Greater Right Hemisphere Recruitment in Response to Figurative Speech in Autism

Background: Interpreting figurative speech involves inferring speaker’s intent by integrating word meaning with context. This may pose challenge to individuals with autism perhaps due to their weak central coherence (Frith, 1989). It has been found that such difficulties are prevalent even when individuals exhibit otherwise fluent language ability (Szatmari et al., 1990). A pun is a figure of speech in which a speaker deliberately invokes multiple meanings through a word or phrase likely resulting in a joke. Comprehending puns may represent a unique challenge for individuals with autism since it involves identifying multiple meanings of a word, embedding it in right contexts, and understanding the underlying humor.

Objectives: The goal of the current study was to delineate the role of core cortical language areas (LIFG: left inferior frontal gyrus and LSTG: left superior temporal gyrus) and hemispheric differences in their recruitment in autism while comprehending figurative speech.

Methods: Sixteen high-functioning young adults with autism and 16 age and IQ-matched typical control participants took part in the study. The stimuli consisted of a series of sentences presented visually, in a blocked design format, in the MRI scanner.  The sentences were grouped into two conditions: pun and literal. In the pun condition, the last word of the sentence was a pun that evoked multiple meanings (e.g., my advanced geometry class is full of squares). A 24-second fixation repeated at several intervals during the scan formed the baseline for comparison.  Each sentence was presented for 5000 ms and each block consisted of six sentences.  Following the fMRI session, participants completed a short debriefing in which they were asked about their understanding of pun, the difficulty of the task, and the speed at which they performed the task. In addition to activation analyses, an Independent Component Analysis (ICA) was performed to determine the degree to which the components comprising the left hemisphere language regions correlated with the predicted BOLD signal for each group.   

Results: Participants with autism, relative to typical controls, showed an increase in overall activation while comprehending sentences containing puns, particularly within the right hemisphere as well as in relatively posterior brain areas. There was also reduced response in LIFG, LSTG, and in LSFG, and more distributed recruitment of regions in autism relative to control participants (p = 0.001; k = 64 voxels). A two-way ANOVA conducted to partial out the effect of VIQ confirmed that the differences in activation in these regions were due to a main effect of group. An Independent Component Analysis indicated that the component comprising of the LH language regions was significantly more correlated with the predicted BOLD signal for the control than for the autism group. Furthermore, symptom severity in autism was found to be negatively correlated with LMTG response to pun [F(2)=6.79, R²=0.80].

Conclusions: The difference in the recruitment of brain areas in autism (decreased left hemisphere activation, reduced activation in regions associated with humor) as compared to that of controls may suggest compensatory processing and alternate neural routes to deal with language difficulties.