The objectives of this descriptive study were to provide summary findings on a battery of clinical memory measures from the Test of Memory and Learning in children and adolescents with autism. By definition subjects with autism have “impairments in communication”—this criterion alone is associated with a broad spectrum of cognitive profiles and deficits (Happe, Ronald, & Plomin, 2006
; Munson, Dawson, et al., 2008
; Munson, Faja, Meltzoff, Abbott, & Dawson, 2008
). In the current study only autism subjects with nonverbal intellectual abilities ≥85 were included, but verbal intellectual abilities were free to vary. Indeed, in this autism sample although the mean VIQ was average, it was almost a standard deviation below the control sample and likewise, reflected considerably more variability in the range of verbal abilities. Variability in cognitive performance represents a common finding in autism (Towgood, Meuwese, Gilbert, Turner, & Burgess, 2009
). Clearly, the reduced overall level of verbal intellectual functioning in autism creates natural differences in cognitive abilities between the autism and control subjects in this investigation. Increased variability in verbal and semantic functions also clouds group comparisons, where some children with autism may have frank deficits and others no impairment, all within the same grouping. Although verbal abilities were reduced and more variable within the autism group, their overall levels of verbal and nonverbal intellectual functions were nonetheless in the average to above average range. As already mentioned, Dennis and colleagues (2009)
argue that when examining children with developmental disabilities controlling for IQ may unduly constrain how a disorder affects cognition, understanding that the IQ variable represents a commonality factor reflecting nonspecific cognitive ability often discussed in terms of a general variable or “g” (Oberauer, Schulze, Wilhelm, & Suss, 2005
). One way to overcome such issues is to first examine within group comparisons within a cognitive domain compared to a reference point. For example, on psychometric testing IQ and memory metrics are significantly correlated (Oberauer et al., 2005
; Leeson et al., 2010
), including IQ and CMI correlations on the TOMAL (Hoerig, David, & D’Amato, 2002
). A common clinical interpretive method in examining memory performance is to compare memory scores to IQ scores, with the assumption that the IQ score represents a reference where in nonpathological circumstances memory scores should approximate the reference intellectual score (Lezak, Howieson, & Loring, 2004
). In fact, in other studies examining diverse pediatric conditions excluding autism (Allen et al., 2010
; Thaler, Allen, McMurray, & Mayfield, 2010
; Howes, Bigler, Lawson, & Burlingame, 1999
; Gutteling et al., 2006
; Porter, Lawson, & Bigler, 2005
), the TOMAL CMI consistently was within a few points of the intellectual reference measure in the control samples. Consistent with this observation, the CMI in the controls for this investigation differed only by .35 and .5 standard deviations for VIQ and NVIQ, respectively. However, in the autism group the CMI was .85 and 1.42 standard deviations lower than VIQ and NVIQ, respectively. Clearly, these subjects with autism not only had lower memory performance in comparison to the typical developing control sample, but also exhibited within group lower memory performance compared to their average to above average intellectual scores.
Turning to the other TOMAL index memory and subtest scores when statistically compared to the control sample, overall memory performance in autism reflected reduced ability across all aspects of memory. Large between-groups effect sizes were found for all composite scores and for a majority of subtests. Even for the memory tasks where autism subjects performed more closely to controls, including Memory for Location, memory span for imitating simple hand positions sequences (Manual Imitation), and word list selective reminding (Word Selective Reminding-delayed condition only), moderate effect sizes were present. Given the exploratory nature of this study and to facilitate comparison of present results to previous research, statistical controls for multiple comparisons were not employed. However, the robustness of observed effects across TOMAL scores suggests that most of these differences would survive correction.
These findings of generally reduced memory performance in autism using a clinical battery of memory tests are similar to those of Lajiness-O’Neill et al. (2005)
, who reported composite TOMAL scores in the low average range among a younger sample of participants with autism. It should be noted that five subjects with autism from the original Utah cohort, were included in the Lajiness-O’Neill et al. investigation, so there was some overlap in subject composition. The Williams et al. (2006a)
study matched and controlled for verbal IQ so their approach was statistically different than the analysis of the current investigation, but still demonstrated lowered memory performance on the WRAML in subjects with autism. The extent and scale of reduced memory performance in the present study was greater than the findings of Williams et al. (2006a)
, who reported a more restricted profile of decreased memory performance in their sample of children and adolescents with HFA, but their autism group did not differ from their control sample in VIQ whereas in the current study VIQ was significantly lower in the autism group. In the Williams et al. (2006b)
study tasks involving complex verbal and auditory recall revealed deficits in the autism group, while simpler auditory and visual-spatial tasks did not (Williams et al., 2006b
). To investigate the possibility that verbal ability discrepancies may partly account for the broad pattern of reduced memory performance on the TOMAL, a subset of the autism group was matched with controls on verbal IQ. In this more conservative analysis, t
tests revealed that group differences remained significant for all but those TOMAL subtests that were associated with moderate effect sizes in the VIQ-uncontrolled analysis: memory for location, manual imitation, and delayed word selective reminding (see ). This matched IQ comparison confirms in this sample that subjects with autism displayed reduced memory ability on the TOMAL even after controlling for IQ.
Comparing autism performance to the national normative standard for the TOMAL, only Object Recall and Digits Forward were performed below the average range. The autism group in this study performed best on the Manual Imitation task, a nonlanguage sequential recall test using simple hand gestures, where performance by the subjects with autism was exactly at the norm for the TOMAL standardization sample. This type of recall is consistent with previous findings suggesting that basic serial recall may be intact in autism (Bennetto, Pennington, & Rogers, 1996
; cf. Bowler & Gaigg, 2008
; Williams, 2006a
). Other TOMAL subtests with scaled scores ≥9.0 included Paired Recall, Abstract Visual Memory, Memory for Location and Word selective Reminding. Likewise, delayed recall was not significantly different from immediate recall in either the autism or control group, indicating no abnormal decay in retained information.
In that delayed recall was not disproportionately degraded in the autism subjects compared to their immediate recall implies intact retrieval once the information has been processed. These findings are in line with previous research (Minshew & Goldstein, 1993
; Williams et al., 2006b
), further supporting the proposition that recall for adequately encoded information is intact in autism. Overall, the current finding that memory in autism is not disproportionately affected by a delay corresponds with previous research (Lajiness-O’Neill et al., 2005
; Williams et al., 2006a
) that suggests that initial information encoding and organization, rather than storage and retrieval, are the primary memory deficits in autism. Likewise, since the majority of TOMAL memory measures were performed within the average range suggests basic cognitive functions in autism associated with memory processing may be adequate, but somewhat inefficient resulting in reduced performance when compared to within Group IQ measures or the control sample. Some have postulated that the child with autism is challenged by the complexity of a stimulus to be processed resulting in a “part-oriented strategy” that is simply less efficient, disrupting memory processing and ability level (Bertone, Mottron, Jelenic, & Faubert, 2005
; Tsatsanis et al., 2011
While the use of clinical and nationally standardized memory measures constitutes a strength in the present study, in that a broadband assessment of memory functioning using a conormed set of tasks was possible, such an approach does not allow for systematic test modifications that can elucidate cognitive processes and mnemonic strategies. The current findings document reduced memory performance but without more experimental methods, do not provide an explanatory mechanism why reduced memory performance occurs in autism. Nonetheless, some qualitative speculations about the data from the present study can be made. For example, some of the largest between group effect sizes were exhibited on tests requiring recall of contextually organized information (Memory for Stories, Facial Memory and Abstract Visual Memory). Experimental investigations of cognitive style in autism have suggested that affected individuals are less likely to make spontaneous use of relational information to enhance memorization and recall (Bowler, Gaigg, & Gardiner, 2010
). Thus, as the information load increases, as in a story content or array of faces, the use of relational information may become more essential to effective memory performance.
Recent research on the neurodevelopmental underpinnings of abnormal language development in lower functioning individuals with autism has turned to episodic memory functioning as a potential contributing factor (Boucher, Mayes, & Bigham, 2008
). Boucher, Bigham, Mayes, and Muskett (2008)
hypothesized that language impairment in low-functioning autism arises in part from the effects of declarative memory dysfunction on semantic-linguistic development (Ullman, 2004
). In this model, dysfunction in explicit memory processing, present early in development, disrupts the formation and integration of episodic memories that eventually become semantic memories or knowledge. In an early test of this “declarative memory hypothesis,” Boucher, Bigham et al. (2008)
measured visual recognition memory in children and adolescents with autism who had low or high verbal functioning, compared to nonverbally matched, same-mental age peers with and without intellectual disability. They found disproportionately impaired recognition memory that was uniquely related to episodic tasks for the low-functioning autism group. The results of a supplemental analysis in the current study showed that performance on an extensive clinical battery of episodic memory tasks is moderately related to measures of semantic-verbal conceptual abilities, both for typically developing children and adolescents and those with autism.
In addition to limitations already mentioned, several limitations are apparent in this research. Although the TOMAL is standardized from ages 5 to 19, which encompassed the age ranges of the current sample, a host of developmental issues may influence memory performance that simply cannot be addressed by this type of cross-sectional design (Shing et al., 2010
). As already identified, the issues of general cognitive ability versus specific memory impairment in autism remain unresolved by the design of the current study and its descriptive analysis. Ideally, in future studies cognitive ability in a number of domains (i.e., language, including language subtypes (Rapin, Dunn, Allen, Stevens, & Fein, 2009
), visuospatial ability, executive skill, etc.), in addition to just an IQ metric, could be stratified both in typical developing as well as autism subjects to better explore relationships between general cognition, other cognitive domains, and memory function. There are probably complex interrelationships across different cognitive domains in autism, where examination of memory function should not be viewed as a single factor (Gustafsson & Paplinski, 2004
). While the current cross-sectional study demonstrates reduced memory performance in a sample of children and adolescents with high functioning autism, generalization of such findings cannot be made from a single investigation. The current study is the first to use the TOMAL to show reduced memory performance in autism, but additional studies would be needed to show how generalizable this TOMAL pattern of memory performance is in autism.
Autism is a clinical diagnosis with no proven diagnostic biomarker. However, tremendous strides are being achieved in terms of genetic markers which may define certain aspects of the disorder. For example, recently loci on chromosomes 10 and 16 have been identified that relate to the common profile of lowered VIQ to NVIQ that often characterizes an autism sample (Chapman et al., 2010), including the one in this investigation. If a cognitive biomarker is proven to be present in autism, this could prove to be an exceptional method to study memory differences in autism.
In conclusion, these findings indicate that episodic memory performance is broadly reduced in autism. Since retention following a 30-min delay was not disproportionately affected in autism indicating adequate retrieval of information, reduced episodic and declarative memory in autism may be most affected by deficits in information encoding and organization, possibly due to inefficient cognitive processing strategies rather than storage and retrieval as the primary factors that limit memory performance in autism.