Sensory Processing Patterns and Fusiform Activity During Face Processing in Autism Spectrum Disorder
Sensory Processing Patterns and Fusiform Activity During Face Processing in Autism Spectrum Disorder
Sensory Processing Patterns and Fusiform Activity During Face Processing in Autism Spectrum Disorder
A growing body of evidence has indicated that individuals with autism spectrum disorder (ASD) exhibit abnormal reac-
tions to sensory stimuli and impaired face processing. Although behavioral studies have reported that individual differ-
ences in sensory processing patterns are correlated with performance in face processing tasks, the neural substrates
underlying the association between sensory processing patterns and face processing remain unknown. Using functional
magnetic resonance imaging, the present study examined the relationships between sensory processing patterns assessed
with the Adolescent/Adult Sensory Profile (AASP) and brain activity during a one-back task with two types of stimuli (face
or house pictures). We enrolled 18 Japanese adults with ASD and 19 age- and IQ-matched controls. Sensation Avoiding
scores, which were assessed using the AASP, were positively correlated with right fusiform activity during the presenta-
tion of pictures of faces in the ASD group, but not in the control group. This suggests that abnormal sensory processing
patterns in ASD are associated with abnormal face-related brain activity, possibly resulting in impaired face processing.
Autism Res 2020, 00: 1–10. © 2020 The Authors. Autism Research published by International Society for Autism Research
published by Wiley Periodicals, Inc.
Lay Summary: Sensory abnormalities are one of the most common symptoms in people with autism spectrum disorder
(ASD). This study shows that individuals with ASD who react abnormally to sensory stimuli also exhibit atypical brain
activity when recognizing faces. Abnormal sensory processing may partly explain the difficulty that people diagnosed
with ASD have in identifying others’ faces.
Keywords: autism spectrum disorder; face processing; sensory processing; sensory profile; fMRI; fusiform gyrus
From the Research Center for Child Mental Development, Hamamatsu University School of Medicine, Hamamatsu, Japan (A.K.-F., T.I., K.W., H.I., K.S.,
K.J.T.); United Graduate School of Child Development, Hamamatsu University School of Medicine, Hamamatsu, Japan (A.K.-F., T.I., K.W., K.S., K.J.T.);
Miyagi Children’s Hospital, Sendai, Japan (K.W.); Department of Contemporary Education, Chubu University, Kasugai, Japan (H.I.); Ogasa Hospital,
Kakegawa, Japan (K.S.); Kojin Hospital, Nagoya, Japan (A.S.); Research Center for Child Mental Development, University of Fukui, Fukui, Japan (K.H.);
United Graduate School of Child Development, University of Fukui, Fukui, Japan (K.H.); Department of Neuropsychiatry, Faculty of Medical Sciences,
University of Fukui, Fukui, Japan (K.H.); School of Contemporary Sociology, Chukyo University, Toyota, Japan (M.T.)
Received January 7, 2019; accepted for publication February 3, 2020
Address for correspondence and reprints: Kenji J. Tsuchiya, Research Center for Child Mental Development, Hamamatsu University School of Medicine,
Handayama 1 Higashiku, Hamamatsu 431-3192, Japan. E-mail: [email protected]
Published online 00 Month 2020 in Wiley Online Library (wileyonlinelibrary.com)
DOI: 10.1002/aur.2283
© 2020 The Authors. Autism Research published by International Society for Autism Research published by Wiley Periodicals, Inc.
Abbreviations: ASD: individuals with autism spectrum disorder; TD: typically developing individuals.
For behavioral data in the one-back task, statistics on direct group comparisons in each picture type (face, house) are shown.
carefully and to memorize them temporarily. They were fMRI Data Acquisition
also required to press a button with their right index fin-
ger as quickly as possible when an identical picture was T2*-weighted images with blood oxygenation level-
successively presented. Ten pictures served as target stim- dependent contrast were collected with a 3-T MRI scanner
uli in each block. A fixation cross was presented for 20 sec (Signa HDxt, GE Healthcare) at the Kojin Hospital (Nagoya,
before and after each stimulus block. In addition, a 25-sec Japan) using gradient-echo echo-planar imaging. The
fixation block was inserted at the beginning of the experi- following parameters were used: repetition time
ment, and a termination message was presented for 5 sec (TR) = 2,500 msec, echo time (TE) = 30 msec, field of
at the end of the experiment. view = 210 × 210 mm2, slice thickness = 3.0 mm with
ASD1 [−50, −74, −8] [44, −72, −10] – [16, −4, −16]
ASD2 [−44, −48, −26] [40, −52, −20] – –
ASD3 [−44, −56, −22] [42, −68, −18] [−18, −2, −28] –
ASD4 – [46, −52, −18] – [26, 0, −30]
ASD5 – [44, −50, −24] – [22, −6, −12]
ASD6 [−40, −50, −20] [44, −52, −20] [−20, −4, −26] [24, −6, −12]
ASD7 – – – [28, 4, −28]
ASD8 – [44, −56, −18] – –
ASD9 [−44, −48, −26] [46, −48, −22] [−28, −2, −22] [22, −4, −18]
ASD10 [−42, −50, −16] [40, −58, −18] [−22, −4, −14] [24, 0, −14]
ASD11 [−46, −46, −28] [46, −48, −26] [−22, −8, −24] [24, −6, −18]
ASD12 [−48, −60, −22] [40, −54, −18] [−18, −8, −14] [16, −4, −16]
ASD13 [−46, −50, −24] [44, −58, −14] [−24, −6, −18] [30, −6, −16]
ASD14 [−20, −62, −8] [40, −72, −16] [−16, −6, −16] [22, −8, −12]
ASD15 [−40, −50, −14] [42, −64, −12] – [16, −6, −20]
ASD16 [−44, −60, −14] [46, −64, −18] [−18, 2, −22] [20, 0, −16]
ASD17 [−40, −42, −26] [46, −50, −18] – [20, −4, −16]
ASD18 [−46, −44, −18] – [−18, 2, −22] [34, −2, −24]
TD1 [−38, −66, −10] [40, −52, −20] [−20, −10, −12] –
TD2 [−48, −60, −18] [42, −56, −10] [−16, −4, −18] [20, −4, −16]
TD3 [−44, −52, −24] [40, −56, −10] [−16, −4, −16] [22, −6, −12]
TD4 [−36, −60, −8] [40, −48, −12] [−22, 0, −16] [22, −2, −16]
TD5 [−48, −64, −18] [40, −56, −20] [−22, −8, −14] [26, −2, −18]
TD6 [−50, −60, −16] [50, −46, −18] [−18, −6, −20] [18, −6, −22]
TD7 [−46, −58, −22] [48, −48, −24] – [30, 2, −24]
TD8 – – – –
TD9 [−40, −80, −14] [38, −40, −18] [−26, −4, −14] [20, 0, −16]
TD10 [−46, −74, −14] [40, −74, −12] [−18, −8, −14] [20, −6, −16]
TD11 [−42, −54, −22] [44, −72, −18] [−26, 0, −24] [20, −2, −26]
TD12 [−42, −48, −16] – [−18, −4, −16] [24, −8, −12]
TD13 [−40, −48, −16] [46, −46, −20] [−16, −2, −18] [24, 4, −28]
TD14 [−38, −44, −24] – – [20, −4, −16]
TD15 [−40, −60, −18] [46, −46, −20] [−18, −2, −18] [26, 0, −18]
TD16 [−44, −52, −20] [42, −50, −16] [−22, −12, −14] [16, −4, −18]
TD17 [−38, −54, −20] [46, −60, −16] [−20, −4, −14] [24, −8, −14]
TD18 [−42, −72, −6] [48, −56, −20] – –
TD19 [−48, −64, −20] [48, −58, −20] [−26, −4, −22] [26, 0, −14]
Figure 2. Group-level brain activation during the one-back task. The bilateral fusiform gyrus and amygdala showed increased activity
for the face > house comparison when the two groups were combined. R: right, L: left.
Right amygdala 24 −6 −14 7.18 653 Localizer analysis identified peak coordinates of each
Left amygdala −20 −6 −14 5.77 664 participant (Table 2). For participants whose peak was not
Right cerebellum exterior 6 −44 −16 5.36 5731 identified in any ROI, we used local maxima revealed by
Right superior frontal gyrus 28 44 40 5.08 1384
the whole-brain group-level contrast of the face condition
Right thalamus proper 26 −24 12 4.57 107
Right fusiform gyrus 44 −52 −18 4.52 33 versus the house condition in the left fusiform gyrus, right
Left supramarginal gyrus −60 −56 30 4.49 389 fusiform gyrus, left amygdala, and right amygdala (x = −42,
Left fusiform gyrus −42 −50 −20 4.47 16 y = −50, z = −20 for the left fusiform gyrus; x = 44, y = −52,
Left parietal operculum −32 −32 20 4.46 51 z = −18 for the right fusiform gyrus; x = −20, y = −6, z = −14
for the left amygdala; and x = 24, y = −4, z = −14 for the
Abbreviation: MNI: Montreal Neurological Institute.
right amygdala) (P < 0.05, FWE corrected for multiple com-
reaction to face pictures was significantly delayed com- parisons at voxel level; Fig. 2 and Table 3).
pared to that of house pictures (Table 1). The effect of We calculated the partial correlations between scores in
Group and the interaction of Group × Picture Type were each quadrant of the AASP and beta value for the face
not significant (β = −22.810, 95% CI −62.856 to 17.237, condition in each ROI by controlling for full-scale
P = 0.26, and β = −0.201, 95% CI −22.552 to 22.151, IQ (Table 4). In the ASD group, right fusiform gyrus activ-
P = 0.97, respectively). The effect of Group (β = 0.042, ity was positively correlated with Sensation Avoiding
95% CI −0.033 to 0.116, P = 0.27) and that of Picture scores (r = 0.78, Bonferroni-corrected q = P × 48 = 0.009;
Type (β = −0.016, 95% CI −0.052 to 0.021, P = 0.39) on Fig. 3). Other correlations did not survive Bonferroni cor-
accuracy were not significant. However, we observed a rection in the ASD group. In the TD group, no significant
significant interaction of Group × Picture Type correlations were detected. For the bilateral amygdala, no
(β = −0.069, 95% CI −0.121 to −0.017, P = 0.009). We significant correlation was observed in the ASD group,
conducted post hoc pairwise comparisons using the TD group, or a combination of the two groups.
“pwcompare” command in Stata, and found that the We further tested the differences in correlation
accuracy in the face condition was significantly lower between right fusiform activity and Sensation Avoiding
than that in the house condition in the ASD group (con- scores among groups. We observed that the correlation
trast = −0.085, 95% CI −0.135 to −0.034, Bonferroni- value was significantly higher in the ASD group than in
corrected q < 0.001) but not in the TD group (con- the TD group (z = 2.56, P = 0.01). In addition, we divided
trast = −0.016, 95% CI −0.065 to 0.033, Bonferroni- each group into two subgroups on the basis of cut-off
corrected q = 1). Conversely, group differences were not points for the Sensation Avoiding quadrant (42 for ages
significant for the face condition (contrast = −0.016, 95% below 35 years, and 40 for ages 35 years and above), and
CI −0.065 to 0.033, Bonferroni-corrected q = 1) or the compared right fusiform activity among these subgroups.
Left Right Left Right Left Right Left Right Left Right Left Right
Correlation Low registration 0.03 0.17 0.26 0.52 0.08 0.09 0.17 0.21 0.29 0.30 0.25 0.15
coefficient (r) Sensation seeking 0.18 0.32 0.27 0.48 0.01 0.11 0.16 −0.10 0.10 −0.24 0.19 0.13
Sensory sensitivity 0.06 0.11 0.33 0.55 −0.23 −0.20 0.10 0.06 0.21 0.21 −0.04 −0.05
Sensation avoiding 0.19 0.37 0.56 0.78 0.09 0.11 0.15 0.04 0.29 0.22 0.14 −0.01
Uncorrected Low registration 0.87 0.31 0.31 0.03* 0.75 0.72 0.32 0.21 0.27 0.24 0.31 0.54
P-value Sensation seeking 0.30 0.06 0.29 0.05 0.98 0.67 0.35 0.58 0.70 0.35 0.45 0.60
Sensory sensitivity 0.74 0.51 0.19 0.02* 0.36 0.43 0.55 0.71 0.41 0.41 0.89 0.85
Sensation avoiding 0.26 0.03* 0.02* 0.00** 0.73 0.66 0.38 0.83 0.26 0.40 0.58 0.96
Bonferroni Low registration 1 1 1 1 1 1 1 1 1 1 1 1
corrected Sensation seeking 1 1 1 1 1 1 1 1 1 1 1 1
q-value Sensory sensitivity 1 1 1 1 1 1 1 1 1 1 1 1
Sensation avoiding 1 1 0.97 0.009** 1 1 1 1 1 1 1 1