled 7 - 5 2 with a mean of 21. With regard to the 26 babies who continued the conditioning procedure with a tone of 2000 Hz and 65-70 dB, the training trials required for reaching test criterion were 3-26 with a mean of 11. Finally, the 8 babies who were presented with the aforementioned tone also on the contralateral ear needed 6 - 2 2 (mean of 12) training trials. The BERA results were normal in 31 of the 34 babies, missing (due to irritability) in two babies, and abnormal in one baby. This baby (who had successfully conditioned to tones of 80 as well as 70 dB presented to the left ear) had no brainstem responses below the 80 dB (SPL) level (left ear) or the 100 dB level (right
TABLE I TRAINING TRIALS REQUIRED TO REACH TEST CRITERION ON DIFFERENT TONES Tones 2000 Hz 75-80 dB 4000 & 1000 Hz 75-80 dB 2000 Hz 65-70 dB 2000 Hz 65-70 dB (C0ntralateral ear)
Subjects (no.)
Training trials (Range)
(Mean)
34
10-83
36
34
7-52
21
26
3-26
11
8
6-22
12
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ear). A follow-up BERA, however, showed responses at 45 and 85 dB on the left and right ear, respectively. As to the 5 subjects who exhibited failures in the conditioning procedure, the following data were obtained. One of them achieved test criterion on the first tone used. Yet, he failed on the second tone (i.e., 1000 Hz and 75 dB). His BERA showed responses at 80 dB (SPL) on the left ear (the one used for conditioning) and at 100 dB on the right ear. Two other subjects failed to condition to the first tone, while were successful on the learning control strategy. The BERA of these babies indicated deafness. The last two subjects failed to condition on the first tone, and also failed on the learning control strategy. Their BERA appeared normal.
Discussion The findings indicate that the classical conditioning procedure could be implemented with almost all the babies included in the study. This evidence seems relevant since many of the babies showed very limited or variable interest for" the surrounding environment. Thus, the use of a procedure based on environmental appetitive reinforcers might have encountered serious difficulties [4,8,28]. In view of the findings, one may consider the classical conditioning procedure a suitable supplement to BERA assessment in developmentally impaired infants. Within such a perspective, the practical question immediately arises of how the conditioning procedure should be used or, more specifically, of which sound frequencies and intensities it should involve. Given the preliminary nature of the present study and the limited knowledge about the relations between conditioning and sound perception, answers to the question can only be tentative. One could assume that for babies with normal BERA, conditioning with 2 - 3 sound frequencies (even at high levels of intensity) may be sufficient. In these cases, in fact, the emphasis might be on ensuring that the subject is able to attach signalling value to sounds. In babies with abnormal BERA, on the other hand, conditioning may be extended over tones of different frequencies and intensities. Although in the present study only relatively high intensities were used, it would seem possible that the same conditioning procedure be extended to lower intensities [12]. In these situations, the presence of conditioned responses to different sounds would rectify the indications of BERA [6,11]. On the contrary, lack of conditioned responses to sound (in the presence of conditioned responses to visual stimuli, i.e., the learning control strategy) would strongly support BERA results. A completely different situation would emerge if the baby fails to condition to sound but also to visual stimuli (i.e., as observed in two subjects of the present study). In those circumstances, any conclusion about hearing functioning would have to be postponed to subsequent assessments. In summary, it can be argued that classical conditioning may be accepted as a supplementary method in hearing assessment. However, new research is needed to establish how far conditioning has to be extended (i.e., with regard to sound
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frequencies and intensities) in connection with different BERA results. On the basis of this research, evidence will also be gathered as to the real cost (i.e., time-cost) of the conditioning procedure. Eventually, ways could be investigated to reduce such cost.
Acknowledgements This research was supported by funds from the Lega F. D'Oro Research Center (Italy). The authors are very grateful to Prof. P. van den Broek and Prof. J.J. Eggermont for their helpful comments on the paper.
References 1 ,~db.m, G., Perception, Consciousness, Memory: Reflections of a Biologist, Plenum Press. New York, 1980. 2 Arslan, E., Prosser, S. and Michelini, S., Simultaneous recording of auditory evoked potentials, Scand. Audiol., 13 (1984) 75-81. 3 Barr, B., Stensland Junker, K. and Sw~ird, M., Early discovery of hearing impairment: a critical evaluation of the BOEL test, Audiology, 17 (1978) 62-67. 4 Berg, K.M. and Smith, M.C., Behavioral thresholds for tones during infancy, J. Exp. Child Psychol., 35 (1983) 409-425. 5 Butter, C.M., Neuropsychology: The Study of Brain and Behavior, Brooks/Cole, Belmont, CA, 1968. 6 Cornacchia, L., Vigilant, E. and Arpini, A., Comparison between brainstem-evoked response audiometry and behavioral audiometry in 270 infants and children, Audiology, 21 (1982) 359-363. 7 Donchin, E., Heffley, E., Hillyard, S.A., Loveless, N.. Maltzman, 1., Ohman. A., R6sler, F., Ruchkin, D. and Siddle, D., Cognition and event related potentials. II. The orienting reflex and P300, Ann. N.Y. Acad. Sci., 425 (1984) 39-57. 8 Greenberg, D.B., Wilson, W.R., Moore, J.M. and Thompson, G., Visual reinforcement audiometry (VRA) with Down's syndrome children, J. Speech Hear. Disord., 43 (1978) 448-458. 9 Hecox, K. and Galambos, R., Brain stem auditory evoked responses in human infants and adults, Arch. Otolaryngol., 99 (1974) 30-33. 10 Knobeloch, C. and Kanoy, R.C., Hearing and language development in high risk and normal infants, App. Res. Ment. Retard., 3 (1982) 293-301. 11 Kraus, N., Ozdamar, 6., Stein, L. and Reed, N.. Absent auditory brain stem response: peripheral hearing loss or brain stem dysfunction?, Laryngoscope, 94 (1984) 400-406. 12 Lancioni, G.E. and Hoogland, G.A., Hearing assessment in young infants by means of a classical conditioning procedure, int. J. Pediatr. Otorhinolaryngol,, 2 (1980) 193-200. 13 Lloyd, L.L., Spradlin, J.E. and Reid, M.J., An operant audiometric procedure for difficult-to-test patients, J. Speech Hear. Disord., 33 (1968) 236-245. 14 Mj6en, S., ABR in pediatric audiology, Scand. Audiol. Suppl., 13 (1981) 141-146. 15 Mj6en, S., Langslet, A., Tangsrud, S.E. and Sundby, A., Auditory brainstem responses (ABR) in high-risk neonates, Acta Paediatr, Scand., 71 (1982) 711-715. 16 Mokotoff, B., Schulman-Galambos, C. and Galambos, R., Brain stem auditory evoked responses in children, Arch. Otolaryngol., 103 (1977) 38-43. 17 Ohman, A,, The orienting response during Pavlovian conditioning. In D. Siddle (Ed.), Orienting and Habituation: Perspectives in Human Research, Wiley, New York, 1983, pp. 315-369. 18 Parving, A., Elberling, C. and Salomon, G., Slow cortical responses and the diagnosis of central hearing loss in infants and young children, Audiology, 20 (1981) 465-479. 19 Ravizza, R.J. and Belmore, S.M., Auditory forebrain: evidence from anatomical and behavioral
228
20 21 22 23 24 25 26 27 28 29 30
experiments involving human and animal subjects. In R.B. Masterton (Ed.), Handbook of Behavioral Neurobiology, Vol. 1, Plenum Press, New York, 1978, pp. 459-501. Schulman-Galambos, C. and Galambos, R., Brain stem auditory evoked responses in premature infants, J. Speech Hear. Res., 18 (1975) 456-465. Schulman-Galambos, C. and Galambos, R., Brain stem evoked response audiometry in newborn hearing screening, Arch. Otolaryngol., 105 (1979) 86-90. Sinnott, J.M., Pisoni, D.B. and Aslin, R.N., A comparison of pure tone audiometry thresholds in human infants and adults, Infant Behav. Dev., 6 (1983) 3-17. Skinner, P. and Glattke, T.J., Electrophysiologic response audiometry: state of the art, J. Speech Hear. Disord., 42 (1977) 179-198. Stein, L.K., An electrophysiological test of infant hearing, Am. Ann. Deaf, 121 (1976) 322-326. Stensland Junker, K., Barr, B., Maliniemi, S. and Wasz-H0ckert, O., BOEL screening: a program for the early detection of communicative disorders, Audiology, 17 (1978) 51-61. Sutton, S. and Ruchkin, D.S., The late positive complex: advances and new problems, Ann. N.Y. Acad. Sci., 425 (1984) 1-23. Thompson, R.F., Introduction to Physiological Psychology, Harper International Edition, New York, 1975. Thompson, G. and Folsom, R., Hearing assessment of at-risk infants, Clin. Pediatr., 20 (1981) 257-261. Wong, D. and Shah, C.P., Identification of impaired hearing in early childhood, Can. Med. Assoc. J., 121 (1979) 529-546. Worthington, D.W. and Peters, J.F., Electrophysiologic audiometry, Ann. Otol. Rhinol. Laryngol., 89 (5 Pt 2 Suppl. 74) (1980) 59-62.