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The Autistic Brain: Birth Through Adulthood Eric Courchesnea,C, Elizabeth Redcayb and Daniel P

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The Autistic Brain: Birth Through Adulthood Eric Courchesnea,C, Elizabeth Redcayb and Daniel P The autistic brain: birth through adulthood Eric Courchesnea,c, Elizabeth Redcayb and Daniel P. Kennedya Purpose of review Introduction We discuss evidence of brain maldevelopment in the first years Autism is a behaviorally defined disorder clinically of life in autism and new neuroanatomical and functional characterized by social deficits, language impairments, evidence from later ages of development. and restricted and repetitive behaviors and interests Recent findings [1,2]. Research has revealed additional abnormalities in Head circumference, an accurate indicator of brain size in sensory, motor, attention, memory, speech, exploring children, was reported to jump from normal or below normal size novelty and many other areas of behavioral and cognitive in the first postnatal months in autistic infants to the 84th functioning [3]. percentile by about 1 year of age; this abnormally accelerated growth was concluded by 2 years of age. Infants with extreme Autism is most often first clinically recognized and head (and therefore brain) growth fell into the severe end of the diagnosed at between 2 and 4 years of age. However, clinical spectrum and had more extreme neuroanatomical parental comments, single case reports, and retrospective abnormalities. In the frontal and temporal lobes in autism, there studies suggest that subtle motor, sensory, attention and have been reports of abnormal increases in gray and white matter social behavioral abnormalities may often be present, but at 2 to 4 years; reduced metabolic measures; deviant diffusion clinically overlooked, during the first or second years of tensor imaging results in white matter; underdeveloped cortical life [4–7]. Neural maldevelopment must underlie and minicolumns; and reduced functional activation during socio- precede these early autistic behavioral abnormalities, but emotional, cognitive and attention tasks. Cerebellar abnormalities little is known about defects and abnormal processes at included abnormal volumes, reduced number and size of Purkinje this very early age. neurons in the vermis and hemispheres, molecular defects, and reduced functional activation in posterior regions. By contrast, studies of older children and adults have Summary provided magnetic resonance imaging (MRI), functional A new neurobiological phenomenon in autism has been MRI, and postmortem evidence of cerebral, cerebellar, described that precedes the onset of clinical behavioral and limbic abnormalities [3,8–11]. Therefore, although symptoms, and is brief and age-delimited to the first two years autism is clearly understood to be a disorder of early of life. The neurobiological defects that precede, trigger, and brain development, until recently there has been a large underlie it may form part of the developmental precursors of gap in the knowledge about its origins, and therefore some of the anatomical, functional, and behavioral about whether or not findings on older patients reflect manifestations of autism. Future studies of the first years of life early maldevelopmental processes. may help elucidate the factors and processes that bring about the unfolding of autistic behavior. In the past few years, studies have helped to fill this gap Keywords by providing information about brain growth abnormal- autism, brain growth, development, neuroimaging, head ities within the first years of life in autism. In this review, circumference, MRI, fMRI, postmortem we place these new results into the context of recent neuroimaging studies of autism at later ages, thereby Curr Opin Neurol 17:489–496. # 2004 Lippincott Williams & Wilkins. providing a first look at aspects of brain maldevelopment Departments of aNeurosciences, and bPsychology, University of California, San from birth to adulthood in this disorder. Consistent Diego, California, USA; and cCenter for Autism Research, Children’s Hospital Research Center, San Diego, California, USA patterns of neural maldevelopment are observed, and hypotheses and new evidence regarding defects under- Correspondence to Eric Courchesne, Center for Autism Research, 8110 La Jolla lying growth abnormalities are discussed. Shores Drive, Suite 201, San Diego, CA 92037, USA Tel: +1 858 551 7925; e-mail: [email protected] Brain growth abnormality from birth to Current Opinion in Neurology 2004, 17:489–496 adulthood in autism Abbreviations Brain development in autism from 2 years of age onward ASD autism spectrum disorder has been the subject of recent MRI studies, as we DTI diffusion tensor imaging discuss below. However, because autism is not typically HC head circumference MRI magnetic resonance imaging clinically recognized before 2 to 4 years of age, no MRS magnetic resonance spectroscopy neuroimaging evidence exists regarding brain growth PDD–NOS pervasive developmental disorder not otherwise specified abnormality from birth to 2 years of age. Fortunately, # 2004 Lippincott Williams & Wilkins records of age-related changes in head circumference 1350-7540 (HC) from birth can provide clues about brain growth DOI: 10.1097/01.wco.0000137542.14610.b4 489 490 Neuroimaging during these first two years of life. Studies of the increase than the PDD–NOS infants (Fig. 2). This is correlation between HC and MRI brain volume have consistent with a previous prediction [14] that brain shown that HC in young autistic and normal children is overgrowth may be earlier, more rapid and more an accurate index of brain volume, although it is a poor substantial in more severely affected autistic children. index of brain volume at progressively older ages [12]. Moreover, the study reported that in their ASD group, HC measures thus offer an opportunity to assay brain brain size at birth and overgrowth by the end of the first growth in autism at early ages. year of life were strongly correlated with abnormal cerebellar and cerebral volumes, respectively, at 2–5 A process of brain overgrowth in the first two years of years of age. life Longitudinal changes in HC during the first 2 years of This evidence indicates a process of early, brief and age- life were analyzed in a sample of autism spectrum limited brain overgrowth in autism during the first two disorder (ASD) patients that included both autistic years of life. To our knowledge, this is the first evidence disorder (the severe end of the spectrum) and pervasive of brain maldevelopment in process before the overt developmental disorder not otherwise specified (PDD– clinical behavioral manifestation of the disorder. Further NOS; the mild end) patients [13 ..]. Compared with the studies will be needed to delineate the ages of onset, Centers for Disease Control and Prevention HC norms, peak, and cessation of this process more precisely. HC in the ASD groups was at the 25th percentile at birth and then increased rapidly to the 84th percentile by 6–14 Neuroanatomical abnormalities at 2–5 years of age months of age (Fig. 1). This period of abnormally By 2 to 3 years of age, 90% of autistic toddlers had brain accelerated HC increase, and therefore brain growth, was volumes that exceeded normal average toddlers; cerebral apparently largely concluded before the end of the gray and white matter and cerebellar white matter second year of life (Fig. 1). volumes were abnormally large [14]. This first report of The same study also reported that those at the more severe end of the spectrum, the autistic disorder infants, Figure 2. Increase in head circumference from birth to 6–14 months had a substantially greater rate and amount of HC of age between infants with Autistic Disorder and infants with PDD- NOS Figure 1. Age-related changes in head circumference during infancy Mean 3 in autism spectrum disorder Head Circum- ference 2 Mean 2 Z score Head Circum- P=0.02 1 ference 1.5 P=0.001 Z score 1 0 0.5 –1 0 –2 –0.5 –3 P=0.001 Birth 6–14 mo –1 Birth 1–2 3–5 6–14 15–28 Autistic disorder (n=17) Age, mo PDD-NOS (n=5) At birth and at 1–2 months of age, head circumference in a longitudinal PDD–NOS indicates pervasive developmental disorder not otherwise autism spectrum disorder group was statistically significantly below the specified. At each age and for each group, short horizontal bars indicate Centers for Disease control and Prevention (CDC) mean for healthy mean head circumference. The infants with Autistic Disorder (closed infants, but by 6–14 months of age, it was more than 1.0 SD (84 circles; n = 17) had a greater rate of growth in head circumference percentile) above the mean for healthy infants. The CDC mean of healthy between birth and 6–14 months of age than did those with PDD–NOS infants at each age is 0. Error bars are SEM. (open circles; n = 5). Reproduced with permission from Courchesne et al. [13 ..]. Reproduced with permission from Courchesne et al. [13..]. The autistic brain Courchesne et al. 491 brain and cerebral enlargement in young children was By 2 to 4 years of age, autistic children had the most recently replicated in an independent study of 3–4-year- extreme enlargement of gray and white matter volume in old autistic and normal children which also found larger frontal and temporal lobes; white matter abnormality was than normal volumes of whole brain, cerebrum, and maximal in the frontal and parietal lobes (Fig. 3) [16]. In cerebellum and additionally found amygdala enlarge- contrast, the occipital lobes were not significantly ment [15]. enlarged. Consistent with this differential enlargement of the frontal and temporal gray matter, an MRI sulcal mapping study of autistic preadolescents showed an- terior and superior shifting of several sulci, with the greatest deviations from normal being the superior Figure 3. In autistic 2–4-year-old children frontal lobes have the most abnormal enlargement of white and gray matter volumes frontal, inferior frontal, and superior temporal sulci and the Sylvian fissure [17]. 3 White Cerebellar maldevelopment is certain, but complex. By 2 matter ** to 4 years of age in autistic children, cerebellar gray matter volume was not enlarged, and lobules VI–VII of 2 * the posterior vermis were actually reduced [14].
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