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JAMA Network logoLink to JAMA Network
. 2019 Jan 2;76(2):135–151. doi: 10.1001/jamapsychiatry.2018.3645

Patterns of Nonsocial and Social Cognitive Functioning in Adults With Autism Spectrum Disorder

A Systematic Review and Meta-analysis

Tjasa Velikonja 1,2,, Anne-Kathrin Fett 3, Eva Velthorst 1,2
PMCID: PMC6439743  PMID: 30601878

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.

a

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.

b

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.

c

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
Schneider et al,73 2013 X X X
Schneider et al,74 2015 X X X
Schuwerk et al,75 2015 X
Senju et al,76 2009 X
Shamay-Tsoory,77 2008 X X
Spek et al,78 2010 X X X
Spek et al,79 2011 X X
Stewart et al,80 2013 X X
Sucksmith et al,81 2013 X X
Sumiyoshi et al,82 2011 X X
Tobe et al,83 2016 X X
Torralva et al,12 2013 X X X X X X X
Wallace et al,16 2008 X
Wallace et al,84 2010 X
Walsh et al,85 2016 X
White et al,86 2006 X X X
White et al,87 2011 X
Williams et al,21 2005 X
Williams et al,88 2014 X
Williams et al,89 2018 X
Wilson et al,90 2014 X X X X
Zwickel et al,91 2011 X

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.

Figure 1.

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.

Figure 2.

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.

Supplement.

eAppendix. Supplemental Material

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