Comparison of the developmental changes of the brainstem auditory evoked response (BAER) in taurine-supplemented and taurine-deficient kittens

0736-5748/91 $3.00+0.00 Pergamon Press plc ISDN

Int. J. Devl. Neuroscience, Vol. 9, No. 6, pp. 571-579, 1991.

Printed in Great Britain.

C O M P A R I S O N OF THE D E V E L O P M E N T A L C H A N G E S OF THE BRAINSTEM A U D I T O R Y E V O K E D RESPONSE (BAER) IN T A U R I N E - S U P P L E M E N T E D A N D T A U R I N E - D E F I C I E N T KITTENS M.-H. VALLECALLE-SANDOVAL,*'I" G. HEANEY,~ E. SERSEN~ and J. A. STURMANt tDepartment of Developmental Biochemistry, ~:Departmentof Psychology, Institute for Basic Research in Developmental Disabilities, 1050 Forest Hill Road, Staten Island, NY 10314, U.S.A. (Received 13 March 1991; in revised form 22 July 1991; accepted 26 July 1991)

Ahstraet--A similar development of the brainstem auditory evoked response is present in taurinesupplemented and taurine-deficient kittens between the second postnatal week and the third month of life. Between birth and the second postnatal week kittens from mothers fed the 1% taurine diet showed earlier maturation of the brainstem auditory evoked response as indicated by lower threshold, shorter P1 latency and shorter central conduction time when compared to the kittens from mothers fed the 0.05% taurine diet. These results suggest an important role of taurine in the anatomical and functional development of the auditory system. Key words: BAER, BAER latency, hearing threshold, nutrition, taurine, kitten.

It has long been known that taurine is one of the most abundant free amino acids present in m a m m a l s , in some tissues being the free amino acid present in the greatest concentration, e.g. as in the mature retina 32'4t'53 and the developing brain. 55'58 The concentration of taurine in fetal and newborn mammalian brain is several-fold greater than in mature brain of the same species and the decrease occurs approximately by the time of weaning, 57 therefore, the possible role of taurine on the development of the m a m m a l i a n nervous system has been the subject of much recent research.55'56'sa'62This interest was heightened by the observation that cats fed a diet deficient in taurine become taurine deficient and suffer visual dysfunction and retinal degeneration. 2't9'45"47'48"5°Lake et al. 33 reported a significant reduction of optic nerve fiber density in taurine-depleted rats. It is now widely accepted that dietary taurine is essential for cats, and possibly for primates, including humans. 29 Female cats deprived of taurine have reproductive failure, and surviving kittens have low-birth-weight, p o o r growth rates and lowered postnatal survival rates as c o m p a r e d to taurine-supplemented kittens. 6°-63 Neuronal development is impaired. The cerebellar external granule layer is still present eight weeks after birth, 6°'6t precursor cells from the germinative ventricular region fail to migrate and differentiate normally resulting in an abnormal visual cortex development. 39'4° Kittens born from taurine-deficient mothers have decreased retinal and tapetal taurine content at weaning. 24 Rhesus monkeys raised from birth to 26 months old on a low-taurine human infant formula showed degeneration of the outer segments of their retinal cone photoreceptor cells. 59 The concentration of taurine in plasma and urine of human p r e t e r m infants fed synthetic formulas derived from cow's milk (which contains little or no taurine) decreases with time after birth, whereas similar infants fed pooled human milk did not exhibit such decreases. 15 Infants fed totally using solutions of nutrients administered parenterally (which contain no taurine) also have reduced concentrations of taurine in their plasma and have ophthalmologically and electrophysiologically demonstrable retinal damage.16-~a'46 In addition to its role in vision, the high concentration of taurine in the organ of Corti (in the mouse it is higher than any other amino acid 7) also suggests a possible role in the auditory system. Despite the extensive review on the biology of taurine 68 and its electrophysiological actions, 23 very little has been reported on the function of taurine in the cochlea, which will help to determine the effect of taurine in the auditory system. Since its description by Jewett, 25, the brainstem auditory evoked response ( B A E R ) has become a valuable non-invasive tool to assess auditory function in a variety of both adult and immature vertebrate species including man, 2°'3t'54 r a t , 4'26'42 cat, t4'26"35'51"66 ferret, 28"37 rhesus monkey, 1"9 mouse, 21'22 gerbil, 52 rabbit, 36 guinea pig, 27'65 hamster. 49 *Author to whom correspondence should be addressed. 571

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Brainstem auditory evoked potentials are the far-field reflection of the sequential activation of the auditory pathway, providing a unique opportunity to study the development from the acoustic nerve to the inferior colliculus in the same subject from birth to maturity. The cat is more dependent on dietary taurine and suffers greater taurine depletion than do other species. Since significant effects on the B A E R have been shown in human preterm infants fed formula without taurine 64 and in ferrets depleted of taurine by giving 13-alanine in the drinking water, 7 we decided that the cats would be a suitable model with which we could explore this phenomena further. We utilized threshold and wave latency measures of B A E R in kittens born from taurine-supplemented and taurine-deficient mothers to define the possible effects of taurine on the maturation of both peripheral (e.g. the cochlea) and central portions of the auditory pathway. EXPERIMENTAL PROCEDURES Materials Twenty-three female kittens from 12 litters, born and raised locally in our animal colony, were studied from the fourth postnatal week through 12 weeks old. Of these, 9 kittens from 5 litters ( N - l , 2, 3, 1,2), were studied from the first postnatal week, and 6 kittens from 5 litters ( N - I , 1, 1. 1, 2), were studied from the second postnatal week. Kittens used in this study were bred as follows: when in estrus, females were caged with a male for one week; conception was defined as the middle of this period, and the pregnancy confirmed by x-ray 4-6 weeks postconception. Kittens were nursed by their mothers as follows: Ten kittens of mothers fed the diet supplemented with 1% taurine and nine of mothers fed the diet supplemented with 0.05% taurine. 62 Three kittens of mothers fed a taurine-deficient diet with 0.02% taurine, and one kitten of a mother fed a taurine-free diet. Due to the low survival rate of kittens of mothers fed the taurinedeficient diet we were unable to increase these samples, and they were included in one group which will be referred to as 'deficient'. Their increased susceptibility to anesthesia also limited their testing; therefore, none could be tested before two weeks of age and only one at two weeks old. All kittens were in good health and showed clear external ear canals. None had any history of neurologic or audiologic disease. Stimuli The click stimuli consisted of 0.1 msec square wave rarefaction clicks computer generated at a rate of 10.3 Hz. They were delivered monaurally through a 5 cm length of plastic tube coupled with a specially constructed earpiece and inserted into the entry of the kitten's left and then right ear canal. Maximum click intensity was 80 dB peak equivalent SPL (peak SPL) determined at the earpiece opening with a Bruel and Kjaer sound level meter, 2230, and it was varied over 50 dB range from 80 to 30 dB peak SPL. Recording Procedure Stainless steel subdermal electrodes were inserted subcutaneously at vertex and left and right mastoids. An electrode on the neck served as ground. Electrode resistance was below 3 kohms. At the time of recording, the kittens > 2 weeks old were anesthetized with ketamine administered intramuscularly in doses of 10 mg/kg diluted in 1 cc of saline solution. Ketamine was chosen because of its described lack of effect on B A E R waveform and latency. 4 They were placed on a hammock with the head supported by an adjustable platform. Signals were recorded using Grass 7P511J amplifiers with a gain of 200 k, filtered with a bandpass of 100 Hz-3 kHz, and averaged on line with a PDP 11-23 computer. The analysis epoch for each channel was 12.8 msec, the sampling rate was 109 kHz, and all averages were based on 256 sweeps. An artifact rejection algorithm was used to reject overload conditions. Latency measures were determined off-line from the click onset to the vertex-positive and vertex-negative peak of each prominent wave, and scored blindly with respect to taurine status by two investigators independently. As established by others, z5 vertex-positive peaks (upward deflections in our figures) were designated in sequence of time with arabic numerals. Negative peaks

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were assigned the number of the preceding positive peak. The prefix P or N denotes whether a peak is vertex-positive or vertex-negative. Testing began at a click intensity of 80 dB peak SPL; the intensity was then reduced in 20 dB steps until was no longer discernible, then, increased by 10 dB. The lowest click intensity at which P4 was detectable on at least two trials was designated threshold. A series of trials with intensities decreasing in 20 dB steps was then presented in order to provide duplicate recordings for each intensity. Ipsilateral and controlateral responses were obtained from left ear stimulation in each kitten. Recordings in which the ipsilateral BAER was clearly recognizable at 50, 70 and 80 dB peak SPL were included in our analysis. Mean values were compared to those of adult cats fed the 0.05% taurine diet which has been defined to be the 'control' diet. 62

Statistical Analyses Differences in thresholds and latencies between the taurine groups were evaluated by means of analyses of variance using the BMDP statistical analyses package. 8 All kittens were tested only at 4 and 8 weeks and these data were analyzed with group and age as independent variables using program 2V. Separate analyses, using program 7D, were performed for the remaining time periods using the data that were available. Results were considered statistically significant if P -< 0.05. RESULTS

Maturation of the BAER Threshold The BAER thresholds to clicks as a function of postnatal age for each taurine group are plotted in Fig. 1. The 1% taurine kittens recorded before the second postnatal week showed lower threshold (47.50 dB peak SPL +- 2.57) than the 0.05% taurine kittens (64.67 dB peak SPL+4.62) and this difference was statistically significant (F= 7.95,p = 0.03). On the second postnatal week, the average threshold for all kittens was between 62 and 53 dB peak SPL improving drastically over the following two weeks. By the fourth week of age, the mean threshold for all kittens was within 1 SO of the adult control cat value (42.50 dB peak SPL) and remained at it throughout the third postnatal month. No group differences were statistically significant.

Maturation of BAER Waveform BAERs recorded from a single kitten for each taurine group between 2 postnatal weeks and 12 postnatal weeks are shown in Fig. 2; stimuli were 70 dB peak SPL clicks. Between 7 and 11 postnatal days, 8 kittens (5 fed a 0.05% taurine diet and 3 fed a 1% taurine diet) were recorded; BAERs were present in 6 of them only at higher intensities (80 and 70 dB peak SPL) and possessed four waves which reached adult-like waveform morphologies by the second postnatal week. Each of these waves possessed a positive and a negative deflection clearly identifiable in all kittens. The eight subsequent positive and negative peaks were labeled as PIN1 through P4N4. Sometimes, among the three groups of animals, a fifth wave, labeled P5N5, of small amplitude and not consistent was present but was not analyzed in this investigation.

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Fig. 2. A typical BAER development in a taurine-deficient (A), 0.05% taurine (B) and 1% taurine kitten (C), recorded at 2, 4, 8 and 12 postnatal weeks. Stimuli: 10.3/see monaural rarefaction clicks at 70 dB peak SPL. All averages were based on 256 sweeps. Recording electrodes: left mastoid to vertex (CZM 1). The four vertex-positive potentials are labeled from 1-4 and plotted upwards. Zero time indicates the time of the click sound at the earphone. An amplitude of i p,V is indicated by the calibration marker. B A E R Wave Latency Maturation In all kittens, B A E R latencies of waves 1-4 declined abruptly throughout the first four postnatal weeks. After the fourth postnatal week the period of fast latency decline was followed by a period of progressive decline that continued into the second or third postnatal month, depending on the wave studied. The rate of developmental change of all the mean B A E R peak latencies is shown in Fig. 3. In all kittens, from the second postnatal week to the third postnatal month, P1 presented a smaller absolute decrease in latency (0.97 ms, 1.03 ms, 0.36 ms, in taurine-deficient, 0.05% and 1% taurine kittens, respectively), when compared to P4 (2.02 ms, 2.76 ms, 1.91 ms in taurinedeficient, 0.05% and 1% taurine kittens, respectively), but P1 attained the adult control cat value (mean = 1,85 ms) at an earlier age (four postnatal weeks) than P4 (eight postnatal weeks). N4 presented a larger decrease in latency (2.17 ms, 3.34 ms, 2.14 ms in taurine-deficient, 0.05% and 1% taurine kittens, respectively) when compared to the other three negative peaks which had a symmetrical decrease in latency. The B A E R latencies for each wave did not differ between the three groups at 4 nor at 8 weeks of age; although, before the second postnatal week the 1% taurine kittens possessed shorter P1

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latency when compared to the 0.05% taurine kittens; this difference was statistically significant (F-- 7.84, p = 0.05).

Latency Maturation as a Function of Intensity Changes in mean values of latency versus intensity functions for each peak, positive as well as negative, are plotted as a function of postnatal age in Fig. 4. The slopes of latency versus intensity functions were steep at young ages (2 to 4 postnatal weeks) in the three groups of kittens and became shallower as kittens matured. With a 20 dB decrease in click intensity (from 70 dB peak SPL to 50 dB peak SPL), P1 decreased just 0.03 ms in the taurine-deficient kittens at 8 weeks compared to 0.19 ms and 0.23 ms in the 0.05% and 1% taurine kittens. Maturation of the Central Conduction Time (CCT) Central conduction time (CCT) is defined as the peak 4 minus peak 1 latency (P4-P1) time interval, and is generally considered as a specific index of neural function being independent of peripheral auditory factors which are indexed by peak 1 latency. Fig. 5 shows the CCT, the P1 and the P4 mean values for the three groups of kittens, as a function of age; they were obtained in response to clicks at 70 dB peak SPL and compared to adult control cat means. In all kittens, the mean value for peak 1 latency was within 1 SD of the mean of the adult control cat value by the fourth postnatal week, whereas peak 4 latency was within 1 SD of the mean adult control cat value (2.35 ms) by the eighth postnatal week. As a result of the asymmetrical rate of developmental change in the peak latencies, the CCT decreased with age, in general, but the difference in its detailed behavior only approached statistical significance ( F = 2.94, p = 0.08) in the three groups of kittens. The mean value of the CCT of the 1% taurine kittens recorded before the second postnatal week was significantly shorter ( 4. 05- 0. 42 ms) when compared to the 0.05% taurine kittens ( 4 . 4 8 - 0.16 ms), and followed a steep decrease until reaching the fourth postnatal week; at this age, the averaged CCT of the 1% taurine kittens was shorter (2.96 - 0.23 ms), but not significantly so, relative to 3.18 - 0.24 ms in the taurine-deficient kittens, and to 3.03 -+ 0.18 ms for the 0.05% taurine kittens ( F = 2.58, p = 0.10). At eight weeks of age, all three groups reached an averaged CCT within about 1 SD of the adult control cat value.

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DISCUSSION The present investigation confirms that the B A E R is a relatively non-invasive tool for obtaining longitudinal data on auditory brainstem maturation in developing kittens. The general maturation trends in our kittens are similar to those reported in other vertebrate species including cats subjected to similar investigation. 37"51'66"67The three groups of kittens show a similar development in

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their BAER thresholds and peak latencies between the second postnatal week and the third month of life. Before the second postnatal week, the kittens of mothers fed 1% taurine diet showed earlier BAER maturation as indicated by lower threshold, shorter P1 latency and shorter CCT when compared to the kittens of mothers fed 0.05% taurine diet. Extensive biochemical data on taurine-deficient and kittens of mothers fed 0.05% taurine diet was reported. 63 The taurine concentration in all brain regions is very sensitive to their mother's diet: the higher the maternal diet is in taurine, the greater the taurine content of the offspring. The difference between the taurine-supplemented and the taurine-deficient kittens might have been substantially greater if a sample of kittens fed the 0% taurine diet could have been included in our study. This limitation was due to two factors: female cats fed the taurine-deficient diet have difficulty in maintaining pregnancy to term and those which are carried to term result in low-birth-weight kittens, 6°'62 with a high mortality rate. In addition, these kittens have a markedly reduced ability to withstand the anesthesia necessary for the recordings. While behavioral, H'38 and acoustically evoked cochlear potentials44 may be present in some kittens near birth and between birth and 6 days of life, suggesting a functional cochlea, such kittens are characterized by an extremely immature auditory function ;66 the cochlea as the middle ear cavity are anatomically immature, therefore, the acoustic transmission of energy is poor compared to that in adult. 3 The endocochlear potentials recorded from kittens during the first week of life show low amplitudes and become mature by the end of the first month of life.~2 Between the second and fourth postnatal week, the differentiation of the auditory system is great, m anatomical modifications of the cochlea and middle ear occur during at least the first postn a t a l m o n t h . 3°'34'43 Therefore, the observed sharp decline of thresholds between the end of the first postnatal week and the fourth week of life is primarily associated with maturation of the peripheral auditory system, the endocochlear potential growth being the main specific developmental change that corresponds with improving thresholds, occurring simultaneously with the nearly completed anatomical maturation of the basal cochlea and the resorptions of middle ear fluids. 66 The early stages of development of the auditory system in the cats are characterized by large reductions in BAER latencies. 67 For the three groups of kittens, the mean latency of P1 reached the adult control cat mean by the fourth week of age, while P4 was still 15-20% longer than the adult control cat mean for the supplemented and the taurine-deficient kittens, respectively. The earlier shortening of P1 latency suggests changes in peripheral processing while the behavior of P4 suggests that the central portions of the auditory system continue undergoing maturational changes throughout the third month of life.

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T h e r a t e o f t h e B A E R ' s l a t e n c y d e c l i n e d u r i n g t h e d e v e l o p m e n t c o u l d b e d e t e r m i n e d by s e v e r a l f a c t o r s (i.e. c o c h l e a r t r a v e l t i m e to t h e a r e a o f t h e b a s i l a r m e m b r a n e r e s o l v i n g t h e signal, s y n a p t i c d e l a y s , c o n d u c t i o n v e l o c i t i e s , m y e l i n a t i o n ) . W a l s h et al. 67 s u g g e s t t h a t t h e B A E R l a t e n c y d e l a y o f w a v e 1 in y o u n g k i t t e n s is m a i n l y r e l a t e d to d e l a y s w i t h i n t h e c o c h l e a . T h e m a j o r e v e n t t h a t o c c u r s e x t e n s i v e l y d u r i n g t h e p o s t n a t a l d e v e l o p m e n t is m y e l i n a t i o n , a n d it is d i r e c t l y r e l a t e d to c o n d u c tion v e l o c i t i e s . ~3 T y s o n et al. 64 d e m o n s t r a t e d t h a t h u m a n infants__<1300 gr birth w e i g h t fed a t a u r i n e - s u p p l e m e n t e d d i e t h a d s h o r t e r B A E R l a t e n c i e s at 37 w e e k s p o s t m e n s t r u a l a g e , c o n s i s t e n t w i t h o u r f i n d i n g o f s h o r t e r C C T in t h e 1% t a u r i n e g r o u p p r i o r to 2 w e e k s o f age. T h e s e d a t a ind i c a t e t h a t t a u r i n e a p p e a r s to i n f l u e n c e t h e d e v e l o p m e n t o f t h e a u d i t o r y f u n c t i o n i n g .

Acknowledgements--The expert assistance of Mr Michael Donadio, technical assistance of Mr Jeffrey Messing and Mrs Agnes Heaney, art work by Ms Lucille Donadio, secretarial assistance of Mrs Ann Parese, and practical help from Mr Michael Natelli and Ms Lorinda Matarazzo of IBR Animal Colony Facility throughout this study are gratefully acknowledged. This work was supported by the Office of Mental Retardation and Developmental Disabilities and NIH grant HD 16634.

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