Vol. 13, N«. 1 Printed in U.S.A.

PSYCHOPHVSIOLOCY

Copyright ^ 1976 by T!ie Society for PsychophysJoiogical Research

Conditioning of Evoked Potentials in Children of Differing Intelligence G. LELORD, F . LAFFONT, AND PH. JUSSEAUME Laboratoire de Neurophysiologie du conditionnement, Service d'Explorations Fonctionnelles Psychopathologiques, C.H.U. Bretonneau—Tours (France)

ABSTRACT This study compared the conditioning of averaged evoked potentials in three groups of children (average age 11 yrs): (I) normals, (H) IQ between 50 and 60, (III) IQ between 20 and 50. Sound was the conditioned stimulus, light the unconditioned stimulus, 68 sessions were recorded in 34 children. Decrease in the number and in the amplitude of potentials evoked by sound was observed from group I to group III, whereas generalized slow waves increased from group I to group HI. Conditioning was different in the three groups. In the normal child it modified the conditioned evoked potential to sound. In the mentally retarded child, it modified generalized slow waves and brought about the reproduction of a temporal sequence. DESCRIPTORS: Average evoked potentials. Event related slow potentials, Sensorial conditioning, Intelligence. Evoked potential (EP) measures may give different results depending on IQ leveL Chalke & Ertl (1965) noted the latency of the visual EP was greater in subjects with low IQ. This is also true for the auditory EP (Nodar & Graham, 1968). Amplitude of the EP is greater in intelligent subjects (Rhodes, Dustman, & Beck, 1967). However mongoloid retardates have been noted to have greater amplitudes than normal subjects (Barnet & Lodge, 1967; Straumanis, Shagass, & Overton, 1970). Studying the variability of EP in subjects at varying IQ levels, Callaway (1973) showed that low variability is associated with high IQ. Inspired by techniques of electroencephalographic conditioning (Popov, Heuyer, Kieffer, Agathon, & Lelord, 1958) in which sound and light are coupled, Lelord, Gousset, and HeninRibeyrolles (1967) and Latfont, Andre, Jusseaume, Bnineau, & Lelord (1967) reported low amplitude of conditioned EP in mentally retarded subjects. The purpose of the present study was to compare the characteristics of these conditioned potentials in children of three different intelligence levels. This study was supported by INSERM (CL 75. i.205.6), Fondation de France, Securite Sociale, et Fondation pour ia Recherche Medicate Fran^ai.se. Address requests for reprints to: ProfesseurG. Lelord, Service ^'Explorations Fonctionnelles Psychopathologiques, C.H.U. Bretonneau, 37 033—^Tours Cedex—France.

Methods Apparatus and Procedure The subject was isolated in a dark sound proof room and sat in a comfortable armchair. Silver chloride electrodes were placed on the scalp (vertex, the right frontal, temporal, and occipital areas). The common reference lead was placed on the left ear lobe. The signals were amplified by an Alvar Electronic AC amplifier set for a bandpass down 3 dB at 0.1 Hz (2 sec time constant) and 100 Hz and providing a gain of 10^. The conditioned stimulus was a brief sound of 4 msec, 1K Hz, 25dB above the average threshold of 3 normal hearing adults, the unconditioned stimulus a 0.1 tnsec flash of light from a lamp placed 40 cm in front of the subject'.^ eyes and giving an intensity of !2(X)lux. Instruction was not given to either the normal or the retarded since it could aot be understood by the severely retarded children. Background EEG was recorded during the whole experiment. For all subjects stimuli were given when muscular artifacts were absent. The evoked potentials were averaged in groups of 20 trials with a 400 channel digital computer and recorded on paper by an x-y plotter. The epoch was 2 sec. Eye movements were recorded. One pair of electrodes was placed in the horizontal plane at the outer canthi, and one pair in the vertical plane, in the pupillary line just above the eyebrow and 2 cm under the margin of the inferior eyelid. it was possible to record the ocuiogram in less than half the patients because usually they would not tolerate electrodes near the eyes. Since the ocular electrodes were also unpleasant for normal children, ocular movements were recorded in only half of the normal subjects. Generally each subject had two 1 hr se.ssions. During each .session there were 10 series of 20 trials. Trials were given at

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random intervals varying from 4 to 30 sec. In the first 2 series of the first session, sound was given alone to obtain habituation (sound alone). In the next 16 series (8 during the first session, 8 during the second), light was presented 800 msec after sound to produce conditioning (sound and light: SL). In the last 2 series of the second session, the sound was again given alone so that extinction of the conditioned responses could be studied (sound after SL). Sixty-eight sessions were conducted in 34 children. Subjects TTiree groups of children aged 7 to 13 were examined: 1)11 healthy non retarded children, 6 boys and 5 girls (average age 10 yrs, 9 mos), pupils in public schools, were brought to the laboratory by their parents, nurses, medical students, or friends of the laboratory. 2) 12 mildly retarded children (8 boys, 4 girls) with IQ between 50 and 60, average age 12 yrs. pupils in special centers for mental retardates, were brought by their educator. Mental retardation appeared as an isolated phenomenon. History of retardation was found in 8 of the families; no pathological antecedents were found except for one case of prematurity. Slow psychomotor development was noted in all (first words, first steps). The children were cooperative and had few "emotional" problems except for passiveness and inhibition in one child, anorexia in another, irrilabiiity and restlessness in a third. Neurological examination was normal. Five children had difficulty in reading and writing, 3 were not well lateralized. There were no important morphological anomalies except for one child being exceptionally small but he had no endocrine problems. The EEG showed slow waves rather abundant in relation to age in 3 subjects, and spikes during hyperpnea and intermittent light stimulation in 2. All children were capable of acquiring academic skills. 3). 11 children severely retarded (6 boys, 5 girls) with IQ between 20 and 50, average age 8 yrs 8 mos, who were hospitalized on a child psychiatry ward. The children selected had a minimum of behavior problems, neurological difficulties or epilepsy. However, because of the severity of mental retardation, there were some associated symptoms. Three children had Down's syndrome (confirmed by kariotype). In the history of these II children there was 1 case of prematurity, 2 cases of reanimation at birth, 2 cases of convulsions. There were 2 cases of anxiety with tendency toward depression, 2 ca.ses of restlessness, 1 case with sterotypies, ! case with signs of autism. The neurological examination was normal except for clumsiness and coordination difficulties; 5 children did not yet speak. Physical examination noted many morphological anomalies: one hypotrophy, one megacolon, one club foot, one scaphocephaly, one facial asymmetry with prognathism, one cataract with some vision preserved, one non-characteristic anomaly of the eye fundus. The EEG .showed slow waves in 2 cases and moderately intense paroxysmal activity in 3 cases. Measures Percentage of Responses. The responses were counted in relation to the number of tracings recorded in a given group. Results were presented in percentages but chi squares were computed in absolute numbers. Criteria for presence or absence of responses corresponded to whether the amplitude measures were higher or lower than 4 /xV. Amplitude. Oscillations appearing during the first 100 n>sec or during the following 400 msec were measured from peak to peak. The amplitude of late slow potentials was measured from a

Fig. t. Idealized (occipital) evoked responses during coupling of sound and light. S = sound; L = light. The tracing represents the average response to 20 stimulations. Amplitudes are measured in three windows: 1) early phenomena, first 100 msec; 2) evoked potentials, next 300 msec; 3) late slow waves, last 400 msec. Negative deflections are upward.

horizontal line bisecting the difference between the upper and the lower peaks recorded during the first 100 msec (Fig. I).

Results Significant diiFerences in the number and in the amplitude of evoked potentials and slow waves were observed among the different groups. The .02 level of confidence was accepted. Evoked Potentials As summarized in Table 1, the number of potentials evoked by sound diminished from Group I to Group III. Table 1 provides the pair-wise contrasts. In direct comparisons of Group I to Group III, significant differences were found at the vertex and on the occiput for potentials evoked by sound alone (x^(l)=8.33 and 18.42, respectively) and by sound from the SL series (x^(l)=21.2 and 36.6 respectively). Table 1 also shows that EP amplitude diminished from Group 1 to Group III for all response categories of response recorded at the vertex and the occiput. Pair-wise contrasts are provided in Table 1. Although not significant in either Group II or Group in, there was an increase in occipital EP amplitude evoked by the sound during the SL series as contrasted to the sound-alone series in Group I, ?(18)=2.66. Early rhythmic oscillations appearing in the 100 msec following the sound (amplitude: 10 to 15 /iV, frequency: 7 to 9 Hz) were observed before conditioning in 8 subjects in Group I, 4 subjects in Group II, and 1 subject in Group III. These phenomena were not significantly modified by conditioning in the three groups. Slow Waves As shown in Table 2, generalized positive slow waves (400 to 800 msec) observed during coupling

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EVOKED POTENTIALS AND INTELLIGENCE IN CHILDREN TABLE 1 Percentage and amplitude of evoked responses Vertex

Groups

Statistics"

Souiid Alone

Sound + Light

Occipital

Sound After SL

Light

Sound Alone

Sound + Light

91% 16.1* 32% 0.11 27%

70% 17.6* 43% 3.5

Sound After SL

Light

Percentages

xH\) II III

100% 0.29 96% 5.45* 68%

96%

100% .00 100% 10.9* 68%

0.34 97%'

28.9* 80%

96% 0.60 95% 0.9 92%

86% 13.5*

32% 2.07

3.3%

14%

26

22

7.91*

6.05*

13

12

3,01*

1.77

97% 0.99 94% 0.40 93%

Amplitudes , '(21) 11 '(21) III

25 2.63* 19 3.40*

8

23 2.52* 17.5 6.40* 8 .

19 1.31 17 4.50* 7

20 5.70* 12 2.95*

21 1.62 19.5 4.70* 10

:

9

8

29 4,70* 17.5 2.66* 12

"Values of x^ and / contra,st means immediately above and below each .statistic. *p < .02.

sound and light were practically absent in Group I but were present in 30% ofthe tracings of Group III, Generalized negative slow waves evoked by sound after the SL series were absent in Group I, but were present in 14% ofthe tracings of Group III, Table 2 provides pairwise contrasts of the means between Groups I and II and between Groups II and III, The amplitude of positive slow waves to sound

was increased by coupling sound and light in Groups II and III {f( 15) = 2,84 and f(17)=2,79, respectively). Finer analysis showed localized slow waves at the vertex and in the occipital area, but the differences in numbers and amplitudes observed between Groups I, II, and III were not statistically significant.

TABLE 2 Percentage and amplitude of generaiized slow waves Positive Groups

Statistics"

Sound Atone

Sound + Light

0% 12.5% 2.4 32%

2% 6.10* 8% 5.84* 30%

7^ 0.67 8

19 2.32 13 2.84* 12

Negative

Sound After SL

Light

Sound Alone

Sound + Light

SmmA After SL

Light

Percentages I 11

in

xW)

x'(i)

0% 29% 0.38 41%

3% 4.80 8% 5.07 16%

9% 4% 3.72 18%

6%. 0.42 5% 2.65 9%

0%

14%

3% 4.68 8%. 0.16 6%

16

20 4.24* 13 0,45 14

0%

Amplitudes i juV)

12 0.64 10

19 3.34* 11 0.80 10

V and ( values contrast means immediately above and below each statistic. *P < .02.

25 10 0.27 9

15 .2.21 10 0.55 11

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LELORD, LAFFONT, AND JUSSEAUME

Reproduction of Time Interval In some subjects sound after SL series reproduced the whole sequence of responses formerly observed during coupling sound and light. The conditioned response "to time" resembled an evoked potential or a slow wave. It was observed in 2 subjeets in Group I, 6 subjects in Group II (5 slow waves, 1 evoked potential followed by a slow wave), 8 subjects in Group III (5 evoked potentials, 3 slow waves). Eyeblinks In some tracings eyeblinks appeared. They occurred usually after the light (43% of the tracing), but could be evoked by the sounds: sound alone (9% of the tracings), sound of SL series (11%), sound after SL series (9%). Discussion The decrease in the number and in the amplitude of potentials evoked by sound from Groups I to III shows that these responses are weaker when IQ is low. If one considers thepercentage of responses as a relatively rough indication of their variability these results are in agreement with those of Callaway {1973) who noted greater variability in dull subjects; Also observed was a decrease in amplitude from Groups I to III. The fact that Group III included 3 mongoloid retardates did not modify those results, Several authors observed high amplitude responses in these children for auditory, visual (Barnet & Lodge, 1967) and somatic evoked potentials (Bigum, Dustman, & Beck, 1970). Here the comparison of the 3 mongoloid to the other 8 retarded in Group III shows that visual and auditory responses are similar. However, in the 3 mongoloids during coupling sound and light occipital responses to sound seem to be higher than in the other 8 retardates. Auditory EP variations are not related to eyeblinks which are observed in normals as well as in patients in 9 to J1% of the tracings. Gn the contrary,

Vol. 13, No. 1

potentials evoked by the sound are recorded on almost all the tracings, both at the vertex and on the occipital region in normal children and at the vertex in patients. It seems that sound and light stimuli are too weak to produce here an eyeblink conditioning. The decrease of EP amplitude from Group I to Group III does not depend on the age differences between these groups. In fact, in normal children the size of EP is maximum about 9 and decreases from 9 to 12 (Callaway & Halliday, 1973), and in this study, the smallest EPs are recorded in Group III (8,8) and the largest in Group I (12), The absence of conditioning of the evoked potential in Groups II and III confirms the observations of Lelord et a!. (1967). After coupling, the increase in amplitude of the potential evoked by sound at the occiput is not observed in mentally retarded patients. This result is similar to the observation made by Shipley (1970) who gave sound and light together, and recorded a facilitation in normal subjects but not in retarded ones. On the contrary, the presence of potentials evoked "by time," important in Group III, shows a capacity for reproducing temporal sequences. This particular form of acquisition mentioned by Popov (1948), Rusinov (1959), Lelord e t a l . (1967) in normal children and more recently analyzed as "emitted potential" (Sutton & Dore, 1973; Picton & Hillyard, 1974) seems to be particularly marked in retarded subjects. This reproductive capacity may be a substitute for associative phenomena which fail to appear in these patients. Whereas evoked potentials decrease from Group I to Group III, generalized slow waves increase from Group I to Group III. The increase is mostly in number, especially for positive slow waves which are practically absent in Group I and frequent in Group III. The phenomena are similar to slow waves observed in newboms (Laffont, Bruneau, Andre, & Lelord, 1973). Later, these generalized slow waves, much more frequent in autistic than in retarded children, characterize emotional disorders rather than mental retardation (Lelord, Laffont, Jusseaume, & Stephant, 1973),

REFERENCES Bamet, A. B., & Lodge, A. Click evoked EEG responses in normal and developmentalty retarded infants. Nature, 1967, 214, 252-255. Bigum, H. B., Dustman, R. E., & Beck, E. C. Visual and somato-senspry evoked responses from mongoloid and nor-

mal children. Electroencephalography & Clinical Neurophysiology, 1970, 2S, 576-585. Caliaway, E. Des correiatiqns entre des potentials evoques moyens et la mesure de I'intelligence. In A. Fessard & G. Lelord (Eds.), Average evoked responses and their ctinditioning in normal subjects and psychiatric patients. Paris:

Inserm, 1973. Pp. 213-222. Callaway, E., & Hailiday, R. A. Evoked potential variability: Effects of age, amplitude and methods of measurement. , Electroencephatography •& Clinical Neurophysiology, 1973, 34, 125-133. i Chalke, F. C. R., & Ertl, } . Evoked potentials and intelligence j Life Science, 1965, 4, 1319-1322. \ Laffont, F.. Andre, E., Jusseatjme, Ph., Bruneau, N., & Lelord, -i G. Relations entre potentiels evoques et intelligence. Comptes -, Reiidus Societi- biologie (Paris), 1972, 166, 1503-1509. t Laffont, R., Bruneau, N., Andre, E., & Leiord, G. Con- i

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EVOKED POTENTIALS AND INTELLIGENCE IN CHILDREN

ditionnement des activite.s electrocorticales chez le nouveau.ne. Comptes Rendus Societc- biologie (Paris), 1973, 167, 717-724. Lelord, G., Gousset, A., & Henin-Ribeyroiles, D. Interet des methodes de conditionnement electrophysioiogique dans i'etude de la debilite mentale. In B. W. Richard (Ed.), ier Congres Association Internationale Etude Scientifique Arrieration Mentale. Reigate: Michael Jackson Publi.shing Co.. 1967. Pp. 368-376. Lelord, G., Laffont, F.. Jusseaume, Ph., & Stephant. J. L. Comparative study of conditioning of averaged evoked re.sponses by coupling sound and light in normal and autistic children. Psychophysiology, 1973, 10, 415-425. Nodar, R. H.. & Graham. J. T. An investigation of auditory evoked responses of mentally retarded adults during sleep. Etectroencephalography & Clinical Neurophysiology, 1968. 25, 73-76. Picton, T. W., & Hillyard, S. A. Human auditory evoked potentials II. Eifects of attention. Electroencephalography

Conditioning of evoked potentials in children of differing intelligence.

Vol. 13, N«. 1 Printed in U.S.A. PSYCHOPHVSIOLOCY Copyright ^ 1976 by T!ie Society for PsychophysJoiogical Research Conditioning of Evoked Potentia...
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