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Table 2 Included studies on episodic long-term memory

From: Brain correlates of declarative memory atypicalities in autism: a systematic review of functional neuroimaging findings

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

  1. ADI Autism Diagnosis Interview; ADI-R Autism Diagnostic Interview-Revised; ADOS Autism Diagnostic Observation Schedule; AMSE Autism Mental Status Exam; ASD Autism Spectrum Disorder; ASSQ Autism Spectrum Screening Questionnaire; DMN (Default Mode Network); DSM-IV Diagnostic and Statistical Manual of Mental Disorders, 4th version; DSM5 Diagnostic and Statistical Manual of Mental Disorders, 5th version; ICD-10 International Classification of Diseases, 10th version; LTM Long-term memory; PFC prefrontal cortex; TD Typically Developing)