Key Points
Question
What are the patterns of nonsocial and social cognitive functioning in adults with autism spectrum disorder?
Findings
In this systematic review and meta-analysis of 75 studies comprising 3361 individuals with autism spectrum disorder and 5344 neurotypical adults, those with autism spectrum disorder showed the greatest impairments in theory of mind and emotion perception and processing, followed by processing speed and verbal learning and memory.
Meaning
The severity of impairments across domains of nonsocial and social cognition in adults with autism spectrum disorder identified highlight key intervention targets and suggest significant implications for clinical practice.
Abstract
Importance
Many studies have investigated impairments in cognitive domains in adults with autism spectrum disorder (ASD). Yet, to date, a comprehensive overview on the patterns of cognitive functioning is lacking.
Objective
To provide an overview of nonsocial and social cognitive functioning in various domains in adults with ASD, allowing for comparison of the severity of deficits between different domains.
Data Sources
A literature search performed in an academic medical setting was conducted using PubMed, PsycINFO, Embase, and Medline databases with the combination of the following free-text and Medical Subject Headings where applicable: [cogniti* OR neurocogniti* OR neuropsycholog* OR executive function* OR IQ OR intelligence quotient OR social cognition OR emotion perception OR affect perception OR emotion recognition OR attribution OR ToM OR mentalising OR mentalizing OR prosody OR social knowledge OR mind reading OR social cue OR social judgment] AND [autis* OR ASD OR Asperger OR Asperger’s OR PDD OR pervasive developmental disorder]. The search was further limited to studies published between 1980 (first inclusion of autism diagnosis in the DSM-III) and July 2018.
Study Selection
Studies included were published as a primary peer-reviewed research article in English, included individuals with ASD 16 years or older, and assessed at least 1 domain of neurocognitive functioning or social cognition using standard measures.
Data Extraction and Synthesis
Of 9892 articles identified and screened, 75 met the inclusion criteria for the systematic review and meta-analysis.
Main Outcomes and Measures
Hedges g effect sizes were computed, and random-effects models were used for all analyses. Moderators of between-study variability in effect sizes were assessed using meta-regressions.
Results
The systematic review and meta-analysis included 75 studies, with a combined sample of 3361 individuals with ASD (mean [SD] age, 32.0 [9.3] years; 75.9% male) and 5344 neurotypical adults (mean [SD] age, 32.3 [9.1] years; 70.1% male). Adults with ASD showed large impairments in theory of mind (g = −1.09; 95% CI, −1.25 to −0.92; number of studies = 39) and emotion perception and processing (g = −0.80; 95% CI, −1.04 to −0.55; n = 18), followed by medium impairments in processing speed (g = −0.61; 95% CI, −0.83 to −0.38; n = 21) and verbal learning and memory (g = −0.55; 95% CI, −0.86 to −0.25; n = 12). The least altered cognitive domains were attention and vigilance (g = −0.30; 95% CI, −0.81 to 0.21; n = 5) and working memory (g = −0.23; 95% CI, −0.47 to 0.01; n = 19). Meta-regressions confirmed robustness of the results.
Conclusions and Relevance
Results of this systematic review and meta-analysis suggest that adults with ASD show impairments in social cognitive domains and in specific nonsocial cognitive domains. These findings contribute to the understanding of the patterns of cognitive functioning in adults with ASD and may assist in the identification of targets for cognitive interventions.
This systematic review and meta-analysis provides an overview of nonsocial and social cognitive functioning in various domains in adults with autism spectrum disorder, allowing for comparison of the severity of deficits between different domains.
Introduction
Autism spectrum disorder (ASD) is characterized by persistent deficits in social communication and social interaction, along with restricted, repetitive patterns of behavior, interests, or activities (per the Diagnostic and Statistical Manual of Mental Disorders [Fifth Edition] [DSM-5]).1 In addition to genetic and neurobiological factors, these behavioral patterns are suggested to be primarily underpinned by impairments in nonsocial and social cognition,2,3,4 which are also direct contributors to individuals’ poor adaptive functioning.2 Autism spectrum disorder alters functioning in many domains throughout an individual’s life span (eg, unemployment, social relationships, and quality of life2,5). However, despite similar ASD prevalence rates of 1% among children and adults6 and clear challenges that persist into adulthood, research and treatment efforts have been largely dedicated to children.7 The identification of treatment targets for adults with ASD and development of successful treatment strategies for this population have been recognized as priority areas for research by the Special Interest Group at the International Meeting for Autism Research.8
A critical question that has remained largely unaddressed concerns the identification of cognitive domains that are most severely impaired in adults with an ASD diagnosis. This lack of knowledge is surprising considering the importance of cognitive skills (eg, attention) relative to the early detection and recognition of ASD.9 Existing research has largely focused on impairments in the following 2 key cognitive domains: (1) the inability to attribute mental states, beliefs, intents, and so forth to oneself and others to understand their actions, also referred to as theory of mind,4 and (2) impairments in executive dysfunction (eg, planning, cognitive flexibility, and inhibition).10,11 However, a wider range of cognitive domains appears to be altered, including working memory,12,13 processing speed,14 attention,15 and verbal learning.16
Despite huge efforts of individual studies to increase the understanding of the cognitive deficits in adults with ASD, sample sizes were often small,17,18,19 yielding inconsistent findings.20 Moreover, most studies have focused on a single cognitive domain,16,21,22 and methods of assessment used vary across studies.14,23 Therefore, answering this important clinical question requires a comprehensive overview of the literature. By aggregating all available literature, it is possible to directly compare the relative severity of impairments across various cognitive domains. A greater understanding of the cognitive performance of adults with ASD can inform cognitive theories24 and may provide insight on the progression of ASD symptoms into adulthood. The lack of such information limits treatment development in this area.20
The present systematic review and meta-analysis aimed to systematically map the severity of impairments across domains of nonsocial and social cognitive functioning in adults with ASD compared with the neurotypical adult population. To help explain any variability between studies, potential moderators of impairments observed in these individuals were evaluated. A detailed evaluation and comparison of nonsocial and social cognitive deficits in adults with ASD will advance knowledge about the expression of ASD in later life and may help pinpoint targets for nonsocial and social cognitive intervention.
Methods
Search Strategy
This systematic review and meta-analysis followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) reporting guideline recommendations.25 A literature search performed in an academic medical setting was conducted using PubMed, PsycINFO, Embase, and MEDLINE databases with the combination of the following free-text and Medical Subject Headings where applicable: [cogniti* OR neurocogniti* OR neuropsycholog* OR executive function* OR IQ OR intelligence quotient OR social cognition OR emotion perception OR affect perception OR emotion recognition OR attribution OR ToM OR mentalising OR mentalizing OR prosody OR social knowledge OR mind reading OR social cue OR social judgment] AND [autis* OR ASD OR Asperger OR Asperger’s OR PDD OR pervasive developmental disorder]. The search was further limited to studies published between 1980 (first inclusion of autism diagnosis in the DSM-III) and July 2018, among individuals 16 years or older.
Inclusion Criteria
Studies were included if they fit 5 criteria. First, they had to be published as a primary peer-reviewed research article in English. Second, they had to include individuals with ASD 16 years or older (confirmed diagnosis with either the DSM, International Classification of Diseases [ICD], or another valid diagnostic measure) (complete measures are listed in Table 1 and Table 2). Third, they had to assess at least 1 domain of nonsocial or social cognition using standard measures. Fourth, they had to provide sufficient information to allow for effect size calculations (eg, mean [SD] for the ASD group and the neurotypical control group). Fifth, an age- and IQ-matched neurotypical control group had to be included.
Table 1. Studies Included in the Systematic Review and Meta-analysis, With Details for the ASD Group and the Neurotypical Control Groupa.
Source | Country | ASD Group | Neurotypical Control Group | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
No. | Male, % | Age, Mean (SD), y | Diagnosis Criteria Used | Education, y | Full-scale IQ | Verbal IQ | Performance IQ | No. | Male, % | Age, Mean (SD), y | Education, y | Full-scale IQ | Verbal IQ | Performance IQ | ||
Altgassen et al,26 2012 | Germany | 25 | 80 | 21.8 (6.7) | DSM-IV-TR + ADI-R/ADOSb,c | NA | NA | NA | NA | 25 | 76 | 21.8 (6.1) | NA | NA | NA | NA |
Ambery et al,18 2006 | UK | 27 | 81 | 37.6 (14.6) | ICD-10b,c | NA | NA | 106 | 104 | 20 | 80 | 33.5 (12.0) | NA | NA | 107 | 109 |
Baron-Cohen et al,27 1997 | UK | 16 | 81 | 28.6 (9.7) | DSM-IV-TR | NA | NA | NA | NA | 50 | 50 | 30.0 (9.1) | NA | NA | NA | NA |
Baron-Cohen et al,22 2001 | UK | 15 | 100 | 29.7 (14.5) | Confirmed diagnosis | NA | 115 | NA | NA | 14 | NA | 28.0 (9.0) | NA | 116 | NA | NA |
Baron-Cohen et al,28 2014 | UK | 811 | 44 | 34.7 | Confirmed diagnosis + AQb | NA | NA | NA | NA | 3096 | 34 | 34.4 | NA | NA | NA | NA |
Beacher et al,29 2012 | UK | 29 | 52 | 32.8 (9.1) | DSM-IV-TR + DISCOb | NA | NA | NA | NA | 32 | 50 | 30.4 (7.7) | NA | NA | NA | NA |
Bellebaum et al,30 2014 | Germany | 10 | 10 | 30.9 (5.0) | Confirmed diagnosisb,c | NA | 111 | NA | NA | 12 | 25 | 27.0 (5.7) | NA | 112 | NA | NA |
Blair et al,31 2002 | UK | 12 | 100 | 29.9 (7.3) | DSM-IV | NA | 89 | 88 | 95 | 12 | 75 | 31.5 (13.3) | NA | 81 | 82 | 81 |
Boraston et al,32 2007 | UK | 11 | 82 | 36.7 | Confirmed diagnosis + ADOS | NA | NA | 118 | 117 | 11 | 82 | 33.8 (13.2) | NA | NA | 108 | 114 |
Bramham et al,33 2009 | UK | 45 | 82 | 32.8 (12.5) | ADI-R/ICD-10b,c | NA | 107 | 106 | 106 | 31 | 65 | 32.8 (9.0) | NA | 110 | 108 | 111 |
Brown and Klein,34 2011 | Canada | 16 | 67 | 25.7 (7.9) | Confirmed diagnosis | 14 | NA | NA | NA | 16 | 67 | 26.6 (7.0) | 15 | NA | NA | NA |
Channon et al,35 2011 | UK | 20 | 75 | 38.5 (14.2) | DSM-IVb | 15 | 109 | NA | NA | 18 | 72 | 43.8 (13.7) | 15 | 111 | NA | NA |
Channon et al,36 2014 | UK | 21 | 76 | 40.0 (14.9) | DSM-IV | NA | 108 | NA | NA | 21 | 76 | 43.7 (13.1) | NA | 108 | NA | NA |
Corden et al,37 2008 | UK | 21 | 76 | 33.8 (13.6) | Confirmed diagnosis + ADOSb | NA | 118 | 116 | 116 | 21 | 76 | 32.1 (11.6) | NA | 117 | 115 | 115 |
Crane et al,38 2013 | UK | 28 | 50 | 41.6 (16.5) | DSM-IV/ICD-10 + AQ | NA | 117 | 115 | 115 | 28 | 50 | 40.5 (17.2) | NA | 115 | 111 | 117 |
David et al,39 2008 | Germany | 24 | 58 | 32.3 (10.0) | Confirmed diagnosis + AQ | 15 | NA | NA | NA | 24 | 54 | 30.6 (5.1) | 18 | NA | NA | NA |
Davids et al,40 2016 | Netherlands | 36 | 83 | 58.6 (7.8) | DSM-IV/DSM-5 + ADOS | NA | 106 | NA | NA | 36 | NA | 59.4 (8.3) | NA | 107 | NA | NA |
Dziobek et al,41 2006 | Germany | 21 | 90 | 41.6 | DSM-IV + ADI/Rb | 17 | 122 | NA | NA | 20 | 90 | 39.9 (12.6) | 17 | 124 | NA | NA |
Dziobek et al,42 2006 | US | 17 | 82 | 41.4 | DSM-IV + ADI-Rb | 17 | 113 | NA | NA | 17 | 88 | 40.2 | 16 | 115 | NA | NA |
Dziobek et al,43 2008 | US | 17 | 76 | 42.4 | DSM-IV + ADI/Rb | 16 | 110 | NA | NA | 18 | 78 | 48.6 | 16 | 112 | NA | NA |
Eack et al,14 2013 | US | 43 | 67 | 24.9 (5.5) | Confirmed diagnosis + ADOS/ADI/Rc | NA | 107 | NA | NA | 24 | 67 | 26.2 (5.5) | NA | 113 | NA | NA |
Eack et al,44 2015 | US | 45 | 89 | 24.6 (5.7) | ADOSc | NA | 113 | NA | NA | 30 | 73 | 26.4 (5.8) | NA | 105 | NA | NA |
Faja et al,45 2009 | US | 39 | 61 | 24.0 (7.4) | ADI-R/ADOS/DSM-IV | NA | 110 | 110 | 109 | 33 | 67 | 24.6 (7.1) | NA | 111 | 107 | 110 |
Geurts and Vissers,19 2012 | Netherlands | 23 | 78 | 63.6 (7.5) | Confirmed diagnosis + AQ | NA | NA | 109 | NA | 23 | 78 | 63.7 (8.1) | NA | NA | 110 | NA |
Globerson et al,46 2015 | Israel | 23 | 100 | 26.2 (3.5) | Confirmed diagnosis + ADOS | NA | NA | NA | NA | 32 | 100 | 26.2 (3.5) | NA | NA | NA | NA |
Golan et al,47 2006 | UK | 22 | 77 | 30.9 (11.2) | Confirmed diagnosis | NA | NA | 110 | 115 | 24 | 79 | 25.3 (9.1) | NA | NA | 116 | 112 |
Golan et al,23 2007 | UK | 50 | 80 | 27.5 (8.5) | DSM-IV | NA | 114 | 112 | 112 | 22 | 77 | 24.3 (7.7) | NA | 114 | 114 | 111 |
Gonzalez-Gadea et al,48 2013 | Argentina | 23 | 65 | 33.3 (9.8) | DSM-IV + AQb,c | 15 | NA | NA | NA | 21 | 52 | 38.3 | 16 | NA | NA | NA |
Haigh et al,49 2018 | US | 76 | 85 | 24.2 (6.4) | Confirmed diagnosis + ADOS/ADI-Rb | NA | 109 | NA | NA | 64 | 77 | 25.7 (4.9) | NA | 106 | NA | NA |
Hill and Bird,50 2006 | UK | 22 | 73 | 31.1 (13.1) | DSM-IV | NA | 110 | NA | NA | 22 | 64 | 33.4 (14.5) | NA | 108 | NA | NA |
Holdnack et al,13 2011 | US | 43 | 80 | 22.1 | DSM-IV-TR | NA | 86 | NA | NA | 43 | 81 | 22.6 (7.1) | NA | 102 | NA | NA |
Johnston et al,51 2011 | UK | 24 | 79 | 27.8 (8.7) | ICD-10 + ADI-R/ADOSb | NA | 103 | NA | NA | 14 | 71 | 28.7 (11.1) | NA | 108 | NA | NA |
Jolliffe and Baron-Cohen,52 1999 | UK | 34 | 88 | 26.7 | Confirmed diagnosisb | NA | NA | NA | NA | 17 | 88 | 30.0 (9.1) | NA | NA | NA | NA |
Joshi et al,53 2014 | US | 26 | 77 | 27.5 (6.2) | DSM-IV | NA | 109 | NA | NA | 52 | 77 | 27.5 (4.1) | NA | 113 | NA | NA |
Kéri,54 2014 | Hungary | 18 | 78 | 28.5 (12.0) | ADI-R | 12 | 113 | NA | NA | 20 | 65 | 29.1 (10.4) | 12 | 110 | NA | NA |
Kiep and Spek,55 2017 | Netherlands | 139 | 71 | 36.5 | DSM-IV-TR + ADI-R | NA | 109 | 108 | NA | 60 | 58 | 37.6 | NA | 110 | 110 | NA |
Koolen et al,15 2014 | Netherlands | 15 | 93 | 37.5 (13.1) | DSM-IV + ADOSb | NA | 126 | 100 | NA | 15 | 93 | 28.0 (13.6) | NA | 117 | 101 | NA |
Kuschner et al,56 2009 | US | 14 | 100 | 24.1 (8.7) | ADI + ADOS | NA | 96 | 100 | 106 | 23 | 100 | 22.9 (7.4) | NA | 99 | 99 | 100 |
Lahera et al,57 2014 | Spain | 22 | 86 | 21.9 (6.7) | DSM-IV-TR + ADI-Rb | NA | NA | NA | NA | 26 | 65 | 22.9 (4.8) | NA | NA | NA | NA |
Lai et al,58 2012 | UK | 64 | 50 | 27.5 | DSM-IV/ICD-10 + ADI-Rb,c | NA | 114 | 113 | 111 | 64 | 50 | 28.1 | NA | 118 | 115 | 117 |
Lever and Geurts,59 2016 | Netherlands | 118 | 70 | 47.6 (14.9) | DSM-IV + ADOSc | NA | 115 | NA | NA | 118 | 70 | 47.7 (15.4) | NA | 114 | NA | NA |
Lopez et al,60 2005 | US | 17 | 82 | 29.0 (8.0) | Confirmed diagnosis + ADI-R/ADOS/GARS | NA | 77 | 73 | 84 | 17 | 82 | 29.4 (11.4) | NA | 89 | 92 | 88 |
Lugnegård et al,61 2013 | Sweden | 53 | 49 | 27.3 (4.1) | DSM + DISCO 11 | NA | NA | NA | NA | 50 | 38 | 28.8 (9.3) | NA | NA | NA | NA |
Martin and McDonald,62 2004 | Australia | 14 | 93 | 19.6 (1.7) | DSM-IVb,c | NA | NA | NA | NA | 24 | 42 | 19.7 (3.4) | NA | NA | NA | NA |
Mathersul et al,63 2013 | Australia | 40 | 77 | 37.2 (16.2) | DSM-IV-TR + ADI-R/ADOSb | 15 | 114 | NA | NA | 33 | 73 | 41.7 (17.2) | 16 | 114 | NA | NA |
Mathewson et al,64 2011 | Canada | 15 | 80 | 35.5 (2.7) | DSM-IV/ADI-R/ADOSb | NA | 101 | NA | NA | 16 | 75 | 35.7 (10.6) | NA | 107 | NA | NA |
Mayer and Heaton,65 2014 | UK | 19 | 79 | 40.4 (11.3) | Confirmed diagnosis + ADOS | NA | 113 | 111 | 113 | 19 | 79 | 38.3 (9.0) | NA | 119 | 118 | 118 |
Murray et al,66 2017 | UK | 20 | 100 | 30.6 (6.5) | ICD-10 + AQb,c | NA | NA | 105 | NA | 20 | 95 | 30.6 (6.3) | NA | NA | 111 | NA |
Nakahachi et al,67 2006 | Japan | 16 | 75 | 28.0 | DSM-IV | NA | 101 | 107 | 91 | 28 | 75 | 28.3 | NA | 103 | NA | NA |
Otsuka et al,68 2017 | Japan | 62 | 60 | 26.5 | DSM-IV-TR | 15 | 111 | 113 | 105 | 21 | 67 | 24.9 (6.3) | 15 | 113 | 113 | 111 |
Parsons and Carlew,69 2016 | US | 8 | 75 | 22.9 (5.3) | ADOSb | NA | NA | 102 | NA | 10 | NA | 18.8 (0.8) | NA | NA | 100 | NA |
Philip et al,70 2010 | UK | 23 | 69 | 32.5 (10.9) | DSM-IV + ADOS/AQ | NA | 101 | 98 | 104 | 23 | 74 | 32.4 (11.1) | NA | 111 | 107 | 113 |
Ponnet et al,71 2004 | Belgium | 19 | 74 | 21.1 (4.8) | ICD-10b | NA | 106 | 108 | 104 | 19 | 74 | 21.9 (6.6) | NA | 114 | 116 | 110 |
Schneider et al,72 2013 | Australia | 24 | 71 | 27.7 (7.7) | Confirmed diagnosis + ADOS-G/RAADS-R | 14 | 113 | 111 | 111 | 20 | 80 | 31.4 (6.7) | 13 | 114 | 111 | 114 |
Schneider et al,73 2013 | Germany | 30 | 57 | 32.7 (9.9) | DSM-IV + AQ/ADOS-Gb | 13 | NA | NA | NA | 28 | 53 | 34.3 (9.7) | 13 | NA | NA | NA |
Schneider et al,74 2015 | Germany | 24 | 58 | 36.1 (9.6) | ICD-10 + ADOS-G | NA | 111 | 111 | 109 | 24 | 54 | 34.2 (8.8) | NA | 107 | 107 | 106 |
Schuwerk et al,75 2015 | Germany | 18 | 67 | 24.1 (7.0) | ICD-10 | NA | NA | 104 | 91 | 19 | 68 | 25.3 (3.8) | NA | NA | 103 | 98 |
Senju et al,76 2009 | UK | 19 | 85 | 36.8 (14.3) | NA | 115 | 116 | 109 | 17 | NA | 39.6 (11.7) | NA | 115 | 116 | 111 | |
Shamay-Tsoory,77 2008 | Israel | 18 | 94 | 21.9 (6.3) | ICD-10 + ADI-Rb,c | 12 | NA | NA | NA | 21 | 71 | 23.4 (6.2) | 13 | NA | NA | NA |
Spek et al,78 2010 | Netherlands | 61 | 85 | 42.3 | ADI-R + DSM-IV-TRb | NA | 112 | NA | NA | 32 | 75 | 43.7 (10.5) | NA | 106 | NA | NA |
Spek et al,79 2011 | Netherlands | 82 | 86 | 39.2 | Confirmed diagnosis + ADI-Rb | NA | 110 | 110 | NA | 41 | 73 | 39.3 (9.7) | NA | 114 | 112 | NA |
Stewart et al,80 2013 | UK | 11 | 64 | 27.2 (7.5) | DSM-IV | NA | NA | NA | NA | 14 | 57 | 26.4 (5.6) | NA | NA | NA | NA |
Sucksmith et al,81 2013 | UK | 329 | 49 | 35.5 (11.0) | DSM-IV/ICD-10b | NA | NA | NA | NA | 187 | 50 | 34.3 (10.7) | NA | NA | NA | NA |
Sumiyoshi et al,82 2011 | Japan | 22 | 86 | 26.5 (7.4) | DSM-IV | NA | 94 | NA | NA | 15 | 73 | 29.7 (6.4) | NA | 100 | NA | NA |
Tobe et al,83 2016 | US | 19 | 89 | 39.4 (12.5) | DSM-IV + ADOS | NA | NA | NA | NA | 73 | 62 | 36.0 (11.8) | NA | NA | NA | NA |
Torralva et al,12 2013 | Argentina | 25 | 72 | 33.9 (11.1) | DSM-IV + CAST/AQ | 15 | NA | NA | NA | 36 | 60 | 36.4 (9.9) | 16 | NA | NA | NA |
Wallace et al,16 2008 | UK | 28 | 89 | 32.0 (9.0) | ICD-10 + ADI-R | NA | NA | NA | 101 | 28 | 89 | 31.0 (9.0) | NA | NA | NA | 98 |
Wallace et al,84 2010 | UK | 26 | 88 | 32.0 (9.0) | DSM-IV | NA | NA | NA | 101 | 26 | 88 | 31.0 (9.0) | NA | NA | NA | 98 |
Walsh et al,85 2016 | Canada | 23 | 78 | 30.8 (8.5) | Confirmed diagnosis + ADOS-G | NA | 97 | 97 | 98 | 23 | 78 | 28.4 (9.3) | NA | 97 | 94 | 98 |
White et al,86 2006 | UK | 16 | 62 | 32.3 (14.2) | Confirmed diagnosis + AQ | NA | 115 | 113 | 108 | 24 | 50 | 37.7 (12.4) | NA | 112 | 117 | 111 |
White et al,87 2011 | UK | 16 | 75 | 33.0 (10.3) | Confirmed diagnosis + ADOS-G | NA | NA | 111 | 106 | 15 | 73 | 36.5 (9.9) | NA | NA | 114 | 110 |
Williams et al,21 2005 | US | 31 | 93 | 26.6 (8.7) | ADOS/ADI-Rb | NA | 109 | 111 | 103 | 25 | 84 | 26.8 (9.1) | NA | 110 | 108 | 110 |
Williams et al,88 2014 | UK | 17 | 82 | 31.1 (9.6) | DSM-IV-TR + ADOSb,c | NA | 114 | 111 | 113 | 17 | 82 | 31.9 (14.2) | NA | 118 | 115 | 117 |
Williams et al,89 2018 | UK | 22 | 82 | 35.8 (11.5) | ICD-10 + ADOS | NA | 101 | 102 | 101 | 21 | 76 | 36.3 (12.0) | NA | 107 | 107 | 106 |
Wilson et al,90 2014 | UK | 89 | 100 | 26.0 (7.0) | ICD-10 + ADI-Rb | NA | 110 | 110 | 108 | 89 | 100 | 28.0 (6.0) | NA | 114 | 109 | 116 |
Zwickel et al,91 2011 | UK | 19 | NA | 37.0 | Confirmed diagnosis + ADOS-G | NA | NA | 115 | NA | 18 | NA | 39.0 | NA | NA | 115 | NA |
Abbreviations: ADI-R, Autism Diagnostic Instrument Revised; ADOS, Autism Diagnostic Observation Schedule; ADOS-G, Autism Diagnostic Observation Schedule–Generic; AQ, Autism Spectrum Quotient Questionnaire; ASD, autism spectrum disorder; CAST, Childhood Asperger Syndrome Test; DISCO, Diagnostic Interview for Social and Communication Disorders; GARS, Gilliam Autism Rating Scale; ICD-10, International Statistical Classification of Diseases, 10th Revision; NA, not available; RAADS-R, Ritvo Autism and Asperger Diagnostic Scale–Revised; UK, United Kingdom; US, United States.
In addition to the 75 included studies, a study by Zwickel91 reporting outcomes only on social perception and knowledge is also listed but was excluded from the present meta-analysis.
Other psychiatric disorder and/or neurological disorder (not including epilepsy or intellectual disability because this was part of the inclusion criteria) was an exclusion criterion for the ASD group.
Substance use/abuse was an exclusion criterion for the ASD group.
Table 2. Studies Included in the Systematic Review and Meta-analysis, Summarizing the Domains of Nonsocial Cognition and Social Cognition in Adults With Autism Spectrum Disorder.
Source | Nonsocial Cognition | Social Cognition | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Reasoning and Problem Solving | Processing Speed | Attention and Vigilance | Working Memory | Visual Learning and Memory | Verbal Learning and Memory | Verbal Comprehension | Verbal Fluency | Overall Neurocognition | Theory of Mind | Emotion Perception and Processing | Social Perception and Knowledge | |
Altgassen et al,26 2012 | X | X | X | X | ||||||||
Ambery et al,18 2006 | X | X | X | X | X | |||||||
Baron-Cohen et al,27 1997 | X | |||||||||||
Baron-Cohen et al,22 2001 | X | |||||||||||
Baron-Cohen et al,28 2014 | X | |||||||||||
Beacher et al,29 2012 | X | |||||||||||
Bellebaum et al,30 2014 | X | |||||||||||
Blair et al,31 2002 | X | X | X | |||||||||
Boraston et al,32 2007 | X | |||||||||||
Bramham et al,33 2009 | X | X | X | X | X | |||||||
Brown and Klein,34 2011 | X | X | ||||||||||
Channon et al,35 2011 | X | X | ||||||||||
Channon et al,36 2014 | X | X | ||||||||||
Corden et al,37 2008 | X | |||||||||||
Crane et al,38 2013 | X | X | ||||||||||
David et al,39 2008 | X | X | X | X | X | |||||||
Davids et al,40 2016 | X | X | X | |||||||||
Dziobek et al,41 2006 | X | X | X | |||||||||
Dziobek et al,42 2006 | X | X | ||||||||||
Dziobek et al,43 2008 | X | |||||||||||
Eack et al,14 2013 | X | X | X | X | X | X | X | X | ||||
Eack et al,44 2015 | X | |||||||||||
Faja et al,45 2009 | X | |||||||||||
Geurts and Vissers,19 2012 | X | X | X | X | X | X | X | |||||
Globerson et al,46 2015 | X | |||||||||||
Golan et al,47 2006 | X | |||||||||||
Golan et al,23 2007 | X | |||||||||||
Gonzalez-Gadea et al,48 2013 | X | X | X | X | ||||||||
Haigh et al,49 2018 | X | X | ||||||||||
Hill and Bird,50 2006 | X | X | X | X | ||||||||
Holdnack et al,13 2011 | X | X | X | X | X | |||||||
Johnston et al,51 2011 | X | X | ||||||||||
Jolliffe and Baron-Cohen,52 1999 | X | |||||||||||
Joshi et al,53 2014 | X | X | X | X | ||||||||
Kéri,54 2014 | X | X | ||||||||||
Kiep and Spek,55 2017 | X | X | X | |||||||||
Koolen et al,15 2014 | X | X | X | X | X | X | ||||||
Kuschner et al,56 2009 | X | |||||||||||
Lahera et al,57 2014 | X | X | ||||||||||
Lai et al,58 2012 | X | X | ||||||||||
Lever and Geurts,59 2016 | X | X | X | X | ||||||||
Lopez et al,60 2005 | X | X | X | |||||||||
Lugnegård et al,61 2013 | X | X | ||||||||||
Martin and McDonald,62 2004 | X | |||||||||||
Mathersul et al,63 2013 | X | |||||||||||
Mathewson et al,64 2011 | X | X | ||||||||||
Mayer and Heaton,65 2014 | X | |||||||||||
Murray et al,66 2017 | X | X | ||||||||||
Nakahachi et al,67 2006 | X | X | ||||||||||
Otsuka et al,68 2017 | X | X | X | X | X | X | ||||||
Parsons and Carlew,69 2016 | X | |||||||||||
Philip et al,70 2010 | X | X | ||||||||||
Ponnet et al,71 2004 | X | |||||||||||
Schneider et al,72 2013 | X | |||||||||||
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Exclusion Criteria
After initial screening of the abstracts, studies were excluded for 3 reasons. First, studies were excluded if the sample included a nonclinical population (eg, with autistic-like traits). Second, studies were excluded if participants were initially seen with comorbidity of any neurological conditions altering cognition (eg, epilepsy). Third, studies were excluded if no data on any of the specified cognitive domains were available (if only total IQ was reported, the study was excluded).
Screening Process
In total, 9892 potentially eligible articles were identified (Figure 1). After the first screening of titles (stage 1), 7488 articles were reviewed by their abstracts (stage 2). Stage 2 yielded 1268 articles for full-text reviews (stage 3). Thirty percent of the stage 1 yield were double screened by 2 of us (T.V. and A.K.F./E.V.), with Cohen κ interrater reliability values of 0.95 and 0.98, respectively, which represents an excellent strength of agreement.92 Consensus decisions were made on the inclusion of any inconsistently screened articles (included by one reviewer and excluded by the other). Five articles did not report the mean scores on the measures of interest and/or reported the means in figures only (for which the exact numbers could not be extracted). Missing data could not be obtained after contacting the authors. The resulting 76 studies that met all the inclusion criteria are listed in Table 1 and Table 2. All included domains with associated measures and parameters (ie, the measure outcomes) are listed in Table 3.
Figure 1. PRISMA Flow Diagram.
PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) flow chart of the systematic review process.
Table 3. Nonsocial and Social Cognitive Domains and Parameters.
Test | Parameters |
---|---|
Reasoning and Problem Solving | |
Tower of Hanoi Tower of London Tower of California (D-KEFS) |
No. of steps/movements to complete the task Total to complete |
Block design (WAIS-III/WAIS-R) Matrix reasoning (WASI) Picture completion (WAIS-III) Letters and Numbers |
No. of correctly completed designs No. of correct responses |
WCST | WCST categories No. of preservative errors |
Zoo map subtest (BADS) | Time to complete Accuracy score |
Six elements (BADS) | No. of rule breaks |
Action program score (BADS) | No. of stages completed |
Temporal judgment task (BADS) | No. of correct responses |
Key search total (BADS) | Search strategy |
Hayling Test | Time to complete |
Problem-solving subtest (MCCB) | NA |
Modified Card Sorting Test | No. of categories No. of preservative errors |
California design fluency test (D-KEFS) | Filled dots (No. of perseverations) |
Embedded Figures Test | Accuracy No. correct Time to complete |
Go/No Go Test (attention/inhibition for executive function) | Errors of omission (as percentage of trials) Errors of commission (as percentage of trials) |
Trail-making test (number-letter switching) (DKEFS) | Number-letter switching |
Color inhibition/switching subtest (DKEFS) | NA |
Behavior Rating Inventory of Executive Functioning–Adults | Global score |
Processing Speed | |
Stroop Color–Word Reading Test | Total No. of words |
Stroop Color–Word Interference Test | No. of errors made Time to complete |
California Stroop test (D-KEFS) | NA |
Processing speed subtest (MCCB) | NA |
Trail-Making A or Trail-Making B | Time to complete |
Processing Speed Index | NA |
Attention and Vigilance | |
Attention/vigilance subtest (MCCB) | NA |
Sustained Attention to Response Task | Mean reaction time for correct responses No. of commission errors (incorrectly pressing the response key) No. of omission errors (not pressing key when a response is required) |
Stroop (selective attention) | Standardized interference score |
Color-word interference test (from DKEFS battery) | Interference control error score |
Trail-Making A and Trail-Making B | Trail-Making A minus Trail Making B (the difference between the response time) |
Go/no go subtest of the Test for Attentional Performance | NA |
Continuous Performance Task | NA |
Working Memory | |
Digit Ordering Test | No. of correctly repeated digit series |
Letter-number sequencing subtest of the Wechsler Memory Scale–Third Edition | No. of correct strings recalled |
Arithmetic WAIS-III | NA |
Digit span (WAIS-R) | Total No. of recalls |
Backward Digit Span | Total No. of recalls |
N-Back Letter Task | Response time |
Working Memory Test Battery | Average No. of recalls |
Working Memory Index | NA |
Visual Learning and Memory | |
Doors and People Test of Verbal and Visual Recall and Recognition | NA |
British Picture Vocabulary Scale–Revised | Total No. of correct responses |
People Test of Recall and Recognition | No. of correct recalls |
Visual learning subtest (MCCB) | |
Recognition Memory Test for Faces | No. of items correct |
Recognition of faces on the Wechsler Memory Scales immediate and delayed facial memory tasks | No. of faces recognized (immediately/delayed) |
Woodcock Johnson revised picture recognition subtest | No. of correct identifications |
Rey Osterreith Complex | Total No. of correct elements |
Benton Facial Recognition Test | No. of correct recalls |
Verbal Learning and Memory | |
Doors and People Test of Verbal and Visual Recall and Recognition | NA |
Recognition Memory Test for Words (verbal memory) | No. of correct responses |
Verbal learning subtest (MCCB) | NA |
Rey Auditory Verbal Learning Test and variations (eg, Dutch) | Direct recall total Delayed total No. of correct words |
Verbal Comprehension | |
Vocabulary test (German version of the WASI) | No. of correct words |
Comprehension (WAIS-III) | NA |
Vocabulary (WAIS-III/WAIS-R/WASI) | No. of correct words |
Information (WAIS-III/WAIS-R/WASI) | NA |
Verbal Fluency | |
California Verbal Fluency Test | Words from certain category or words beginning with a certain letter |
COWAT | Words from certain category or words beginning with a certain letter |
Verbal Fluency Test | No. of words generated |
Semantic verbal fluency test and phonetic verbal fluency test (short versions of the Dutch version of COWAT) | Total words produced Words from certain category or words beginning with a certain letter |
COWAT | Total No. of responses |
Category Fluency | NA |
Regensburger Word Fluency Test | NA |
Japanese Verbal Learning Task | NA |
Overall Neurocognition | |
BADS | Total score |
Theory of Mind | |
Emotion Quotient | Total score on scale |
Eyes Task | No. of correctly chosen emotions fitting eye expression |
Reading the Mind in the Eyes Test | No. of correctly chosen emotions fitting eye expression No. of mental state and gender attributions correctly identified |
Strange Stories Task | Total score |
Happe Theory of Mind Stories | NA |
Frith-Happe Animations Triangles (theory of mind task) | NA |
Multifaceted Empathy Test | Total score on empathy questionnaire |
Interpersonal Reactivity Index | Total score on empathy questionnaire |
Movie for the Assessment of Social Cognition | No. of correctly identified feelings/intentions |
Mayer-Salovey-Caruso Emotional Intelligence Test | Total score |
Cambridge Mind Reading face battery | NA |
Cambridge Mind Reading voice battery | NA |
Faux Pas | Faux pas score |
Social Attribution Task | No. of correctly attributed social meanings |
Mentalistic Interpretation | Quality of mental states interpretation/selection of best alternatives |
Emotion Perception and Processing | |
Ekman and Friesen Test of Facial Affect Recognition | No. of correctly identified emotions |
Basic Emotion Recognition Task | NA |
Penn Emotion Recognition Test | No. of correctly identified emotions Time |
Vocal Emotion Recognition Task (prosody task 1) | Percentage correct |
Emotion hexagon task from the FEEST | Percentage correct |
Social Perception Score | Total score |
Japanese and Caucasian Facial Expressions of Emotion Series | NA |
Facial Emotion Recognition | NA |
Voice Emotion Label Task | NA |
Basic Expression Recognition Task | NA |
Karolinska Directed Emotional Faces Task | NA |
Social Perception and Knowledge | |
Social Problem Resolution | Quality of best solutions provided |
Social Problem Fluency | Selection of best alternatives |
Firth-Happe Animations | Correctly identified social scenarios |
Abbreviations: BADS, Behavioral Assessment of Dysexecutive Syndrome; COWAT, Controlled Oral Word Association Test; D-KEFS, Delis-Kaplin Executive Function Scale; FEEST, Facial Expressions of Emotion: Stimuli and Tests; MCCB, MATRICS Consensus Cognitive Battery; NA, not applicable; WAIS-III, Wechsler Adult Intelligence Scale–Third Edition; WAIS-R, Wechsler Adult Intelligence Scale–Revised; WASI, Wechsler Abbreviated Scale of Intelligence; WCST, Wisconsin Card Sorting Test.
Cognitive Domains
The following key domains of nonsocial cognition were included: (1) reasoning and problem solving, (2) processing speed, (3) attention and vigilance, (4) working memory, (5) visual learning and memory, (6) verbal learning and memory, (7) verbal comprehension, and (8) verbal fluency. Social cognition was categorized into the following 3 domains: (1) theory of mind, (2) emotion perception and processing, and (3) social perception and knowledge. The overview of domains followed the Measurement and Treatment Research to Improve Cognition in Schizophrenia (MATRICS) consensus,93 which aimed for more standardized cognitive research in schizophrenia but has previously been adopted for the ASD population.14
Statistical Analysis
Ten meta-analyses were carried out, including domains of nonsocial and social cognition for which at least 3 independent studies were found. The social perception and knowledge domain was reported by only 2 studies and hence was omitted from further analysis. Because one of the included studies only reported outcomes on this domain, the present meta-analysis consisted of 75 studies.
When studies did not provide a total mean score on a particular measure but reported subscores (eg, individual emotions presented separately), data were pooled into an overall mean score. Similarly, when studies reported the mean scores per subgroup (eg, by sex or by diagnosis [Asperger syndrome and high-functioning autism]), data were pooled into an overall mean score. In cases where higher mean scores on cognitive measures corresponded to worse (and not better) performance, effect sizes were reversed. If a study provided more than 1 outcome within the same cognitive domain, the measures were aggregated by computing the mean effect size (and standard error) based on the assumption that the correlation is in the region of 1 between the measures.94 In case of overlapping samples from 2 or more articles reporting outcomes for the same domain, only the largest sample was considered. Meta-analyses were completed using a random-effects model (DerSimonian-Laird estimate), which assumes a distribution of true effect sizes and aims to evaluate the mean of this distribution. When assigning weights to estimate the effect size, the within-studies and between-studies sampling errors are considered.95 All analyses were carried out using statistical software (Stata/MP 15.0; StataCorp LP96).
For each of these individual meta-analyses, we reported the number of studies, total sample size for the ASD group and the neurotypical control group, the mean effect size (Hedges g) with 95% CI, P value, and the results from the Cochran Q test for heterogeneity (Figure 2). The magnitude of Hedges g may be interpreted using Cohen d97 effect sizes convention, described as 0.20 for small, 0.50 for medium, and 0.80 for large. The Cochran Q test acquired for each of the domains represents the weighted sum of squared differences between individual study effects and the pooled effect across studies. The I2 statistic refers to the percentage of variability in point estimates that is due to between-study heterogeneity rather than sampling error.98 A value of 0 suggests the absence of heterogeneity, in which case the random-effects model is simplified to a fixed-effects model. To assess risk of publication bias, the funnel plots for each cognitive domain were examined for asymmetry and then formally evaluated with Egger test. If publication bias was found, the trim-and-fill method was applied,99 providing effect sizes adjusted for publication bias.
Figure 2. Domains of Nonsocial Cognition and Social Cognition in Adults in the Autism Spectrum Disorder (ASD) Group Compared With the Neurotypical Control Group.
Hedges g (mean effect size and 95% CI) provided across all domains. Negative values indicate worse performance in the ASD group compared with the neurotypical control group.
Moderator Analysis
The moderators selected include variables that might alter the observed association between impairments in nonsocial or social cognition and ASD. The sample selection and its characteristics (ie, age, sex, and IQ) can moderate the cognitive performance due to differential developmental trajectories observed for ASD100 and neurotypical individuals.101 Similarly, the assessment methods (eg, what is the response mode required) can have an effect on the cognitive performance.100 Because these variables vary between studies, the findings are difficult to interpret without the inclusion of these moderators in the meta-regression model.
Eight moderators were considered. First was the mean age, previously shown to be associated with the cognitive performance in adults with ASD.102 Second was sex, building on reports on sex-related cognitive profiles.103 Third, diagnostic classification was included due to potential sampling bias and was categorized as diagnosis made using the DSM/ICD, Autism Diagnostic Observation Schedule (ADOS)/Autism Diagnostic Interview Revised (ADI-R)/Autism Spectrum Quotient Questionnaire (AQ)/Diagnostic Interview for Social and Communication Disorders (DISCO), or DSM/ICD plus ADOS/ADI-R/AQ/DISCO.104,105 Fourth was the mean number of years of education.106 Fifth, IQ differences were explored with the following 2 different approaches: (1) we created a variable that indicated whether a significant IQ difference was observed between the study groups (yes or no) and (2) we examined the mean IQ of a study sample because evidence suggests that intelligence may act as a moderator of cognitive presentation.107,108 Sixth was assessment tool format (computer vs traditional administration) and the response mode (verbal vs motor), previously shown to have significant effect on the measure outcomes.100 Seventh was country. Eighth was year of publication.
All moderators were included in the meta-regression model if information was available for a sufficient number of studies (≥4). We also aimed to include the ADOS total score; however, we could not do so due to a lack of data. Considering the number of statistical tests in meta-regressions, a conservative statistical significance (2-sided P < .01) was adopted.
Results
Retrieved Studies
In total, 9892 potentially eligible articles were identified. Most of the 75 included studies were conducted in Europe (50 [66.7%]), followed by studies from the United States and Canada (16 [21.3%]). The sample sizes varied greatly, ranging from 18 participants69 to 3907 participants (including neurotypical adults),28 with 66 studies (88.0%) using samples between 20 and 100 participants. The overall database included a combined sample of 3361 individuals with ASD (mean [SD] age of samples across studies, 32.0 [9.3] years; range, 19.6-63.6 years; 75.9% male) and 5344 neurotypical adults (mean [SD] age of samples across studies, 32.3 [9.1] years; range, 18.8-63.7 years; 70.1% male). The combined mean (SD) IQ across studies was 108.2 (9.1) for the ASD group and 109.8 (7.7) for neurotypical adults.
Nonsocial Cognition
The meta-analyses showed consistent impairments in individuals with ASD across all nonsocial cognitive domains compared with neurotypical controls (Figure 2). The largest impairments were observed for processing speed (g = −0.61; 95% CI, −0.83 to −0.38; n = 21; P < .001), followed by verbal learning and memory (g = −0.55; 95% CI, −0.86 to −0.25; n = 12; P < .001) and reasoning and problem solving (g = −0.51; 95% CI, −0.74 to −0.28; n = 22; P < .001). The least altered domains were attention and vigilance (g = −0.30; 95% CI, −0.81 to 0.21; n = 5; P = .09) and working memory (g = −0.23; 95% CI, −0.47 to 0.01; n = 19; P = .06). There was no heterogeneity across studies on processing speed (Q = 13.42, P = .86) or reasoning and problem solving (Q = 8.83, P = .99), but there was significant variation in studies for verbal learning and memory (Q = 34.76, P < .001). The review of the funnel plots identified outliers on domains of processing speed (1 outlier), working memory (3 outliers), visual learning and memory (2 outliers), and verbal learning and memory (2 outliers). After the removal of these outliers, the magnitude of the effect sizes remained similar (the eAppendix in the Supplement contains the results after the removal of outliers). The only significant Egger test result was found for visual learning and memory. A trim-and-fill analysis did not result in imputation of any studies, and the effect size remained the same.
Social Cognition
The greatest impairments in the ASD group compared with the neurotypical control group were found in theory of mind (g = −1.09; 95% CI, −1.25 to −0.92; number of studies = 39; P < .001) and emotion perception and processing (g = −0.80; 95% CI, −1.04 to −0.55; n = 18; P < .001) (Figure 2). The removal of 4 outliers identified by funnel plot inspection for theory of mind and the removal of 1 outlier for emotion perception and processing did not change the magnitude of the effect sizes. Egger test results were found to be significant for both domains, indicating the existence of reporting bias. However, trim-and-fill analyses did not change any of the results.
Moderators
Meta-regressions showed that included moderators did not account for the heterogeneity between studies. Heterogeneity was not altered by the mean age (β range = −0.01 to 0.13, P range = .06 to .97), sex (β range = −0.01 to 0.35, P range = .06 to .88), diagnostic classification (β range = −0.41 to 0.45, P range = .08 to .84), IQ differences (β range = −0.01 to 1.65, P range = .19 to .99), the mean IQ of the study sample (β range = −0.08 to 0.21, P range = .09 to .99), assessment tool format (β range = −1.32 to 0.20, P range = .02 to .87), the response mode (β range = 0.07 to 1.63, P range = .03 to .95), country (β range = −0.20 to 1.10, P range = .23 to .86), or year of publication (β range = −1.23 to 0.61, P range = .12 to .94).
Discussion
To our knowledge, this the first systematic review and meta-analysis that has investigated the patterns of nonsocial and social cognitive functioning in adults with ASD, allowing for comparison of relative cognitive strengths and weaknesses in the adult ASD population. The meta-analyses included 75 studies, with combined samples of 3361 individuals with ASD and 5344 neurotypical adults. Relative to neurotypical adults, the ASD group showed impairments across all domains of nonsocial and social cognitive functioning, with the largest deficits in social cognition (theory of mind g = −1.09 and emotion perception and processing g = −0.80) (Figure 2). Among domains of nonsocial cognition, the largest magnitude of impairment was found for processing speed (g = −0.61), followed by verbal learning and memory (g = −0.55) and reasoning and problem solving (g = −0.51). The review highlighted working memory (g = −0.23) and attention and vigilance (g = −0.30) as the least altered cognitive domains in adults with ASD. The moderators considered in the present analysis (mean age, sex, IQ, and country, among others) did not change the magnitude of the effect sizes observed.
The present findings help improve our understanding of the patterns of cognitive impairments in adults with ASD. While our results confirm key impairments in social cognition,109,110,111 they also highlight important challenges in nonsocial cognitive processing in ASD in the absence of overall intellectual disability. The most striking impairments in nonsocial cognition were evident in processing speed.
Dominant theories suggest that ASD is a disorder of the “social brain network” mediating social motivational and social cognitive processes, such as face processing, mental state understanding, and empathy.112 However, the findings of our systematic review and meta-analysis add support to the idea that ASD is not characterized by one “primary” cognitive deficit but instead by impairments in a selective range of “higher-order” cognitive abilities.113 This assumption is in agreement with the “multiple-deficit” theory,24 which proposes that autism may be a complex of cognitive disorders and that individuals may be affected differentially in various (possibly independent) cognitive domains. It is possible that certain subgroups experience deficits in multiple domains, while others only show impairments in a single area.
We were unable to examine the association between nonsocial and social cognitive impairments because most studies included in the present meta-analysis exclusively focused on nonsocial or social cognition. To disentangle this association and to increase our understanding of the cognitive mechanisms of ASD, future studies need to consider both domains.
Our findings have important implications for cognitive interventions in ASD. Current interventions in adults with ASD are primarily focused on improving individual adaptive social skills or social cognition114,115,116 (mainly theory of mind114,117), with an overall aim of improving social functioning.118 Our results support interventions that also include nonsocial cognitive domains. Promising findings from a randomized clinical trial by Eack et al119 suggest that cognitive enhancement therapy120 results in significant levels of improvement in nonsocial and social cognition. Cognitive enhancement therapy was initially designed for patients with schizophrenia,120 and the key targets of that intervention are the areas our systematic review and analysis showed to be most impaired (ie, processing speed and emotion perception and processing). Although now defined as distinct neurodevelopmental disorders, ASD and schizophrenia both share clinical and cognitive features,121 with the largest impairments in speed of processing (g = −1.03 for schizophrenia), verbal memory (g = −1.03 for schizophrenia), and executive functioning (g = −0.74 for schizophrenia).122 The broad profile of cognitive deficits in adults with ASD seems to be similar to that of individuals with schizophrenia but less severe (except in working memory, which is largely intact in ASD but not in schizophrenia122). This implies that cognitive training strategies shown to be effective across a range of cognitive domains in schizophrenia123,124 could also be adopted for the adult ASD population. More research should focus on the evaluation of effectiveness of cognitive remediation for adults with ASD.
Our systematic review and meta-analysis focused on cross-sectional studies in adults only. To our knowledge, only a single meta-analysis100 and a single systemic review125 have evaluated nonsocial cognitive deficits in children and adolescents with ASD, tapping into domains of executive functioning, working memory, and verbal fluency. When comparing these findings with the results of the present meta-analysis, we notice different profiles for specific cognitive impairments. Compared with childhood and adolescence studies, impairments in working memory100 and verbal fluency100,125 appear to become less pronounced in adulthood. In contrast, cognitive deficits in mental flexibility and response inhibition100 seem to be large in adults compared with children and adolescents diagnosed as having ASD. These findings may indicate that the pattern of cognitive development is domain specific, with development of some cognitive skills (eg, verbal fluency) delayed initially but eventually catching up to neurotypically developing controls; yet, for other domains (eg, mental flexibility), there might be a lasting developmental lag (as seen in other conditions).126 However, longitudinal studies are needed to unravel the trajectories of nonsocial and social cognitive functioning in ASD, as well as their association with functional and clinical outcomes in daily life.
Limitations and Recommendations
Our findings have to be considered in light of certain limitations. First, the domain-specific meta-analyses would have benefited from a larger number of studies (and larger sample sizes).127 Also, our meta-analyses rely exclusively on English-language peer-reviewed studies, which do not represent possible available evidence in other cultural or language areas. However, more recent data showed no systematic bias from the use of language restrictions in systematic review–based meta-analyses.128 Second, there was heterogeneity in samples regarding the diagnostic criteria used to identify individuals with ASD. However, diagnostic classification, which was included as a potential moderator in the regression models, had no association with the results. Third, some studies included individuals with higher-functioning ASD only, while others used more mixed samples (although still within the normal IQ range). Fourth, the severity of symptoms (measured by the ADOS or equivalent instruments) was rarely reported; therefore, potential cognitive variability within ASD could not be evaluated. However, a recent meta-analysis100 examining effect sizes of executive functioning between different ASD diagnostic classifications failed to find any differences. Another study129 found no association between different cognitive profiles and autism severity in all core domains. Fifth, there was some heterogeneity in types of cognitive measures used; for example, some studies worked with adapted and/or translated versions or different editions, which could have altered the outcomes. Yet, only studies using standard cognitive assessments were included in our systematic review and meta-analysis, and adapted or translated versions have been validated for the population for which they were being used. Sixth, comorbid symptoms are often found in ASD, including depression, anxiety, and attention-deficit/hyperactivity disorder (ADHD), among others.53 These comorbidities were not taken into account in the studies included herein. However, 32 of 75 included studies (42.7%) reported “other psychiatric disorder and/or neurological disorder” to be part of their exclusion criteria. It has been suggested that ADHD in children with ASD might be associated with distinct patterns of cognitive impairment.130 However, despite high comorbidity of ASD and ADHD,131 the 2 diagnoses could not be given simultaneously until the DSM-5 publication.132 Therefore, the cognitive impairments in ASD may be partly altered by comorbid ADHD. A systematic investigation is required to raise awareness about potential cognitive profiles associated with ADHD in ASD.
Conclusions
This systematic review and meta-analysis of impairments in nonsocial cognitive functioning and social cognition among adults with ASD showed that, despite having an intact IQ, there are medium to large deficits observed in 4 key domains of nonsocial and social cognition (theory of mind, emotion perception and processing, processing speed, and verbal learning and memory). While our findings support the key social cognitive theories of ASD, they also stress deficits in nonsocial cognitive areas. These results highlight the importance of a broader approach to our study of cognition and to our understanding of potential cognitive mechanisms underlying symptoms and treatment outcomes.
eAppendix. Supplemental Material
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