Introduction
Cognitive changes are common when people age, but what happens with aging if one has a psychiatric disorder like autism, that is, what if one already has cognitive deficits? Will everything deteriorate faster, or do efficient compensatory mechanisms develop? At present, it is unknown what happens when people with autism age (Rapin and Tuchman
2008; Seltzer et al.
2004; Volkmar et al.
2004).
Autism
1 is a heterogeneous psychiatric disorder which is characterized by social and communicative impairments and restricted, stereotypical patterns of behavior and interests (American Psychiatric Association (APA)
1994,
2000; Kanner
1943; Volkmar et al.
2004). The impairments are thought to last a lifetime (Cederlund et al.
2008; Howlin et al.
2004). Even though some autism symptoms seem to decrease with increasing age, elderly with autism will not reach normal levels of social functioning. A handful of studies focused on elderly with autism (James et al.
2006; Raznahan et al.
2010; Seltzer et al.
2004), but studies focusing on cognition in autism are mainly restricted to childhood and early adulthood. From these studies with young individuals it seems that autism is associated with early neurodevelopmental deficits in the same cognitive mechanisms that are also known to deteriorate with aging.
In both childhood and adulthood individuals with autism show a broad range of cognitive deficits, including executive functioning (EF) deficits (Geurts et al.
2009; Hill
2004; Pennington and Ozonoff
1996; Sergeant et al.
2002). EF is an umbrella term to describe various problems in complex, goal directed actions, and encompasses different cognitive domains such as working memory, cognitive flexibility, planning, and fluency. The idea has been postulated that the developmental pattern of EF in children and adolescents with autism is atypical (Happe et al.
2006; Luna et al.
2007; Pellicano
2010).
This idea stems from the finding that children with autism between 8 and 11 years of age showed several EF deficits, while these deficits did not emerge in children with autism aged 11–16 years (Happe et al.
2006). Also, in a recent longitudinal 3 year follow up, planning capacity in children with autism improved at a faster rate than that of typically developing children (Pellicano
2010). Hence, these findings indicate that EF deficits abate when aging. However, these findings might be in contrast with most recent adult studies in which executive dysfunctions are still present in individuals with autism above 16 years of age (Ambery et al.
2006; Bramham et al.
2009; Goldstein et al.
2001; Hill and Bird
2006; Keary et al.
2009; Lopez et al.
2005; Minshew et al.
2002; Shafritz et al.
2008). In some of these studies even elderly were included (Ambery et al.
2006; Hill and Bird
2006), but while the age range of participants was often large (16–66 year), the effect of age was not explored. In a cross-sectional developmental study (Luna et al.
2007) executive dysfunctions were present in people with autism of different ages (8–12, 13–17, and 18–33 year). Across the three age groups the autism group encountered inhibitory control deficits as well as working memory deficits. However, developmental improvements in inhibitory control were similar in both groups (i.e., parallel development), while the development of working memory was impaired in the autism group (Luna et al.
2007). The smaller extent of improvements in EF in children has also been reported in two longitudinal studies (Griffith et al.
1999; Ozonoff and McEvoy
1994). The combined findings from cross sectional and longitudinal studies suggest that there are different developmental patterns for different aspects of EF. Whether elderly with autism still encounter executive dysfunctions depends on whether deficits associated with autism at young age will remain stable, become more severe, or abate.
Unfortunately, none of the few autism-aging studies (James et al.
2006; Raznahan et al.
2010; Seltzer et al.
2004) systematically examined EF in elderly with autism. However, in case-studies of five elderly people with autism it has been described that each case still encountered EF deficits (James et al.
2006). Since EF-profiles in children and adults with autism show similarities to those seen in healthy elderly, it is surprising that EF has not yet been thoroughly studied in aging individuals with autism. A large body of research on aging in typically developing adults revealed that aging is associated with declines in various cognitive domains (Goh and Park
2009; Salthouse
2004). However, age-related deterioration in EF is thought to underlie most of these age-related declines (Friedman et al.
2009; Salthouse and Meinz
1995; Salthouse and Miles
2002; Verhaeghen and Cerella
2002), such as the decline in memory performance (Friedman et al.
2009; Salthouse
2004). It seems that memory itself is not impaired in adults with autism (Bowler et al.
2009; Bramham et al.
2009), but it is unknown whether memory deficits are present in elderly with autism.
The cognitive challenges healthy elderly people encounter are thought to relate to the structural (Galuzzi et al.
2008; Gunning-Dixon et al.
2009; Mora et al.
2007; Sullivan and Pfefferbaum
2006) and functional changes (Cabeza
2002; Davis et al.
2008; Goh and Park
2009; Park and Reuter-Lorenz
2009) of the brain. Aging is especially thought to affect various frontal brain regions (Galluzzi et al.
2008; MacPherson et al.
2002), which have also been found to function atypically in individuals with autism when performing EF tasks (Gilbert et al.
2008; Just et al.
2007; Kana et al.
2007; Luna et al.
2002,
2007; Schmitz et al.
2006). How the combination of aging and autism affects brain anatomy and brain functioning, and thereby behavior, is largely unknown. The current study will, therefore, provide a direct comparison between elderly with high functioning autism (HFA) and age and gender matched controls on various neuropsychological tests to determine which cognitive deficits are present in elderly with HFA. In this way we can explore whether the deficits are still present or indeed abate as has been suggested in developmental studies focusing on children (e.g. Happe et al.
2006; Pellicano
2010).
Discussion
The major aim of this study was to determine in which cognitive domains elderly with autism have deficits. The current results suggest that elderly with HFA show impairments in sustained attention, working memory, and fluency, while other cognitive domains are intact. Different developmental patterns emerged for fluency and visual memory in elderly with HFA and controls.
In children and adults with autism deficits have been observed in planning, and cognitive flexibility (Hill
2004). In elderly with autism these deficits do not seem to be present. This might suggest that the deficits observed at young age disappear when aging, which is in line with findings from previous studies in children (Happe et al.
2006; Pellicano
2010). As age did not have a specific effect on planning in participants aged between 51 and 83 years, a speculative hypothesis is that the deficit disappears before the age of 50. A longitudinal study is needed to determine whether individuals with autism catch up with their cognitive development for some EF domains (Happe et al.
2006; Pellicano
2010). If so, this would imply that deficits present in childhood or young adulthood are transitory and will disappear when aging. This might, for example, be due to different effects of age on brain development. With respect to cortical volume it seems that the age related reduction seen in specific brain areas of healthy people is less profound in people with autism (Raznahan et al.
2010), which might result in smaller decrease in cognitive abilities (see also McAlonan et al.
2002). Alternatively, although speculative, it could be that individuals with HFA have already acquired compensatory strategies to cope with their cognitive challenges which they can use when they get older (i.e., safeguard hypothesis).
An alternative explanation for the aforementioned findings is that the tasks used were not sensitive enough to determine whether elderly with HFA still have problems in planning, and cognitive flexibility. With respect to planning, this alternative explanation seems implausible, as the task we used (ToL) has repeatedly been used to show that deficits are present in children and adults with autism (Joseph et al.
2005; Pellicano et al.
2006; Robinson et al.
2009; Verte et al.
2005; Wallace et al.
2009; Zinke et al.
2010). With respect to flexibility, the findings in children and adults with autism are not consistent. However, it seems that adults with autism already succeed on the cognitive flexibility tasks we administered (Barnard et al.
2008; Hill
2004; Hill and Bird
2006), as is also the case for elderly with HFA. Therefore, in future studies alternative tasks may be useful to determine whether or not the planning and cognitive flexibility deficits indeed disappear.
With respect to the other cognitive domains, the pattern of findings in elderly with HFA seems to be similar to the pattern seen in children and adults with autism. The deficits in sustained attention, working memory, and fluency (Bramham et al.
2009; Geurts et al.
2004; Johnson et al.
2007; Spek et al.
2008; Zinke et al.
2010) continue to be present, while visual and verbal memory are still intact (Bowler et al.
2009; Williams et al.
2006). Hence, it could well be that for most cognitive domains, aging in elderly with HFA runs in parallel with typical aging. Moreover, a recent study focusing on brain anatomy (cortical thickness and cortical surface area) in people with autism (aged 10 through 60 years) showed that there are no differences in the developmental pattern of the frontal cortex between people with and people without autism (Raznahan et al.
2010). Our findings discussed so far suggest that there might be different developmental patterns for different aspects of cognition (see also Luna et al.
2007), as some deficits remain stable and others seem to disappear. However, from these findings it is not clear whether some of the deficits that remain might become more severe over time.
In line with the aging literature we found that with increasing age, performance decreases for both visual memory (Vakil et al.
2010) and fluency (Clark et al.
2009). However, the effect of aging differed between individuals with and without HFA. Whereas for fluency, the performance decrease was steeper for elderly
without autism, for visual memory elderly
with HFA showed a steeper performance decrease with increasing age. This latter pattern might suggest an accelerated decrease (i.e., double jeopardy).
One could hypothesize that aging and autism form a double jeopardy. The main hypothesis in one of the most dominant models of cognitive aging, the scaffolding theory of aging and cognition (Cabeza
2002; Goh and Park
2009; Park and Reuter-Lorenz
2009), is that when the aging brain degenerates, it will adapt to this degeneration by using different (or additional) brain areas as a compensatory mechanism. This is thought to be a normal adaptation of the brain to reduce the impact of the age-related brain degeneration on cognitive processes. Hence, if the aging brain would not reorganize, the cognitive performance of elderly would be worse. Various neuroimaging findings suggest that similar compensatory processes are already taking place in individuals with autism in adolescence and adulthood. It has been reported that in people with autism, more (and larger) brain areas are recruited during performance on EF tasks to obtain a performance similar to controls (Koshino et al.
2005; Schmitz et al.
2006; Takarae et al.
2007; Thakkar et al.
2008; but patterns of underactivation have also been reported; Kana et al.
2007; Luna et al.
2002; Minshew et al.
2002; Schmitz et al.
2006; Solomon et al.
2009). If normal age-related compensatory processes cannot be recruited in autism because the cognitive reserves are already in use at young age, one would expect a faster decline in cognitive performance in elderly with autism than in healthy controls. However, this account does not explain why the accelerated decrease was only observed for immediate reproduction of visual information.
The present study suffers from some limitations complicating the interpretation of these findings. First, a relatively small number of participants over 60 years of age were included, while it is known that various cognitive problems in healthy aging start to emerge only at the age of 60 (Nilsson et al.
2009; Treitz et al.
2007). Visual inspection of the figures (Figs.
2,
3) suggests that especially after the age of 75 performance is affected differently. Second, even though we verified the clinical diagnosis with a self-report questionnaire, we did not use other diagnostic measures to control whether the autism diagnoses were indeed correct. Third, most of the participants with autism were high functioning and received their autism diagnosis in late adulthood, which implies that the current findings may not be representative for the whole autism population. Moreover, we used the DART as a test of IQ, but this test of verbal intelligence might overestimate the IQs of some participants with autism as individuals with autism are sometimes very good in the automatic, rigid decoding of words, without having corresponding abilities in other skills. Nonetheless, given that for most participants the educational level was at or above average, we believe that we did solely include high functioning individuals.
In sum, aging might have a different impact in people with psychiatric disorders, like autism, than in controls, but the effect of aging in HFA depends largely on the cognitive domain under study. Although the aging trajectory for people with HFA is typical for most cognitive domains (i.e., parallel development), it is atypical and diverges from the normal pattern for some cognitive domains. On the one hand there is suggestive evidence for a double jeopardy aging pattern, while on the other hand there is evidence for a safeguard aging pattern. This divergence of developmental patterns for different cognitive domains has been observed in autism with respect to the cognitive development from childhood to adulthood as well (Luna et al.
2007). The current findings show that knowledge regarding autism based on studies in childhood and adulthood cannot be translated directly to elderly with autism, as different deficits are present depending of the age of individual with autism. Before we can draw firm conclusions, the current findings need to be replicated in a large study in which more elderly above 75 years of age should be included. Also, cognitive domains under study need to be extended to social cognition, as social impairments form an important part of the challenges that elderly with autism encounter.