ISSN 0362-1197, Human Physiology, 2017, Vol. 43, No. 3, pp. 265–273. © Pleiades Publishing, Inc., 2017. Original Russian Text © E.A. Luschekina, O.Yu. Khaerdinova, V.S. Luschekin, V.B. Strelets, 2017, published in Fiziologiya Cheloveka, 2017, Vol. 43, No. 3, pp. 32–42.
Interhemispheric Differences in the Spectral Power and Coherence of EEG Rhythms in Children with Autism Spectrum Disorders E. A. Luschekinaa, *, O. Yu. Khaerdinovaa, b, V. S. Luschekinb, and V. B. Streletsb, ** a
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia bChildren’s Psychoneurology Center, Moscow, Russia *e-mail:
[email protected] **e-mail:
[email protected] Received June 27, 2016
Abstract⎯Electroencephalographic examination of boys aged 4–9 years with autism spectrum disorders (ASDs) showed spectral power values and coherence in high-frequency bands (20–60 Hz) in various brain areas were higher than normal. Differences in spectral power were greater in the anterior areas of the left hemisphere; differences in coherence, in the right anterior and posterior areas. Interhemispheric differences typical of healthy subjects were absent in the children with ASDs. The spectral power of the θ rhythm was lower in autism, especially in the left hemisphere. The spectral power of the α rhythm in the autistic children was lower than normal, especially in the posterior areas of the left hemisphere. The μ rhythm was higher than normal in spectral power and was localized in the right, rather than left, anterior areas. The children were examined again after corrective procedures. The α-rhythm spectral power increased (became closer to the norm) in the left posterior areas, while the γ-rhythm spectral power decreased (became closer to the norm) in the right anterior areas in some of the autistic children. The electrophysiological changes were associated with improved psychological testing results, especially in nonverbal measures. Keywords: autism spectrum disorders, interhemispheric asymmetry, EEG, schizophrenia, psychological development DOI: 10.1134/S0362119717030112
INTRODUCTION In the literature focusing on the specifics of children with autism spectrum disorders (ASDs), attempts to correlate psychological and psychophysiological parameters attract particular attention because the neurophysiological mechanisms of particular functional disorders may thus be identified. The anatomic and physiological factors that contribute to autism development have been analyzed in detail [1–4]. A reduction of connections between various brain structures has been found to correlate with deficits in social and intellectual functioning and a lower capability of personal interaction in autism [5, 6]. A thinner cortex in the anterior regions also correlates with the extent of social disorders as measured by psychological testing [4]. One avenue of research in the field is studying how emotional and cognitive parameters depend on the lateralization specifics in autism [7–12]. Attempts have been made to estimate the contributions to the total autistic phenotype for various EEG rhythms generated in certain regions of the right and left hemispheres of the brain. There are data that generation of various EEG rhythms is distorted because of dysfunction of the right temporal cortex in autism [13]
and schizophrenia [14]. Lateral asymmetry of the EEG rhythms in four quadrants of the cortex has been analyzed in schizophrenia, a broad range of schizotypal disorders has been included in the analysis, and the roles of various rhythms in behavioral disorders in schizophrenia have been described in detail. The analysis has identified the rhythms of interest, which are the rhythms that display the greatest deviation from the norm and may provide a marker of the disease [15]. Rhythms of the α and β2 frequency bands are of interest in schizophrenia [15]. In the case of ASDs, the almost total EEG spectrum can be considered relevant because the μ rhythm reflects the function of mirror neuronal system, which is affected in autism [16–18]; the α rhythm characterizes the development of cortical functions [19]; the θ rhythm reflects the specifics of the functional status and emotional responsiveness [19–21]; and the β2 and γ rhythms are associated with cognitive loading [22]. It should be noted that the responses of EEG rhythms to various stimuli have been examined in the majority of studies focusing on lateralization defects in ASDs [7–14, 24–26]. However, it is still unclear how asymmetry of baseline bioelectrical activity differs between ASD patients and healthy subjects.
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We attempted to associate the specifics in asymmetry of the rhythms of interest with the specifics of mental activity in ASD patients. The patients were examined twice, before and after corrective procedures, in order to evaluate the progress of their development and a correlation between changes in psychological and psychophysiological parameters. The objectives of this work were to study the spectral powers and coherence of the EEG rhythms in a quiet wake state in ASD patients compared with healthy subjects and to evaluate the effect of corrective procedures by psychological and psychophysiological parameters. METHODS We examined two groups of right-handed boys aged from 4 years 5 months to 8 years 9 months. A control group included 24 healthy boys (mean age 6.05 ± 0.86 years), and a test group included 27 ASD patients (mean age 5.79 ± 1.42 years). The ASD diagnosis was confirmed in all patients and corresponded to code F84 of the International Classification of Diseases; all of the patients were high-functioning autists. The parents of all children gave their informed consent to the children’s participation in the study. The EEG was recorded from 16 electrodes according to the conventional 10–20 system with linked earlobe electrodes, using a CONAN 4.5 computerized electrophysiological complex, which included a 16channel amplifier and a personal computer. The EEG was recorded in a range of 0.3–70 Hz at a sampling rate of 256 Hz, a time constant of 0.3 s, and a recording duration of 60–120 s to obtain at least 15 artifactfree segments of 4 s each. The spectral power (SP) and coherence were analyzed for the frequency bands θ (4– 7 Hz), α and μ (7.5–12.5 Hz), β1 (13.5–19.5 Hz), β2 (20–29.5 Hz), and γ1 (30–40 Hz). The subject was at rest with the eyes closed during EEG recording. The μ rhythm was isolated using special software, which detects the μ rhythm by its characteristic response to opening the eyes, and spatiotemporal EEG frequency filtration, which makes it possible to isolate the pure μ rhythm and to study its topography [27]. A conventional primary processing of the EEG data included band filtration to remove power line disturbances and artifacts and was followed by a secondary processing [28]. Spectral parameters of the SP were calculated using fast Fourier transform (FFT). To isolate significant SP and coherence values, normalization was carried out using a natural log function. The resulting values of SP and coherence showed nearly normal distributions, allowing us to employ parametric statistics in data analyses. When coherence was analyzed as depended on the group size, the significance threshold (3σ, p < 0.001) was determined by the Z test. The coherence significance thresholds were 0.482 for the patients and 0.260 for the
healthy children. Here we consider only the changes in coherence that exceeded the respective significance thresholds. A statistical analysis of the SP and coherence data included pairwise comparisons by Student’s t test. EEG SP comparisons in the subjects were carried out using one-factor analysis of variance (ANOVA) for repeated measurements with a correction for multiple comparisons (post hoc test Fisher LSD). The between-group factor (Autism/Norm) was compared with the repeated measurement factors Hemisphere (left or right) and Electrode (symmetrical leads Fp1, 2; F7, 8; F3, 4; T3, 4; C3, 4; T5, 6; P3, 4; and O1, 2). Differences in spectral characteristics were considered significant at p < 0.01. Results significant at p < 0.05 suggested a tendency to significance. The significance of differences in coherence in within-group comparisons (between electrode pairs) was assessed using Student’s paired sample t test. The significance test was used without a correction for multiple comparisons. The ASD patients were additionally tested in parallel by the Psychoeducational Profile (PEP) method [29] in order to evaluate the following parameters: imitation of simple movements, visual and auditory perception, fine motor skills, total motor abilities, eye–hand coordination, and verbal and nonverbal intelligence. The electrophysiological and psychological diagnostic tests were performed twice; the second examination was carried out one year after the first one, after corrective procedures (drug treatment by a psychiatrist and/or a complex of corrective procedures by a psychologist or a special education teacher), in order to evaluate their effect on the EEG and psychological parameters. RESULTS In a quiet wake state with the eyes closed, the focus of μ-rhythm activity was localized to the frontal region of the left hemisphere (F3) in the healthy children (Fig. 1a) and the frontal region of the right hemisphere (F4) in the ASD patients (Fig. 1b). The SP in the patients was almost twice higher than in the healthy children (Figs. 1a, 1b). Thus, μ-rhythm activity in ASDs was higher than normal and was detected in the right, rather than left, hemisphere. The α-rhythm focus was mapped to the posterior regions of the right and left hemispheres with a slight rightward shift in the healthy children; the shift of the α-rhythm focus was greater in the ASD patients (Fig. 1d). The α-rhythm SP in the ASD patients was lower than in the healthy children, and the difference was greater in the left hemisphere (F(2,59) = 6.6122, p = 0.00) (Fig. 2b). Pairwise comparisons by Student’s t test showed significant differences between the ASD and healthy groups for O1 compared with O2 in the posterior regions of the left hemisphere (t = 2.7, p = 0.01). Coherence of the α rhythm in ASDs were lower HUMAN PHYSIOLOGY
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Fig. 1. Spectral power maps of the (a, b; i.e., at the top) μ and (c, d; i.e., at the bottom) α rhythms in ASD patients (on the right) compared with healthy children (on the left).
than normal in the left and right anterior regions. The differences were highly probable (p < 0.01) between the right leads Fp2–F8 and less likely (p < 0.05) between the right leads Fp2–T4 and F8–T8 and the left leads Fp1–F7, Fp1–F3, and F3–F7. The same likelihood (p < 0.05) was observed for a decrease in coherence of the interhemispheric connections FpP1–T4 and F4–P3 (Fig. 3a). In the θ frequency band, differences between the health and ADSs were distinct in the posterior regions (a decrease in ADSs). The differences were greater in the left hemisphere (F(2,118) = 3.1557, p = 0.04). The right anterior regions (lead F4) did not show a significant difference between the healthy and affected chilHUMAN PHYSIOLOGY
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dren, while the left anterior regions (lead F3) displayed a considerable difference (t = 2.07, p = 0.04). A difference between T3 and T4 was minor in the healthy children (T3 < T4); the same trend was observed in the ASD patients, but the T3–T4 difference was greater (t = 1.32, p = 0.019) (Fig. 2a). In the β1 frequency band, differences in SP between the patients and controls were lower than in the α frequency band. However, the SP in the patients was lower than in the healthy children, as in the case of the α frequency band. Interhemispheric differences were also lower, only tending to significance (Fig. 2c). In the β2 frequency band, distinct interhemispheric differences in SP were observed in the anterior regions
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Fig. 2. Interhemispheric differences (log spectral power) in ASD patients (dashed lines) compares with healthy children (solid lines). Plots for the left and right hemispheres are shown on the left and right, respectively. Frequency bands: (a) θ, (b) α, (c) β1, (d) β2, (e) γ1, and (f) γ2.
(Fig. 2d). Coherence of the β1 and β2 rhythms showed opposite changes in the ASD patients compared with the healthy children, but increases prevailed. Increases were more numerous and more likely than in the case of the α rhythm. For instance, in the β1 frequency
band, higher coherence between the leads F8 and P4 of the right hemisphere was highly probable (p < 0.01) (Fig. 3b). In the β2 frequency band, an increase in the interhemispheric connection C3–P4 had a high probability (p < 0.01). Increases in coherence between F8–T4, HUMAN PHYSIOLOGY
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Fig. 3. Maps of background activity coherence in healthy and autistic children. Black lines show connections that are stronger in the ASD patients than in the controls; gray lines, connections that are weaker in the ASD patients than in the controls. Differences in coherence between the autistic and healthy children are significant at (solid lines) p < 0.01 or (thin lines) p < 0.05. Frequency bands: (a) α, (b) β1, (c) β2, and (d) γ1.
F8–T6, F8–P4, C4–P4, T4–O2, Fp1–P3, F7–O2, F3–O2, and T5–T6 were observed at p < 0.05 (Fig. 3c). Thus, β-rhythm coherence in the ASD patients was higher than in the healthy children. This pertains to a greater extent to the right, rather than left, hemisphere and interhemispheric connections. The results obtained for the β1 and β2 frequency bands strikingly differed from each other. Changes in the β1 frequency band were more similar to those observed in the α frequency band, while changes in the β2 frequency bands were more similar to those HUMAN PHYSIOLOGY
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observed in the γ frequency band. Background coherence in the β2, γ1, and γ2 frequency bands in the ASD patients was generally higher than in the healthy children. In the γ2 frequency band, differences from the norm were greater in the frontal regions of the left hemisphere (F(2,118) = 91.02665, p = 0.0000). In addition, distinct interhemispheric differences were observed in the left and right anterior regions for the β2, γ1, and γ2 frequencies in the healthy children, while these differences were not detected in the ASD patients (Figs. 2d–2f). Coherence in the γ1 frequency
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Fig. 4. Diagram of the mean (solid line), minimal (dashed line), and maximal (dash-and-dot line) differences between scores at the first and second (one year after) psychological diagnostic examinations in ASD patients. The scores characterize imitation, perception, fine motor skills, total motor abilities, eye–hand coordination, and nonverbal and verbal intelligence.
band in the ASD patients was higher than in the healthy controls (only increases were observed for all connections, occurring at a varying probability). Differences were greater in the right hemisphere (Fig. 3d). The ADS patients who participated in the psychophysiological study were additionally tested using a psychological diagnostic scale. A first examination showed that all of the functions addressed were less efficient in the ASD patients; impairments were detected for imitation, perception, motor functions, eye–hand coordination, and verbal and nonverbal intelligence. The lowest deviations from the norm were observed for nonverbal intelligence in the ASD patients. A second testing was performed after corrective procedures, one year after the first examination. The ASD patients could be divided into three subgroups. One subgroup (16 patients) showed improvements in all of the parameters under study one year after the first examination; the best improvements were observed for gross motor skills and nonverbal intelligence (Fig. 4). In another subgroup (7 patients), the results of the second psychological testing were much the same as those of the first testing. Differences in background bioelectrical activity between the first and second examinations were analyzed statistically, and the α-rhythm SP in the posterior regions of the left hemisphere was found to increase (to become closer to the norm) in the children of the first subgroup. Both increases and decreases were observed for the β fre-
quency band in this subgroup, while the γ rhythm decreased in SP in the right hemisphere (approximating the norm) and increased in SP in the anterior regions of the left hemisphere (Fig. 5). The children of the second subgroup did not show significant changes in bioelectric activity as compared with the first examination. The other ASD patients (the third subgroup) displayed unstable, oppositely directed results upon repeated examination. DISCUSSION The factors underlying behavioral disorders in autism include anatomic and physiological specifics [1–4], distorted inhibition–excitation balance [30], and exposure to stress at an early age [31]. Certain correlations have been observed between results obtained by psychological diagnostic and neurophysiological methods [4, 10, 32]. Thus, multiple disorders have been described for ASDs, including signs of psychopathy and emotional problems [33]. Inhibition of the µ rhythm during movements has been found to decrease in autistic patients compared with the norm [25, 34]. Data on the µ-rhythm lateralization in ASD patients are discrepant [23]. Our results show that the µ-rhythm SP in ASD children is higher than normal and that the focus of µ activity is in the left, rather than right (as is normal), anterior regions. The findings agree with the ideas that the HUMAN PHYSIOLOGY
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descending control over sensorimotor regions of the left hemisphere is distorted in ASDs and that this distortion eliminates left-side asymmetry, which is characteristic of healthy right-handed subjects [35], and alters the function of the left hemisphere [25]. Changes in µ-rhythm asymmetry may indicate a decrease in dominance of the left hemisphere with respect to motor functions; such a decrease is observed in epilepsy and Down’s syndrome. At the same time, the left-sided localization of the µ rhythm, which normally shows a symmetrical localization, has been considered to provide a specific marker of autism [13]. A decrease in α-rhythm SP and coherence has previously been observed in ASD patients compared with healthy controls [36] and has been reported for adult schizophrenics with a predominance of positive or negative symptoms [15, 37] and adolescents with schizotypal disorders [38, 39]. The interhemispheric differences observed for these parameters in ASDs (the SP greater deviates from the norm in the left hemisphere) are characteristic of schizophrenia with predominantly negative symptoms, while greater deviations of coherence in the right hemisphere are characteristic of schizophrenia with predominantly positive symptoms [15, 37]. Analyses of the θ rhythm shows that the θ-rhythm SP is decreased [40] and that differences between the norm and ASDs are seen in the posterior regions (SP lower in ASDs than in healthy subjects) and are greater in the left hemisphere. Interhemispheric differences are normally insignificant in the left and right temporal regions, and the SP on the left is lower than on the right. This trend is preserved in ASDs, but the difference (the SP on the left is higher than on the right) is greater. The above data are of interest because the temporal leads correspond to the projection of the amygdala, and θ waves in these regions are indicative of the emotional status [19]. The greater the reduction of connections between the amygdala and the temporal gyrus, the greater are the functional disorders in autism. A better development of social functions correlates with the strength of connections between the amygdala and the lower frontal gyrus on the right [12]. Lack of coordination in the activation of the amygdala, the island, and the total limbic system prevents an adequate evaluation of the emotional status [41]. The specifics of affective reactions provide a means to preliminarily diagnose ADSs in early development (starting from one year of age), when behavioral signs of ADSs are indistinct [31]. Given that positive and negative emotions are to a greater extent regulated, respectively, by the left and right hemispheres [42], our findings that the θ-rhythm SP is lower in autists than in healthy children and that the decrease is greater in the left hemisphere may explain why negative emotions prevail in ASD patients and can be considered as manifestations of disordered emotional reactions in ASDs. HUMAN PHYSIOLOGY
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p=0 N1 < N2 γ (30.0–45.0) Fig. 5. Maps of the t statistics for differences in the spectral power of the α (at the top) and γ (at the bottom) rhythms between the first and second (on the right) examinations in ASD patients. Black, a decrease; gray, an increase.
The SPs and coherence in the β and γ frequency bands in ADS patients were higher than in healthy children, and this finding agrees with the data that high-frequency rhythms predominate in cortical regions of autistic patients, presumably, as a result of defects in cortico-thalamic connections [3]. SP deviations from the norm were greater in the frontal regions of the left hemisphere, while deviations in coherence were greater in the anterior and posterior regions of the right hemisphere. An increase in intracortical connections in high-frequency bands has been observed in the anterior regions of the left hemisphere for schizophrenia with predominantly positive symptoms and in the anterior regions of the right hemisphere for schizophrenia with predominantly negative symptoms [15]. Like in the case of schizophrenia with predominantly negative symptoms, it is possible to assume for ASDs
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(this study) that pathological activation of the anterior and posterior regions occurs in the same (right) hemisphere where a decrease in activation of the posterior region is evident from the changes in α-rhythm coherence. The temporal regions of the cortex have also been reported to display changes in high-frequency activity (>40 Hz) in autism and schizophrenia, especially in the light hemisphere [26]. The left-side dominance characteristic of the normally developing auditory system is distorted in autism and schizophrenia, as well as in dyslexia, leading to a broad range of speech disorders [11]. Various specialists usually treat children with ASDs. Their treatment includes medications prescribed by a psychiatrist and/or corrective procedures performed by a psychologist or a special education teacher. Treatment is more or less effective, leading to partial rehabilitation of the patients. The question arises as to whether psychological diagnostic parameters improve and bioelectric activity normalizes during correction of higher mental functions and whether the parameters (in particular, interhemispheric connections) correlate with each other. Our study revealed an association between positive changes in psychological testing results and changes in bioelectric activity in ASD patients. When the α-rhythm SP increased in the left posterior regions and the γ-rhythm CP decreased in the right anterior regions (both of the changes can be considered as normalization) at the second examination compared with the first one, improvements were seen in the results of psychological testing as well. The improvements in nonverbal functions were greater than in verbal functions according to psychological testing, as is also the case in schizophrenia with predominantly negative symptoms [15, 43]. An increase in α-rhythm SP in the left hemisphere, which suggests an increase in relative activity of the right hemisphere, and a decrease in background γ-rhythm SP in the right hemisphere, which facilitates normalization of the reactivity in task performance, favor improvements in nonverbal intelligence parameters. CONCLUSIONS (1) The µ rhythm has a higher spectral power and is localized in the left, rather than right, anterior regions in children with autism spectrum disorders as compared with healthy children. (2) The α-rhythm spectral power in autism spectrum disorders is lower than normal. The deviations from the norm are greater in the left posterior regions. (3) The θ-rhythm spectral power is lower than normal in autism, especially in the left hemisphere. (4) High-frequency rhythms (β2 and γ) in autism spectrum disorders have higher spectral powers and higher coherence than in the norm. Deviations in spectral power are greater in the left anterior regions, and deviations in coherence are greater in the right
hemisphere. Interhemispheric differences in high-frequency rhythms, which are characteristic of healthy subjects, are absent from patients with autism spectrum disorders. (5) A repetitive examination performed after corrective procedures showed that an increase in α-rhythm spectral power in the posterior regions of the left hemisphere and a decrease in γ-rhythm spectral power in the anterior regions of the right hemisphere are associated with improvements in psychological testing parameters, especially those of nonverbal intelligence. ACKNOWLEDGMENTS This work was supported by the Russian Humanitarian Science Foundation (project no. 14-06-00444a). REFERENCES 1. King, B.H. and Lord, C., Is schizophrenia on the autism spectrum?, Brain Res., 2011, vol. 1380, p. 34. 2. Sugranyes, G., Kyriakopoulos, M., Corrigall, R., et al., Autism spectrum disorders and schizophrenia: Metaanalysis of the neural correlates of social cognition, Plos One, 2011, vol. 6, no. 10, e25322. 3. Gregory, M. and Mandelbaum, D., Evidence of a faster posterior dominant EEG rhythm in children with autism, Res. Autism Spectrum Disord., 2012, vol. 6, no. 3, p. 1000. 4. Doyle-Thomas, K., Duerden, E., Taylor, M., et al., Effects of age and symptomatology on cortical thickness in autism spectrum disorders, Res. Autism Spectrum Disord., 2013, vol. 7, no. 1, p. 141. 5. Gobbelé, R., Lamberty, K., Stephan, K.E., et al., Temporal activation patterns of lateralized cognitive and task control processes in the human brain, Brain Res., 2008, vol. 1205, p. 81. 6. Hirnstein, M., Westerhausen, R., Korsne, M.S., and Hugdahl, K., Sex differences in language asymmetry are age-dependent and small: A large-scale, consonant-vowel dichotic listening study with behavioral and fMRI data, Cortex, 2013, vol. 49, no. 7, p. 1910. 7. Dawson, G., Warrenburg, S., and Fuller, P., Cerebral lateralisation in individuals diagnosed as autistic in early childhood, Brain Lang., 1982, vol. 15, no. 2, p. 353. 8. Dawson, G., Webb, S.J., Wijsman, E., et al., Neurocognitive and electrophysiological evidences of altered face processing in parents of children with autism: Implications for a model of abnormal development of social brain circuitry in autism, Dev. Psychopathol., 2005, vol. 17, no. 3, p. 679. 9. Flagg, E., Cardy, J., Roberts, W., and Roberts, T., Language lateralization development in children with autism: Insights from the late field magnetoencephalogram, Neurosci. Lett., 2005, vol. 386, no. 2, p. 82. 10. Sutton, S., Burnette, C., Mundy, P., et al., Resting cortical brain activity and social behavior in higher functioning children with autism, J. Child Psychol. Psychiatry, 2005, vol. 46, no. 2, p. 211. 11. Roberts, T.P.L., Schmidt, G.L., Egeth, M., et al., Electrophysiological signatures: Magnetoencephalographic studies of the neural correlates of language impairment in autism spectrum disorders, Int. J. Psychophysiol., 2008, vol. 68, no. 2, p. 149. HUMAN PHYSIOLOGY
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Translated by T. Tkacheva