Introduction
Methods
Selection criteria
Information sources and search strategies
Results
Studies on working memory
Authors | NASD/NTD | ASD age | Diagnosis method Diagnosis criteria Diagnosis | Material Memory task | Neuroimaging method Memory phase | Memory accuracy | Main results (ASD relative to TD groups) Conclusion |
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Audrain et al. [67] | 24/30 | 28.2 ± 6.59 | ADOS HFA | Visuospatial: abstract images 1-back | MEG Encoding, maintenance, recognition | Similar | Similar WM-related network in the theta frequency band between encoding and recognition and between ASD and TD, differing on maintenance Different WM-related network in the alpha frequency band between encoding, maintenance, and recognition and between ASD and TD Atypical functioning of WM maintenance, lack of inhibition of task-irrelevant processes |
Barendse et al. [68] | 13/13 | 15.3 ± 1.2 | ADOS DSM-IV Autistic disorder, Asperger, PDD-NOS | Visuospatial: faces and houses 1- and 2-back | fMRI Recognition | Similar | Similar activity and functional connectivity Analyses of sparse matrices: reduced global efficiency suggesting an increase in network costs WM difficulties are compensated |
Braden et al. [64] | 16/17 | 50.1 ± 1.7 | ADOS-2 DSM-IV DSM5 ASD | Verbal: letters 0-, 1-, 2-back | fMRI Recognition | Similar | Similar activation of the WM-related network, and similar deactivation of the DMN and salient network Decreased connectivity in the cortico-striatal-thalamic network when increasing memory load Functional brain difference persists with aging |
Chantiluke et al. [59] | 17/22 | 15.2 ± 1.8 | ADI-R and ADOS ICD-10 ASD | Verbal: letters 1-, 2-, 3-back | fMRI Recognition | Reduced | Under placebo: underactivation of the right dorsolateral PFC, and enhanced DMN deactivation Under fluoxetine: normalization of the dorsolateral PFC activation, and sub-normalization of behavioral results Fluoxetine modulates WM brain activation |
Hawco et al. [69] | 24/20 | 22.5 ± 4.7 | ADOS-2 ASD | Spatial: location of a dot 0-, 2-back | fMRI Recognition | Reduced, marginally significant | Greater variability in the pattern of dorsolateral PFC activation, in spite of similar between-group activation and connectivity Idiosyncratic prefrontal activation leads to diminished performance |
Herrington et al. [55] | 12/19 | 13.4 ± 4.2 | ADI-R and ADOS DSM-IV Autism disorder, Asperger, PDD-NOS | Visuospatial: superimposed faces and houses 1-back | fMRI Recognition | Similar | When attending to faces: increased activation within multiple PFC areas, including dorsolateral part Suggests selective attention in order to further discriminate faces |
Kleinhans et al. [57] | 19/21 | 23.5 ± 7.8 | ADI-R and ADOS DSM-IV Autistic disorder, Asperger, PDD-NOS | Visuospatial: neutral faces, or houses 1-back | fMRI Recognition | Similar | Similar activation of bilateral fusiform face areas, less functionally connected with both the subcortical face processing structures and the limbic structures Diminished connectivity within the limbic system supports social impairments |
Koshino et al. [51] | 14/13 | 25.7 | ADI and ADOS HFA | Verbal: letters 0-, 1-, 2-back | fMRI Recognition | Similar | Reduced activation in the left hemisphere, enhanced activation in the right hemisphere and posterior regions Reduced frontal connectivity; enhanced connectivity within posterior/occipital areas Enhanced processing of low-level visual features |
Koshino et al. [56] | 11/11 | 24.5 ± 10.2 | ADI-R and ADOS HFA | Visuospatial: neutral and emotional faces 0-, 1-, 2-back | fMRI Recognition | Similar | Reduced activations in both left inferior prefrontal areas and right posterior temporal areas Reduced fronto-fusiform functional connectivity Less verbally and socially oriented memory for faces |
Larrain-Valenzuela et al. [66] | 21/20 | 21.9 ± 4.1 | AMSE DSM5 ASD | Verbal: consonants Modified Sternberg task | EEG Recognition | Reduced | Modulation of alpha power (occipital cortex) and theta power (left premotor cortex and the right PFC) in TD. Absence of load-dependent modulation of alpha and theta power in ASD Atypical oscillatory activity contributes to WM difficulties |
Luna et al. [60] | 11/6 | 32.3 ± 9.3 | ADI-R and ADOS Autism | Visuospatial: location of a stimulus Oculomotor delayed response | fMRI Recall | Reduced | Decreased activation in both the dorsolateral PFC and the posterior cingulate cortex Fronto-parietal activation is reduced during WM |
Rahko et al. [63] | 28/22 | 14.6 [11.4–17.6] | ADI-R, ADOS, ASSQ ICD1-10, DSM-IV HFA, Asperger | Visuospatial: location of a stimulus 0-, 2-back | fMRI Recognition | Similar | Similar activation of WM-related areas, and similar DMN deactivation. Persistence of DMN when switching from 2- to 0-back in ASD only Inadequate memory load-dependent modulation of brain activity |
Silk et al. [62] | 7/9 | 14.7 ± 2.9 | ADI DSM-IV Autistic disorder, Asperger | Visuospatial: 3-dimensional block shapes Mental rotation task | fMRI Recognition | Similar | Reduced activation in frontal cortical and subcortical structures. Similar parietal activation Dysfunction of the fronto-striatal network |
Urbain et al. [54] | 20/20 | 11.25 ± 1.58 | ADOS HFA | Visuospatial: abstract images 1-, 2-back | MEG Recognition | Similar | Greater load-dependent activation in the left dorsal parietal cortex in the TD, while in the left ventral parietal cortex in ASD More controlled (i.e., top-down) processing of visual stimuli in the TD group, while being more automatic (i.e., bottom-up) in the ASD group |
Urbain et al. [58] | 17/20 | 11.17 ± 1.69 | ADOS HFA | Visuospatial: abstract images 2-back | MEG Recognition | Reduced, marginally significant | Reduced fronto-temporal connectivity in the alpha band Reduced electrophysiological connectivity contributes to WM difficulties |
Vogan et al. [52] | 19/17 | 11.05 ± 1.43 | ADOS HFA | Visuospatial: colored figures 1-back Color Matching Task, 6 levels of difficulty | fMRI Recognition | Reduced | Enhanced posterior activation. Reduced activation of frontal areas and the precuneus Less reliance on the fronto-parietal network for WM |
Vogan et al. [61] | 27/30 | 12.56 ± 1.46 | ADOS ASD | Verbal: letters Letter matching task, 4 levels of difficulties | fMRI Recognition | Reduced | Reduced activation of fronto-parietal areas when increasing the memory load; similar DMN deactivation Inadequate modulation of fronto-parietal activity when increasing WM load |
Vogan et al. [53] | 14/15 | 13.4 ± 1.82 | ADOS ASD | Visuospatial: colored figures 1-back Color Matching Task, 6 levels of difficulty | fMRI Recognition | Similar | 2-years follow-up of Vogan et al. (2014) Minimal age-related changes in load-dependent activation, but greater longitudinal load-dependent deactivation in DMN Inadequate modulation of fronto-parietal activity when increasing WM load |
Yuk et al. [65] | 40/39 | 27.17 ± 6.27 | ADOS ASD | Visuospatial: abstract images 1-, 2-back | MEG Maintenance, recognition | Similar | Maintenance: similar phase synchrony in theta, alpha, or beta bands; additional recruitment of fronto-parietal areas Recognition: diminished theta coherence between right frontal and left parietal areas Decreased theta connectivity; compensatory alpha recruitment |
Effects of the type of material on neuroimaging results
Short-term maintenance and manipulation
Studies on episodic long-term memory
Authors | NASD/NTD | ASD age | Diagnosis method Diagnosis criteria Diagnosis | Material Memory task | Neuroimaging method Memory phase | Memory accuracy | Main results (ASD relative to TD groups) Conclusion |
---|---|---|---|---|---|---|---|
Chan et al. [86] | 21/21 | 10.27 ± 2.26 | DSM-IV Autistic disorder, PDD-NOS | Visuospatial: line drawings Object recognition task | EEG Recognition | Reduced | Greater antero-posterior theta connectivity in the left hemisphere in ASD, and in the right hemisphere in TD. Negative correlation between coherence and performance in ASD only Threshold of connectivity beyond which performance decreased |
Churches et al. [81] | 11/11 | 31.82 ± 6.88 | DSM-IV Asperger | Visuospatial: neutral faces Recognition | EEG Recognition | Reduced | Reduced amplitudes on the N170 potential for both target and non-target faces; reduced amplitude on the N250 potentials to target faces only The development of new face representation is impaired |
Cook et al. [92] | 12/19 | 13.18 ± 1.73 | ADI-R and/or ADOS DSM5 ASD | Visuospatial: object–scene pairs Rate the congruence | fMRI Encoding | Reduced object recognition Similar associative recognition | TD: encoding of subsequently recognized pairs associated with greater activation of the bilateral medial prefrontal cortex for intermediate relative to congruent pairs, and with greater activation of the left medial temporal lobe for congruent relative to intermediate pairs ASD: same level of activation regardless of the level of congruence; higher activations in bilateral, prevailing left medial prefrontal areas, for participant with greater behavioral flexibility Lack of modulation of encoding-related processes with the level of congruency |
Cooper et al. [90] | 24/24 | 30.3 ± 8.4 | DSM5 or ICD-10 ASD | Visuospatial: background, and objects Recognition | fMRI Encoding and recognition | Reduced | Encoding: similar levels of activity and connectivity among prefrontal, hippocampal and parietal areas Recognition: limited differences: reduced left prefrontal activity, and reduced hippocampal connectivity with the fronto-parietal areas Memory representations are processed similarly by the hippocampus; limited pre-retrieval search or post-retrieval monitoring |
Desaunay et al., [79] | 22/32 | 16.51 ± 3.56 | ADI-R and/or ADOS DSM5 and ICD-10 ASD | Visuospatial: picture pairs Associative recognition | EEG Recognition | Reduced | Reduced amplitude on the P2 and FN400 potentials: limited integration of low-level perceptual into high-level conceptual information, decrease in familiarity strength Spatial extension of the LPC: suggests additional recruitment of associative processes Effortful retrieval of associative information compensates for the lower familiarity strength |
Gaigg, et al. [89] | 13/12 | 35.6 ± 10.3 | ADOS DSM-IV ASD | Verbal: word triplets, semantically related or not Associative recognition | fMRI Encoding | Similar | Similar brain activations, including the left inferior frontal gyrus and the left hippocampus, with similar signal change with the degree of relational encoding Only limited signal change in prefrontal and posterior hippocampal regions, when contrasting the degree of awareness for subsequent retrieval Attenuated levels of recollection are related to anomalies in relational encoding processes |
Greimel et al., [82] | 13/13 | 15.9 ± 3.0 | ADI-R and ADOS DSM-IV and ICD-10 HFA, PDD-NOS, Asperger | Visuospatial: objects superimposed with faces or houses Recognition of the objects | fMRI Encoding | Similar | Encoding of subsequently recollected objects presented with a face: reduced activations within bilateral inferior and medial frontal gyri and the right intraparietal lobule Encoding of subsequently non-recollected objects presented with houses: increased activation of the dorsal-medial PFC Incidental encoding of faces in the ASD group is less automatic and less associated with social information |
Gunji et al. [80] | 8/9 | 10.8 ± 2.9 | DSM-IV HFA, Asperger | Visuospatial: self, familiar, unfamiliar faces Recognition of the subject’s own face and familiar faces | EEG Recognition | Similar | Shorter N170 latency No amplitude difference on the early posterior negativity between Self vs. Familiar and Familiar vs. Unfamiliar No amplitude difference on the P300 between familiar and unfamiliar faces Deficit of semantic encoding of faces |
Hogeveen et al. [91] | 47/60 | 18.4 ± 2.81 | ADOS-2 DSM5 ASD | Visuospatial: item-specific or relational encoding Item or associative recognition | fMRI Encoding | Similar (for item and associative recognition) | Increased hippocampal activity along with diminished connectivity between the medial temporal lobe and postero-medial brain regions Hippocampal hyper-recruitment suggests compensation for the decrease in regional connectivity to support the preservation of associative memory |
Lynn et al. [83] | 13/13 15/16 13/14 | 11.7 ± 1.2 15.3 ± 1.8 24.9 ± 4.9 | ADI and ADOS Autism | Visuospatial: faces and cars Recognition | fMRI Encoding and recognition | Reduced (for both faces and cars) | Encoding and recognition: face-specific underconnectivity between bilateral fusiform face areas and the medial PFC Recognition: both general (i.e., cars) and specific (i.e., faces) underconnectivity between the right fusiform face area and the visual cortex Diminished integration of information; abnormalities in perceptual systems also contribute to recognition deficits, especially with faces |
Massand et al. [87] | 22/14 | 25.72 ± 4.76 | ADI-R and/or ADOS DSM-IV ASD | Verbal: high- and low-frequency words Recognition | EEG Recognition | Similar | Parietal rather than anterior early FN400 old/new effect related to familiarity Similar parietal LPC potential related to recollection Preservation of the electrophysiological recollection process |
Massand & Bowler [88] | 15/18 | 38.89 ± 14.77 | ADOS DSM-IV Autism, Asperger | Visuospatial: line drawings of objects Recognition (line drawings) and recall (their color) | EEG Recognition and recall | Reduced recognition | Posterior and attenuated FN400 old/new effect related to familiarity, occurring in a large time-window (300-650 ms) Similar parietal LPC potential related to recollection Preservation of the electrophysiological recollection process |
Neumann et al. [78] | 7/7 | 20.9 ± 10.6 | ADI-R ICD-10 HFA “mnemonist savants” | Verbal: pseudowords Visuospatial: abstract shapes Recognition | MEG Recognition | Reduced (pseudowords) Similar (shapes) | Both stimuli: early right occipital activation (100-200 ms) in ASD only Shapes: bilateral old/new effect (200-500 ms) reflecting familiarity-based recognition, being more left hemispheric in controls Expertise with figural material; pseudowords were processed and recognized similarly to visual material |
Noonan et al. [85] | 10/10 | 23 ± 9.9 | ADI-R and ADOS DSM-IV HFA | Verbal: words read or heard Recognition (item and source) | fMRI Recognition | Reduced | Unexpected enhanced left fronto-parietal functional connectivity Atypical functional connectivity |
O’Hearn et al. [84] | 15/13 16/19 14/15 | 11.7 ± 1.17 15.39 ± 1.17 24.56 ± 4.87 | ADI and ADOS Autism | Visuospatial: faces and cars Recognition | fMRI Encoding and recognition | Reduced (for both faces and cars) | Similarity of fusiform face area activation increased from childhood to adolescence, then decreased from adolescence to adulthood Recognition performance was more related to the similarity score in the left fusiform face area Reduced specialization of the fusiform face area |