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Advancing Our Understanding of the Brain in Autism: Contribution of Functional MRI and Diffusion Tensor Imaging

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Advancing Our Understanding of the Brain in Autism: Contribution of Functional MRI and Diffusion Tensor Imaging REVIEW Advancing our understanding of the brain in autism: contribution of functional MRI and diffusion tensor imaging Neuroimaging research in the last two decades has contributed significantly in illuminating our knowledge of the neurobiology of autism spectrum disorders. Using modern brain imaging methods, particularly functional MRI and diffusion tensor imaging, researchers have examined the make-up and functioning of the brain in autism. Findings of widespread functional, anatomical and connectional abnormalities in the brains of individuals with autism spectrum disorders have helped in conceptualizing autism as a system- wide neural disorder. This review explores the results of functional MRI and diffusion tensor imaging studies to characterize the brain organization in autism spectrum disorders, to establish brain–behavior relationship, to apply the knowledge gained from neuroimaging research to diagnostic classification and to design effective treatment for individuals with autism. 1 KEYWORDS: autism n diffusion tensor imaging n effective connectivity n functional Lauren E Libero connectivity n functional MRI n white matter & Rajesh K Kana*1 1Department of Psychology, University “We must, then, assume that these children have autism. Specifically, the development and imple- of Alabama at Birmingham, CIRC 235G, 1719 6th Avenue South, come into the world with innate inability to form mentation of functional MRI (fMRI) and dif- Birmingham, AL 35294-0021, USA the usual, biologically provided affective contact fusion tensor imaging (DTI) techniques have *Author for correspondence: Tel.: +1 205 934 3171 with people, just as other children come into the facilitated an explosion of research and discov- Fax: +1 205 975 6330 world with innate physical or intellectual handi- ery in the field. Within the last few decades, [email protected] caps. If this assumption is correct, a further study fMRI and DTI have provided scientists with of our children may help to furnish concrete cri- sophisticated neuroimaging tools to study the teria regarding the still diffuse notions about the live human brain in vivo, thus paving the way constitutional components of emotional reactivity. for neurobiologically informed characterization For here we seem to have pure-culture examples of the biological basis of ASD. of inborn, autistic disturbances of affective Despite Kanner’s early suggestion of a biologi- contact.” cal cause for ASD, decades of research have not – Leo Kanner (1943) provided a single and widely accepted etiology of ASD. This may perhaps reflect the inherent dif- In the first historical reference to autism spec- ficulty in explaining a complex multi dimensional trum disorder (ASD), Kanner emphasized the disorder such as ASD, which is essentially a potential biological association of the disorder, constellation of a wide range of impairments in describing how some inborn abnormalities must social, communicative and behavioral domains. be driving the behavioral impairments seen in Shortly after Kanner’s original paper, psycho- the affected children studied [1] . Since 1943, analytic theories emerged, rejecting the possibil- the quest for understanding the biological basis ity of a biological role in the etiology of ASD. of ASD has been the focus of autism research. Indeed, it should be noted that Kanner himself Although such neurobiological pursuits have not came to dismiss a biological link for the disor- resulted in establishing a firm etiology of the der, favoring an etiology for ASD founded in disorder, significant strides have been made in familial relationships and behavioral upbringing these areas have been made. Neuroscience and [2]. This view was then popularized by the pub- genetics research have certainly illuminated our lication of Bettelheim’s famous book The Empty understanding of the biological underpinnings Fortress. Bettelheim’s controversial view focused of ASD and the nature of brain functioning in on ‘refrigerator’ mothers who are cold, distant ASD. Although electrophysiological, cellular and do not provide their babies with adequate and animal models have significantly contrib- stimulation and affection, causing their chil- uted to a better conceptualization of ASD, the dren to withdraw into an autistic state [3]. At a advent of modern neuroimaging techniques time when Freudian psychology ruled, such a have revolutionalized neuroscience research in proposition emphasizing the mother–child bond part of 10.2217/IIM.13.46 © 2013 Future Medicine Ltd Imaging Med. (2013) 5(5), 453–465 ISSN 1755-5191 453 REVIEW Libero & Kana seemed, to many, to be a logical progression of records or interviews of surviving relatives). In thought, on how one could become autistic. By addition, patients can be studied longitudinally contrast to popular psychological theories blam- (allowing for developmental studies of the brain ing inefficient parenting as the cause of ASD, in ASD), a vital dimension in the context of neu- Rimland published his neurobiological theory rodevelopmental disorders such as ASD. fMRI of ASD in 1964 [4]. Rimland argued that there and DTI are also sophisticated and more versa- was no evidence proving the refrigerator mother tile in terms of what they enable researchers to theory, thus the etiology of ASD must have a dif- examine. Data from these modalities can include ferent source. He believed physiological factors, task-based brain activity, blood flow, examining specifically physical abnormalities in the brain the brain at rest, measuring different types of con- (possibly the reticular formation) were respon- nectivity, and establishing links between biology sible for the symptoms of ASD. This was the first and behavior. Neuroimaging studies provide evi- significant step in eroding the negative effects of dence for widespread functional and structural Bettelheim’s claims and moving towards a more abnormalities in the brain, seen early on in babies biological-based understanding of the disorder. and toddlers with ASD [20]. Such evidence has In 1978, Damasio and Maurer published a neu- helped to establish ASD as a disorder of neuro- robiological account of ASD, after finding simi- developmental origin. Neuroimaging studies have larities between the behaviors of individuals with uncovered widespread abnormalities in the autis- ASD and the behavior of adults with frontal cor- tic brain at focal as well as at global levels, leading tex damage [5]. They suggested that dysfunction to a systems-level characterization of the disorder in the mesolimbic cortex, frontal and temporal [20]. This paper will explore the contribution of lobes, neostriatum, and thalamus, may under- neuroimaging, especially fMRI and DTI meth- lie the ASD symptom atology. This marked a ods, in advancing our understanding of the neural movement towards establishing a brain–behavior mechanisms underlying autism. Furthermore, we relationship in ASD. Early studies of the brain will examine the impact of a comprehensive char- in autism focused on auditory nerve and brain acterization of autism in uncovering the causes stem evoked responses [6,7], rapid eye movement of behavioral impairments, in identifying and activity during rapid eye movement sleep [8] and classifying individuals with and without autism, brainwaves measured by EEG [9] with limited and in developing better treatments for affected results. Based on visual observations of affected individuals. children’s physical features, the field also focused on measuring brain volume and cell counts, via Neuroimaging to elucidate brain head circumference measurements [10–13] and functioning in ASD post-mortem investigations [14–19]. While the The number of published fMRI studies in the results of these studies were inconsistent, they field of autism has increased dramatically in highlighted widespread abnormalities in the the last decade, with published biology-based brain in ASD, emphasizing the need for further studies in ASD representing a fourfold increase neurobiological investigations. from 2000 to 2010 [21]. These studies have In the last two decades, neuroimaging research examined several domains of thinking, such as has played an important role in eliminating spec- social, cognitive and visuospatial processing, in ulative psychoanalytic accounts of autism and in children and adults with ASD completing tasks clearing up misconceptions about the disorder. including face processing, theory-of-mind, lan- While previous methods were limited to indirect guage comprehension, embedded figures tasks, or surface measures (event-related potentials, response-inhibition tasks, reward processing, EEG and head circumference) of the brain, or biological motion and working memory. Find- post-mortem samples (necropsy), neuroimaging ings from these studies point to several foci in has supplied a vital avenue for studying the brain the brain that respond differently in individuals in great detail in ASD while at work and in vivo. with autism compared with typically developing fMRI and DTI methods allow researchers to control participants [20,22–24]. In particular, stud- examine not only the organization and connectiv- ies have found decreased activation in the medial ity of the brain but also how the brain responds in and dorsolateral prefrontal cortex and anterior real time to stimuli. Since the brain can be investi- cingulate cortex [25–31], amygdala [32–35], fusiform gated in live humans, information gathered about gyrus [33,34,36–38], superior temporal sulcus (STS) the brain can also be associated
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