Neuroenhancement of Memory for Children with Autism by a Mind-Body Exercise

Agnes S Chan, Yvonne M Y Han, Sophia L Sze, Eliza M Lau, Agnes S Chan, Yvonne M Y Han, Sophia L Sze, Eliza M Lau

Abstract

The memory deficits found in individuals with autism spectrum disorder (ASD) may be caused by the lack of an effective strategy to aid memory. The executive control of memory processing is mediated largely by the timely coupling between frontal and posterior brain regions. The present study aimed to explore the potential effect of a Chinese mind-body exercise, namely Nei Gong, for enhancing learning and memory in children with ASD, and the possible neural basis of the improvement. Sixty-six children with ASD were randomly assigned to groups receiving Nei Gong training (NGT), progressive muscle relaxation (PMR) training, or no training for 1 month. Before and after training, the participants were tested individually on a computerized visual memory task while EEG signals were acquired during the memory encoding phase. Children in the NGT group demonstrated significantly enhanced memory performance and more effective use of a memory strategy, which was not observed in the other two groups. Furthermore, the improved memory after NGT was consistent with findings of elevated EEG theta coherence between frontal and posterior brain regions, a measure of functional coupling. The scalp EEG signals were localized by the standardized low resolution brain electromagnetic tomography method and found to originate from a neural network that promotes effective memory processing, including the prefrontal cortex, the parietal cortex, and the medial and inferior temporal cortex. This alteration in neural processing was not found in children receiving PMR or in those who received no training. The present findings suggest that the mind-body exercise program may have the potential effect on modulating neural functional connectivity underlying memory processing and hence enhance memory functions in individuals with autism.

Keywords: EEG; autism; functional connectivity; memory; mind–body training; neurocognitive enhancement.

Figures

FIGURE 1
FIGURE 1
An illustration of the experimental paradigm of the visual memory task.
FIGURE 2
FIGURE 2
Post-training score minus pre-training score in (A) total recall, (B) semantic clustering, and (C) visual scanning in randomized and organized conditions. Positive values indicate improved performance. The error bars represent 95% confidence interval of the difference between pre- and post-training scores. Control, control group without training; PMR, progressive muscle relaxation; NGT, Nei Gong training. ∗p < 0.05; ∗∗p < 0.01 (paired samples t-test).
FIGURE 3
FIGURE 3
Changes in (A,B) intra-hemispheric and (C,D) inter-hemispheric theta coherence after 1 month in the three groups in the randomized and organized conditions. Positive values indicate increased theta coherence. The error bars represent 95% confidence interval of the difference between pre- and post-training theta coherence values. Control, control group without training; PMR, progressive muscle relaxation; NGT, Nei Gong training. ∗p < 0.05 (paired samples t-test).
FIGURE 4
FIGURE 4
Line topographic maps demonstrate changes in individual theta coherence pairs after training in the randomized and organized conditions across the three groups. Red lines represent coherence pairs showing a significant increase in theta coherence (p < 0.05, paired samples t-test). Control, control group without training; PMR, progressive muscle relaxation; NGT, Nei Gong training.
FIGURE 5
FIGURE 5
Graphical representation of the sLORETA paired t-statistics results comparing the pre- and post-training theta source activity of the three groups in the randomized and organized conditions. The regions colored in yellow/red indicate significantly elevated activity after training, while those colored in blue indicate significantly reduced activity, p < 0.05. Control, control group without training; PMR, progressive muscle relaxation; NGT, Nei Gong training.

References

    1. American Psychiatric Association [APA] (2000). Diagnostic and Statistical Manual of Mental Disorders 4th Edn. Washington, DC: American Psychiatric Association.
    1. Bai X., Towle V. L., He E. J., He B. (2007). Evaluation of cortical current density imaging methods using intracranial electrocorticograms and functional MRI. Neuroimage 35 598–608. 10.1016/j.neuroimage.2006.12.026
    1. Barnea-Goraly N., Kwon H., Menon V., Eliez S., Lotspeich L., Reiss A. L. (2004). White matter structure in autism: preliminary evidence from diffusion tensor imaging. Biol. Psychiatry 55 323–326. 10.1016/j.biopsych.2003.10.022
    1. Binder J. R., Desai R. H., Graves W. W., Conant L. L. (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex 19 2767–2796. 10.1093/cercor/bhp055
    1. Boggio P. S., Ferrucci R., Mameli F., Martins D., Martins O., Vergari M., et al. (2012). Prolonged visual memory enhancement after direct current stimulation in Alzheimer’s disease. Brain Stimul. 5 223–230. 10.1016/j.brs.2011.06.006
    1. Boggio P. S., Khoury L. P., Martins D. C., Martins O. E., de Macedo E. C., Fregni F. (2009). Temporal cortex direct current stimulation enhances performance on a visual recognition memory task in Alzheimer disease. J. Neurol. Neurosurg. Psychiatry 80 444–447. 10.1136/jnnp.2007.141853
    1. Brett M., Johnsrude I. S., Owen A. M. (2002). The problem of functional localization in the human brain. Nat. Rev. Neurosci. 3 243–249. 10.1038/nrn756
    1. Cannon R., Baldwin D. (2012). EEG current source density and the phenomenology of the default network. Clin. EEG Neurosci. 43 257–267. 10.1177/1550059412449780
    1. Cannon R., Kerson C., Hampshire A. (2011). sLORETA and fMRI detection of medial prefrontal default network anomalies in adult ADHD. J. Neurother. Investig. Neuromodulation Neurofeedback Appl. Neurosci. 15 358–373. 10.1080/10874208.2011.623093
    1. Chan A. S. (2013). Contemporary Application of Shaolin Medicine: Dejian Mind-Body Intervention 5th Edn. Hong Kong: Chanwuyi Publishing.
    1. Chan A. S., Cheung M. C., Han Y. M. Y., Sze S. L., Leung W. W., Man H. S., et al. (2009). Executive function deficits and neural discordance in children with autism spectrum disorders. Clin. Neurophysiol. 120 1107–1115. 10.1016/j.clinph.2009.04.002
    1. Chan A. S., Cheung M. C., Sze S. L., Leung W. W., Shi D. (2011a). Shaolin Dan Tian breathing fosters relaxed and attentive mind: a randomized controlled neuro-electrophysiological study. Evid. Based Complement. Alternat. Med. 2011:180704 10.1155/2011/180704
    1. Chan A. S., Cheung M. C., Tsui W. J., Sze S. L., Shi D. (2011b). Dejian mind-body intervention on depressive mood of community-dwelling adults: a randomized controlled trail. Evid. Based Complement. Alternat. Med. 2011:473961 10.1093/ecam/nep043
    1. Chan A. S., Han Y. M. Y., Sze S. L., Cheung M. C., Leung W. W., Chan R., et al. (2011c). Disordered connectivity associated with memory deficits in children with autism spectrum disorders. Res. Autism Spectr. Disord. 5 237–245. 10.1093/ecam/nep043
    1. Chan A. S., Sze S. L., Cheung M. C., Han Y. M., Leung W. W., Shi D. (2011d). Dejian mind-body intervention improves the cognitive functions of a child with autism. Evid. Based Complement. Alternat. Med. 2011:7 10.1155/2011/549254
    1. Chan A. S., Han Y. M. Y., Cheung M. C. (2014a). “Chinese chan-based prospective neuropsychological intervention for autistic children,” in The Comprehensive Guide to Autism eds Patel V. B., Preedy V. R., Martin C. R. (New York, NY: Springer; ) 2333–2355.
    1. Chan A. S., Sze S. L., Woo J., Yu R. H. (2014b). A Chinese Chan-based lifestyle intervention improves memory of older adults. Front. Aging Neurosci. 6:50 10.3389/fnagi.2014.00050
    1. Chan A. S., Han Y. M. Y., Sze S. L., Wong Q. Y., Cheung M. C. (2013a). A randomized controlled neurophysiological study of a Chinese Chan-based mind-body intervention in patients with major depressive disorder. Evid. Based Complement. Alternat. Med. 2013:812096 10.1155/2013/812096
    1. Chan A. S., Sze S. L., Siu N. Y., Lau E. M., Cheung M. C. (2013b). A Chinese mind-body exercise improves self-control of children with autism: a randomized controlled trial. PLoS ONE 8:e68184 10.1371/journal.pone.0068184
    1. Chan A. S., Ho Y. C., Cheung M. C. (1998). Music training improves verbal memory. Nature 396:128 10.1038/24075
    1. Chan A. S., Ho Y. C., Cheung M. C., Albert M. S., Chiu H. F. K., Lam L. C. W. (2005). Association between mind-body and cardiovascular exercises and memory in older adults. J. Am. Geriatr. Soc. 53 1754–1760. 10.1111/j.1532-5415.2005.53513.x
    1. Chan A. S., Sze S. L. (2013). “Shaolin mind-body exercise as a neuropsychological intervention,” in Annals of Traditional Chinese Medicine: Health, Wellbeing, Competence and Aging eds Leung P. C., Woo J., Kofler W. (New Jersey, NJ: World Scientific Publishing; ) 201–211.
    1. Chan A. S., Wong Q. Y., Sze S. L., Kwong P. P. K., Han Y. M. Y., Cheung M. C. (2012). A Chinese Chan-based mind-body intervention for patients with depression. J. Affect. Disord. 142 283–289. 10.1016/j.jad.2012.05.018
    1. Cheung M. C., Chan A. S., Sze S. L., Leung W. W., To C. Y. (2010). Verbal memory deficits in relation to organization strategy in high- and low-functioning autistic children. Res. Autism Spectr. Disord. 4 764–771. 10.1016/j.rasd.2010.02.004
    1. Chiaravalloti N. D., Wylie G., Leavitt V., DeLuca J. (2012). Increased cerebral activation after behavioral treatment for memory deficits in MS. J. Neurol. 259 1337–1346. 10.1007/s00415-011-6353-x
    1. Chiesa A., Calati R., Serretti A. (2011). Does mindfulness training improve cognitive abilities? A systematic review of neuropsychological findings. Clin. Psychol. Rev. 31 449–464. 10.1016/j.cpr.2010.11.003
    1. Clark V. P., Parasuraman R. (2014). Neuroenhancement: enhancing brain and mind in health and in disease. Neuroimage 85 889–894. 10.1016/j.neuroimage.2013.08.071
    1. Coben R., Clarke A. R., Hudspeth W., Barry R. J. (2008). EEG power and coherence in autistic spectrum disorder. Clin. Neurophysiol. 119 1002–1009. 10.1016/j.clinph.2008.01.013
    1. Coffman B. A., Clark V. P., Parasuraman R. (2014). Battery powered thought: enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation. Neuroimage 85 895–908. 10.1016/j.neuroimage.2013.07.083
    1. Davidson R. J., Kabat-Zinn J., Schumacher J., Rosenkranz M., Muller D., Santorelli S. F., et al. (2003). Alterations in brain and immune function produced by mindfulness meditation. Psychosom. Med. 65 564–570. 10.1097/01.PSY.0000077505.67574.E3
    1. De Ridder D., Vanneste S., Kovacs S., Sunaert S., Dom G. (2011). Transient alcohol craving suppression by rTMS of dorsal anterior cingulate: an fMRI and LORETA EEG study. Neurosci. Lett. 496 5–10. 10.1016/j.neulet.2011.03.074
    1. Dickerson B. C., Eichenbaum H. (2010). The episodic memory system: neurocircuitry and disorders. Neuropsychopharmacology 35 86–104. 10.1038/npp.2009.126
    1. Dumpelmann M., Ball T., Schulze-Bonhage A. (2012). sLORETA allows reliable distributed source reconstruction based on subdural strip and grid recordings. Hum. Brain Mapp. 33 1172–1188. 10.1002/hbm.21276
    1. Fletcher P. C., Henson N. A. (2001). Frontal lobes and human memory: insights from functional neuroimaging. Brain 124 849–881. 10.1093/brain/124.5.849
    1. Floel A., Suttorp W., Kohl O., Kurten J., Lohmann H., Breitenstein C., et al. (2012). Non-invasive brain stimulation improves object-location learning in the elderly. Neurobiol. Aging 33 1682–1689. 10.1016/j.neurobiolaging.2011.05.007
    1. Fuchs M., Kastner J., Wagner M., Hawes S., Ebersole J. S. (2002). A standardized boundary element method volume conductor model. Clin. Neurophysiol. 113 702–712. 10.1016/S1388-2457(02)00030-5
    1. Gabrieli J., Poldrack R., Desmond J. (1998). The role of left prefrontal cortex in language and memory. Proc. Natl. Acad. Sci. U.S.A. 95 906–913. 10.1073/pnas.95.3.906
    1. Greenhalgh T. (1997). Assessing the methodological quality of published papers. BMJ 315 305–308. 10.1136/bmj.315.7103.305
    1. Hammer A., Mohammadi B., Schmicker M., Saliger S., Munte T. (2011). Errorless and errorful learning modulated by transcranial direct current stimulation. BMC Neurosci. 12:72 10.1186/1471-2202-12-72
    1. Han Y. M. Y., Chan A. S., Sze S. L., Cheung M. C., Wong C., Lam J. M. K., et al. (2013). Altered immune function associated with disordered neural connectivity and executive dysfunctions: a neurophysiological study on children with autism spectrum disorders. Res. Autism Spectr. Disord. 7 662–674. 10.1016/j.rasd.2013.02.011
    1. Hargus E., Crane C., Barnhofer T., Williams J. M. (2010). Effects of mindfulness on meta-awareness and specificity of describing prodromal symptoms in suicidal depression. Emotion 10 34–42. 10.1037/a0016825
    1. Hasenkamp W., Barsalou L. W. (2012). Effects of meditation experience on functional connectivity of distributed brain networks. Front. Hum. Neurosci. 6:38 10.3389/fnhum.2012.00038
    1. Heeren A., Van Broeck N. V., Philippot P. (2009). The effects of mindfulness on executive process and autobiographical memory specificity. Behav. Res. Ther. 47 403–409. 10.1016/j.brat.2009.01.017
    1. John E. R., Prichep L. S., Fridman J., Easton P. (1988). Neurometrics: computer-assisted differential diagnosis of brain dysfunctions. Science 239 162–169. 10.1126/science.3336779
    1. Kilpatrick L. A., Suyenobu B. Y., Smith S. R., Bueller J. A., Goodman T., Creswell J. D., et al. (2011). Impact of mindfulness-based stress reduction training on intrinsic brain connectivity. Neuroimage 56 290–298. 10.1016/j.neuroimage.2011.02.034
    1. Klem G. H., Lüders H. O., Jasper H. H., Elger C. (1999). The ten-twenty electrode system of the International Federation. International Federation of Clinical Neurophysiology. Electroencephalogr. Clin. Neurophysiol. Suppl. 52 3–6.
    1. Kozasa E. H., Radvany J., Barreiros M. A. M., Leite J. R., Amaro E. (2008). Preliminary functional magnetic resonance imaging Stroop task results before and after a Zen meditation retreat. Psychiatry Clin. Neurosci. 62:366 10.1111/j.1440-1819.2008.01809.x
    1. Kozasa E. H., Sato J. R., Lacerda S. S., Barreiros M. A. M., Radvany J., Russell T. A., et al. (2012). Meditation training increases brain efficiency in an attentional task. Neuroimage 59 745–749. 10.1016/j.neuroimage.2011.06.088
    1. Lam L. C. W., Chau R. C. M., Wong B. M. L., Fung A. W. T., Tam C. W. C., Leung G. T. Y., et al. (2012). A 1-year randomized controlled trial comparing mind-body exercise (Tai Chi) with stretching and toning exercise on cognitive function in older Chinese adults at risk of cognitive decline. J. Am. Med. Dir. Assoc. 13 568.e15–568.e20. 10.1016/j.jamda.2012.03.008
    1. Lancaster J. L., Woldorff M. G., Parsons L. M., Liotti M., Freitas C. S., Rainey L., et al. (2000). Automated Talairach Atlas labels for functional brain mapping. Hum. Brain Mapp. 10 120–131. 10.1002/1097-0193(200007)10:3<120::AID-HBM30>;2-8
    1. Lewis J. D., Elman J. L. (2008). Growth-related neural reorganization and the autism phenotype: a test of the hypothesis that altered brain growth leads to altered connectivity. Dev. Sci. 11 135–155. 10.1111/j.1467-7687.2007.00634.x
    1. Lord C., Rutter M., Couteur A. L. (1994). Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J. Autism Dev. Disord. 24 659–685. 10.1007/BF02172145
    1. Luber B., Lisanby S. H. (2014). Enhancement of human cognitive performance using transcranial magnetic stimulation (TMS). Neuroimage 85 961–970. 10.1016/j.neuroimage.2013.06.007
    1. Marshall L., Molle M., Hallschmid M., Born J. (2004). Transcranial direct current stimulation during sleep improves declarative memory. J. Neurosci. 24:9985 10.1523/JNEUROSCI.2725-04.2004
    1. Mazziotta J., Toga A., Evans A., Fox P., Lancaster J., Zilles K., et al. (2001). A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos. Trans. R. Soc. Lond. B Biol. Sci. 356 1293–1322. 10.1098/rstb.2001.0915
    1. Minshew N. J., Goldstein G. (1993). Is autism and amnesic disorder? Evidence from the California Verbal Learning Test. Neuropsychology 7 209–216. 10.1037/0894-4105.7.2.209
    1. Minshew N. J., Goldstein G. (1998). Autism as a disorder of complex information processing. Ment. Retard. Dev. Disabil. Res. Rev. 4 129–136. 10.1002/(SICI)1098-2779(1998)4:2<129::AID-MRDD10>;2-X
    1. Minshew N. J., Goldstein G. (2001). The pattern of intact and impaired memory functions in autism. J. Child Psychol. Psychiatry 42 1095–1101. 10.1111/1469-7610.00808
    1. Minshew N. J., Goldstein G., Siegel D. J. (1997). Neuropsychologic functioning in autism: profile of a complex information processing disorder. J. Int. Neuropsychol. Soc. 3 303–316.
    1. Mizuhara H., Yamaguchi Y. (2007). Human cortical circuits for central executive function emerge by theta phase synchronization. Neuroimage 36 232–244. 10.1016/j.neuroimage.2007.02.026
    1. Mottron L., Belleville S., Stip E., Morasse K. (1998). A typical memory performance in an autistic savant. Memory 6 593–607. 10.1080/741943372
    1. Mottron L., Morasse K., Bellville S. (2001). A study of memory functioning in individuals with autism. J. Child Psychol. Psychiatry 42 253–260. 10.1111/1469-7610.00716
    1. Newberg A. B., Wintering N., Khalsa D. S., Roggenkamp H., Waldman M. R. (2010). Meditation effects on cognitive function and cerebral blood flow in subjects with memory loss: a preliminary study. J. Alzheimers Dis. 20 517–526.
    1. Norris S. L., Currieri M. (1999). “Performance enhancement training through neurofeedback,” in Introduction to Quantitative EEG and Neurofeedback eds Evans J. R., Abarbanel A. (San Diego, CA: Academic Press; ) 223–240. 10.1016/B978-012243790-8/50011-0
    1. Nyberg L., Marklund P., Persson J., Cabeza R., Forkstam C., Petersson K. M., et al. (2003). Common prefrontal activations during working memory, episodic memory, and semantic memory. Neuropsychologia 41 371–377. 10.1016/S0028-3932(02)00168-9
    1. O’Connor N., Hermelin B. (1989). The memory structure of autistic idiot-savant mnemonists. Br. J. Psychol. 80 97–111. 10.1111/j.2044-8295.1989.tb02305.x
    1. Omizo M. M., Loffredo D. A., Hammett V. L. (1982). Relaxation exercises for the learning disabled and family. Acad. Ther. 17 603–608.
    1. Osaka N., Osaka M., Kondo H., Morishita M., Fukuyama H., Shibasaki H. (2004). The neural basis of executive function in working memory: an fMRI study based on individual differences. Neuroimage 21 623–631. 10.1016/j.neuroimage.2003.09.069
    1. Pascual-Marqui R. D. (2002). Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find. Exp. Clin. Pharmacol. 24 5–12.
    1. Pascual-Marqui R. D., Esslen M., Kochi K., Lehmann D. (2002). Functional imaging with low-resolution brain electromagnetic tomography LORETA: a review. Methods Find. Exp. Clin. Pharmacol. 24(suppl. C) 91–95.
    1. Reaven J. A. (2009). Children with high-functioning autism spectrum disorders and co-occurring anxiety symptoms: implications for assessment and treatment. J. Spec. Pediatr. Nurs. 14 192–199. 10.1111/j.1744-6155.2009.00197.x
    1. Rippon G., Brock J., Brown C., Boucher J. (2007). Disordered connectivity in the autistic brain: challenges for the “new psychophysiology.” Int. J. Psychophysiol. 63 164–172. 10.1016/j.ijpsycho.2006.03.012
    1. Roden I., Kreutz G., Bongard S. (2012). Effects of a school-based instrumental music program on verbal and visual memory in primary school children: a longitudinal study. Front. Psychol. 3:572 10.3389/fpsyg.2012.00572
    1. Roig M., Nordbrandt S., Geertsen S. S., Nielsen J. B. (2013). The effects of cardiovascular exercise on human memory: a review with meta-analysis. Neurosci. Biobehav. Rev. 37 1645–1666. 10.1016/j.neubiorev.2013.06.012
    1. Ros T., Moseley M. J., Bloom P. A., Benjamin L., Parkinson L. A., Gruzelier J. H. (2009). Optimizing microsurgical skills with EEG neurofeedback. BMC Neurosci. 10:87 10.1186/1471-2202-10-87
    1. Rossion B., Pourtois G. (2004). Revisiting Snodgrass and Vanderwart’s object pictorial set: the role of surface detail in basic-level object recognition. Perception 33 217–236. 10.1068/p5117
    1. Rugg M. D., Otten L. J., Henson R. N. A. (2002). The neural basis of episodic memory: evidence from functional neuroimaging. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357 1097–1110. 10.1098/rstb.2002.1102
    1. Sauseng P., Klimesch W., Schabus M., Doppelmayr M. (2005). Fronto-partietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. Int. J. Psychophysiol. 57 97–103. 10.1016/j.ijpsycho.2005.03.018
    1. Short B. E., Kose S., Mu Q., Borckardt J., Newberg A., George M. S., et al. (2010). Regional brain activation during meditation shows time and practice effects: an exploratory FMRI study. Evid. Based Complement. Alternat. Med. 7 121–127. 10.1093/ecam/nem163
    1. Simanova I., Hagoort P., Oostenveld R., van Gerven M. (2014). Modality-independent decoding of semantic information from the human brain. Cereb. Cortex 24 426–434. 10.1093/cercor/bhs324
    1. Smith P. J., Blumenthal J. A., Hoffman B. M., Cooper H., Strauman T. A., Welsh-Bohmer K., et al. (2010). Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom. Med. 72 239–252. 10.1097/PSY.0b013e3181d14633
    1. Snodgrass J. G., Vanderwart M. (1980). A standardized set of 260 pictures: norm for name agreement, image agreement, familiarity, and visual complexity. J. Exp. Psychol. Learn. Mem. Cogn. 6 174–215. 10.1037/0278-7393.6.2.174
    1. Solé-Padullés C., Bartrés-Faz D., Junqué C., Clemente I. C., Molinuevo J. L., Baralló N., et al. (2006). Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. Cereb. Cortex 16 1487–1493. 10.1093/cercor/bhj083
    1. Squire L. P. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99 195–231. 10.1037/0033-295X.99.2.195
    1. Squire L. R., Zola-Morgan S. (1991). The medial temporal lobe memory system. Science 253 1380–1386. 10.1126/science.1896849
    1. Tager-Flusberg H. (1991). Semantic processing in the free recall of autistic children: further evidence for a cognitive deficit. Br. J. Dev. Psychol. 9 417–430. 10.1111/j.2044-835X.1991.tb00886.x
    1. Tang Y. Y., Lu Q., Geng X., Stein E. A., Yang Y., Posner M. I. (2010). Short-term meditation induces white matter changes in the anterior cingulate. Proc. Natl. Acad. Sci. U.S.A. 107 15649–15652. 10.1073/pnas.1011043107
    1. Thatcher R. W., North D., Biver C. (2005a). EEG and intelligence: relations between EEG coherence, EEG phase delay and power. Clin. Neurophysiol. 116 2129–2141. 10.1016/j.clinph.2005.04.026
    1. Thatcher R. W., North D., Biver C. (2005b). Parametric vs. non-parametric statistics of low resolution electromagnetic tomography (LORETA). Clin. EEG Neurosci. 36 1–8. 10.1177/155005940503600103
    1. Thorndike R. L., Hagen E. P., Sattler J. M. (1986). Stanford-Binet Intelligence Test 4th Edn. Chicago: Riverside.
    1. Toichi M., Kamio Y. (2002). Long-term memory and levels-of-processing in autism. Neuropsychologia 40 964–969. 10.1016/S0028-3932(01)00163-4
    1. Toichi M., Kamio Y. (2003). Long-term memory in high-functioning autism: controversy on episodic memory in autism reconsidered. J. Autism Dev. Disord. 33 151–161. 10.1023/A:1022935325843
    1. Volf N. V., Razumnikova M. (1999). Sex differences in EEG coherence during a verbal memory task in normal adults. Int. J. Psychophysiol. 34 113–122. 10.1016/S0167-8760(99)00067-7
    1. Wayne P. M., Walsh J. N., Taylor-Piliae R. E., Wells R. E., Papp K. V., Donovan N. J., et al. (2014). Effect of Tai Chi on cognitive performance in older adults: systematic review and meta-analysis. J. Am. Geriatr. Soc. 62 25–39. 10.1111/jgs.12611
    1. Wechsler D. (2010). Wechsler Intelligence Scale for Children 4th Edn. Hong Kong: King-May Psychological Assessment.
    1. Weiss S., Müller H. M., Rappelsberger P. (2000). Theta synchronization predicts efficient memory encoding of concrete and abstract nouns. Cogn. Neurosci. 11 2357–2361. 10.1097/00001756-200008030-00005
    1. Weiss S., Rappelsberger P. (2000). Long-range EEG synchronization during word encoding correlates with successful memory performance. Cogn. Brain Res. 9 299–312. 10.1016/S0926-6410(00)00011-2
    1. Williams D. L., Goldstein G., Minshew N. J. (2006). The profile of memory function in children with autism. Neuropsychology 20 21–29. 10.1037/0894-4105.20.1.21
    1. Xu J., Vik A., Groote I. R., Laqopopulos J., Holen A., Ellingsen al. (2014). Nondirective meditation activates default mode network and areas associated with memory retrieval and emotional processing. Front. Hum. Neurosci. 8:86 10.3389/fnhum.2014.00086
    1. Zipkin D. (1985). Relaxation techniques for handicapped children: a review of literature. J. Spec. Educ. 19 283–289. 10.1177/002246698501900305

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa