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Sylvian Fissure and Parietal Anatomy in Children with Autism Spectrum

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Sylvian Fissure and Parietal Anatomy in Children with Autism Spectrum Behavioural Neurology 25 (2012) 327–339 327 DOI 10.3233/BEN-2012-110214 IOS Press Sylvian fissure and parietal anatomy in children with autism spectrum disorder Tracey A. Knausa,b,∗, Helen Tager-Flusbergd and Anne L. Foundasa,b,c aBrain and Behavior Program at Children’s Hospital, Louisiana State University Health Sciences Center, New Orleans, LA, USA bDepartment of Neurology, Louisiana State University Health Sciences Center, New Orleans, LA, USA cDepartment of Cell Biology and Anatomy, Louisiana State University Health Sciences Center, New Orleans, LA, USA dDepartment of Psychology, Boston University, Boston, MA, USA Abstract. Autism spectrum disorder (ASD) is characterized by deficits in social functioning and language and communication, with restricted interests or stereotyped behaviors. Anatomical differences have been found in the parietal cortex in children with ASD, but parietal subregions and associations between Sylvian fissure (SF) and parietal anatomy have not been explored. In this study, SF length and anterior and posterior parietal volumes were measured on MRI in 30 right-handed boys with ASD and 30 right-handed typically developing boys (7–14 years), matched on age and non-verbal IQ. There was leftward SF and anterior parietal asymmetry, and rightward posterior parietal asymmetry, across groups. There were associations between SF and parietal asymmetries, with slight group differences. Typical SF asymmetry was associated with typical anterior and posterior parietal asymmetry, in both groups. In the atypical SF asymmetry group, controls had atypical parietal asymmetry, whereas in ASD there were more equal numbers of individuals with typical as atypical anterior parietal asymmetry. We did not find significant anatomical-behavioral associations. Our findings of more individuals in the ASD group having a dissociation between cortical asymmetries warrants further investigation of these subgroups and emphasizes the importance of investigating anatomical relationships in addition to group differences in individual regions. Keywords: Autism, parietal, Sylvian fissure, MRI, language, asymmetry 1. Introduction are the building blocks of language, allowing commu- nication between a sender and receiver [3] Planning Both lesion and neuroimaging studies have shown tool-use actions has been shown to activate the same that the left inferior parietal lobule (supramarginal regions, including left parietal cortex, as planning com- gyrus, Brodmann area,BA 40) plays a critical role in the municative gestures [4]. Action production involves a representation of learned, skilled movements (i.e. prax- distributed network that includes the anterior intrapari- is representations) (for review [1]). Both action pro- etal cortex, which has strong connections to the supple- duction and action understanding are thought to relate mentary motor cortex that functions in action planning to language development and understanding of speech and motor preparation [2]. Action understanding in- and gestures [2]. Action understanding and production volves the mirror neuron system (MNS) [2,5]. Mirror neurons have been found in the inferior frontal gyrus, as well as in parietal areas, namely the supramarginal ∗Address for correspondence: Tracey A. Knaus, Ph.D., Brain and gyrus, providing further support for the importance of Behavior Program at Children’s Hospital of New Orleans, Depart- the inferior parietal cortex in action production and un- ment of Neurology, Louisiana State University Health Sciences Cen- ter, 1542 Tulane Avenue, New Orleans, LA 70112, USA. Tel.: +1 derstanding [6,7, for review, 8]. Theoretically, when 504 896 7745; Fax: +1 504 584 2909; E-mail: [email protected]. we witness actions performed by another the informa- ISSN 0953-4180/12/$27.50 2012 – IOS Press and the authors. All rights reserved 328 T.A. Knaus et al. / Posterior Perisylvian Anatomy in ASD tion is subjected to sensory processing of elemental Deficits in language and communication are a core fea- sensory inputs (e.g. visual gesture or auditory verbal) ture of ASD, however, a range of language abilities is onto higher order association areas (i.e. visual analy- seen in ASD, from those who never develop functional sis of object representation). These representations in language, to those who score normal or above on stan- turn must be mapped onto conceptual systems for the dardized language tests [19]. Subtle language problems individual to know what others are doing (i.e. knowl- exist in all individuals with ASD, particularly pragmat- edge of action). These independent, but related pro- ic or social aspects of language, non-literal interpreta- cesses, must develop and function in an integrated and tion, and semantic processing [20]. Although not part efficient way if the individual is to acquire a gestural of the diagnostic criteria, motor deficits have consis- and language communication system. The right pari- tently been found in individuals with ASD, including etal cortex is more critical than the left homologue in impairments in imitation (for review [21]) and in praxis mediating spatial perception, including the direction of functions [22]. Differences in motor planning [23,24] visually guided movements and in directing attention and difficulties in action understanding [25] have also with reference to body schema (for review [9,10]). been found in people with ASD. Some studies have re- Parietal regions develop in relation to the Sylvian fis- ported deficits of the MNS in ASD (for review [26]) and sure (SF), which is formed by the overgrowth of adja- although still unresolved [27,28], several groups have cent brain regions (i.e. opercula), including the inferior proposed that a dysfunction in the MNS is responsible frontal, superior temporal, and inferior parietal lobes, for core social and language deficits in ASD (i.e. the and is anatomically asymmetric. The left SF is longer broken mirror neuron theory of ASD) (for review [26, in its posterior horizontal extension compared to the 29]). Given the importance of the parietal cortex in ac- right (i.e. a longer horizontal length), while the right tion planning and understanding and in the MNS, these SF is shorter and tends to angle up more sharply (i.e. behavioral findings suggest that there may be dysfunc- longer vertical length) (for reviews [11,12]). This con- tion within these neural systems that could be found at figuration is found in over 75% of adults and children the level of macroscopic anatomical anomalies in the and SF anatomy has been found to be related to handed- parietal region. ness [13,14] and language abilities [15]. In addition, a Several recent studies have examined the anatomy study examining the radiographic correlate of the pos- of the parietal lobe in ASD, with some differences be- terior extent of the Sylvian fossa found an association ing noted. A larger parietal volume has been found in with language laterality based on Wada testing [16]. children, after controlling for total brain volume [30], Several post-mortem studies have shown that the ad- and in adolescents and young adults with ASD [31] jacent parietal operculum develops asymmetrically in relative to controls. Increased cortical thickness has relation to these prominent SF asymmetries. Rubens been documented in parietal regions in children [32] and colleagues found an increase in the parietal oper- and adolescents with ASD [33] compared to typically culum, rostral to the posterior ascending ramus in the developing individuals. In contrast to these findings, left hemisphere (associated with the greater horizontal one recent study found that the left parietal cortex was SF length) and an expansion caudal to the posterior thinner in children and adults with ASD relative to con- ascending ramus in the right cerebral hemisphere (as- trols with this thinner parietal cortex found bilaterally sociated with the shortened horizontal SF length) [17]. in children [34]. Differences in cortical folding have al- A more recent MRI study of healthy adults showed so been found in the parietal cortex in ASD. One study the same relationships with the anterior and posterior reported increased cortical folding in ASD relative to segments of the parietal cortex linked to the SF anato- controls with a stronger effect in children compared to my [11]. These gross anatomical asymmetries may re- adolescents [35]. Another study investigated monozy- late to hemispheric differences in parietal lobe func- gotic twins discordant for ASD compared to typically tions. developing controls and found increased cortical fold- Autism spectrum disorder (ASD) is an umbrella ing in the right parietal lobe in children with ASD and term, including classic autism, pervasive developmen- their unaffected co-twins relative to controls [36]. A tal disorder – not otherwise specified (PDD-NOS), and study of young children found increased white matter Asperger syndrome. ASD is a neurodevelopmental in parietal regions in the ASD group compared to con- disorder definedbysocialdeficits, language and com- trols [37]. A recent study examined the relationship munication impairments, and the presence of restrict- between parietal size and language and motor functions ed or unusual interests or stereotyped behaviors [18]. in children with ASD [38]. They reported a signifi- T.A. Knaus et al. / Posterior Perisylvian Anatomy in ASD 329 cant correlation between left parietal gray matter vol- be associations between SF anatomy and parietal vol- umewithageoffirst word, such that larger volume was umes, based on
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