Elsevier

Behavioural Brain Research

Volume 237, 15 January 2013, Pages 32-40
Behavioural Brain Research

Review
Lifespan development: The effects of typical aging on theory of mind

https://doi.org/10.1016/j.bbr.2012.09.020Get rights and content

Abstract

Whether typical aging is associated with impairments in social understanding is a topic of critical importance in characterizing the changes that occur in older adulthood. Theory of mind (ToM) refers to the ability to represent other's mental states, and has been tested in a variety of different paradigms in older adults. The overarching research question has been whether ToM abilities may rely on other cognitive abilities, such as processing speed or executive functioning, and as such declines in ToM may reflect a decline in general meta-representational abilities. Alternatively, ToM abilities may be relatively spared, suggesting the acquisition of a sort of social wisdom with advancing age. The preponderance of the evidence is in line with the first possibility: namely, ToM, as measured by paradigms involving faces, cartoons, stories, and videos is typically impaired in social aging, and these impairments are at least partly mediated by impairments in executive functions and fluid intelligence (but not typically by crystallized intelligence). Neuroimaging investigations suggest that older adults who perform as well as younger adults may activate compensatory mechanisms, but are impaired in the brain mechanisms most closely associated with ToM ability when their task performance is impaired. Recent methodological advances allowing continuous rather than categorical assessment of ToM show that ToM may be observed to function independently from general cognition in aging, but further investigation is needed to confirm this point. Implications of these findings for the longstanding discussion regarding Theory of Mind's endangered status as a special cognitive module are discussed.

Highlights

► I review the extant literature on aging and social cognition. ► I cover studies investigating theory of mind and moral judgments. ► Theory of mind deficits are partially dependent on deficits in general cognition. ► The brain regions linked to theory of mind show task-specific deficits in aging. ► Aging is a unique method to study whether theory of mind is a specialized module.

Introduction

Social cognition, or how humans understand and interact with other humans, comprises a set of skills whose successful application is critical for the cohesion of individual and societal relationships. For humans, the development of social interaction may represent the pinnacle of evolution of our cognitive architectures. According to Dunbar [1], the relative explosion of neocortex size in humans compared with other primates and with non-primates is tightly associated with the larger social groups in which we embed ourselves. And indeed, understanding our social partners who in turn are attempting to predict our actions is a difficult computational task that may be unparalleled by other evolutionary pressures (such as the use of tools [2]), and thus may have provided selection pressures for larger neocortices. Theory of mind (ToM) is a hallmark ability underlying social interaction, which allows representation of the mental states of others. Evidence from the evolutionary perspective hence suggests that social cognition may comprise a set of abilities (including ToM) that are independent from general cognition, and theorists in cognitive development have separately posited the existence of a Theory of Mind Module [3]: a domain-specific cognitive device that is specialized for the understanding of mental states. An alternative hypothesis, supported by lesion work and by some work in autism, is that Theory of Mind is predicated on meta-representation, which is the domain-general ability to think about and manipulate other representations (such as a mental image of a drawing of a pencil) [4].

Another perspective that could inform this debate is investigating how ToM fares in later lifespan development. If ToM is impaired in aging, does it decline in ways that tie it to more basic cognitive operations? If so, would we be able to conclude that ToM is, in general, predicated on more domain-general cognitive abilities? Reflection on the possible trajectories for ToM in typical aging suggests two hypotheses. First, since ToM is tied to the functioning of a specific cognitive architecture, declines in that cognitive architecture (e.g., [5]) may also be associated with declines in social functioning. The weight of the evidence suggests that older adults do show marked declines in aspects of ‘fluid’ intelligence [5]; those aspects include skills such as working memory, processing speed, and numerical ability. If older adults perform worse at ToM, one explanation is that low fluid ability simply makes the task more difficult for them, independent of any domain-specific difficulties in ToM. Therefore, it is important to note whether effects are independent of differences in these crucial domains of cognition. Executive functioning (e.g., inhibiting prepotent responses, choosing among alternatives) also declines with age [6]. Presumably, such declines might also be associated with difficulties in some of the nuances of social cognition.

Alternatively, a lifetime of accumulation of knowledge about the social world may lead to us becoming much more efficient in our social interactions, and as a result, certain aspects of social cognition may comprise a domain in which experience trumps youth. This view sits well with the evidence from general cognition [5], which argues that older adults show sparing of ‘crystallized’ aspects of intelligence, such as verbal memory, general knowledge, and vocabulary. If older adults show preserved ToM ability, this may result from greater knowledge about social relationships that does not decline in aging. It is important to note here that spared ToM could be due either to fluid declines being compensated for by improved crystallized intelligence, or to a true lack of decline in a specialized ToM module. Initial evidence favored the general hypothesis that ToM is unimpaired with age, but in recent years the preponderance of data has edged toward the alternative that there are specific measurable deficits in ToM with increasing age. This review will first describe the early developmental trajectories of aspects of social cognition such as theory of mind and moral judgments. In doing so, the gradual development of ToM will be revealed, whereby more complex aspects of ToM emerge only once simpler aspects are mastered. Any differences in ToM due to age can thus be interpreted in light of how those specific aspects of ToM map onto the typical developmental trajectory. I will then discuss behavioral evidence concerning social cognition in typical aging, and finally turn to recent neuroimaging results that provide complementary evidence on the effects of normal aging on social cognition.

Section snippets

Theory of mind

ToM is variously referred to as mental state understanding, social understanding, or mentalizing. It is present in typically developing children by approximately age five [7], may be present in adult chimpanzees [8], and is developmentally delayed in individuals with autism spectrum disorders [9]. The typical developmental course of ToM abilities proceeds along roughly the following ‘stages’. Children initially develop shared attention mechanisms that allow them to direct others’ attention by

ToM in later life and its relation to general cognitive ability

The preceding section suggested a clear developmental path for ToM and more complex ToM-based abilities like moral judgments. Thus, one might expect that any declines in ToM due to age might first be observed in more complex tasks (e.g., second order ToM), and ultimately in more basic tasks (e.g., first order ToM). Because the literature and stimuli used to test ToM in aging are varied, this section begins with a brief historical summary of early findings in the field—which hinted that older

Neuroimaging investigations of ToM in aging

Thus far, the application of neuroimaging to understanding the mechanisms of ToM in aging has been spare. This is unfortunate, as given such conflict in findings in the behavioral literature, neuroimaging may be a particularly useful tool for understanding how, if at all, aging affects ToM processes. Early work focused on gross measures of anatomy, including whole brain volume and white matter integrity. Investigations using functional imaging to this date suggest a pattern of compensatory

Conclusion

Much of the early work in social understanding in aging highlighted the need to obtain multiple measures of cognitive functioning such that we might understand better how ToM relates to general cognitive abilities. This is an important question for aging, as if ToM declines independently from other abilities, it becomes critical to find ways to stem this decline; older adults may need help in relearning the subtleties of social communication, especially with strangers whose intentions are not

Acknowledgments

The author wishes to thank Jason Mitchell, Anne Krendl, Diana Tamir, and Rita Ludwig for comments and suggestions on this manuscript.

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