Review
Theory of Mind in normal ageing and neurodegenerative pathologies

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Abstract

This paper reviews findings in three subcomponents of social cognition (i.e., Theory of Mind, facial emotion recognition, empathy) during ageing. Changes over time in social cognition were evaluated in normal ageing and in patients with various neurodegenerative pathologies, such as Alzheimer's disease, mild cognitive impairment, frontal and temporal variants of frontotemporal lobar degeneration and Parkinson's disease. Findings suggest a decline in social cognition with normal ageing, a decline that is at least partially independent of a more general cognitive or executive decline. The investigation of neurodegenerative pathologies showing specific deficits in Theory of Mind in relation to damage to specific cerebral regions led us to suggest a neural network involved in Theory of Mind processes, namely a fronto-subcortical loop linking the basal ganglia to the regions of the frontal lobes.

Highlights

► In normal ageing, disturbances in social cognition seem independent of a more general cognitive decline. ► When neurodegeneration spares brain areas underpinning social cognition, this ability is unaffected. ► Impairment in social cognition is related to increased vulnerability of the frontal lobes with ageing.

Introduction

Social cognition has been defined as the ability to interpret and predict others’ behavior, based on their beliefs and intentions, and to interact in complex social environments and relationships (Baron-Cohen, 2000). The ability to understand and respond to the emotional content and cues present in the environment and the ability to remember emotional information are integral parts of social cognition (Adolphs, 2003, Grady and Keightley, 2002). Social cognition guides both automatic and volitional behavior, being composed of a variety of cognitive, emotional, and motivational processes that modulate behavioral responses. Memory, decision-making, attention, motivation, and emotion are all prominently recruited when socially relevant stimuli elicit behavior (Adolphs, 2009). Most empirical studies in social cognition have focused on developmental diseases (e.g., autism, Asperger's syndrome), or analyzed the consequences of acquired lesions (e.g., brain injury, stroke) on social cognition. Less is known about the integrity of social cognition in elderly individuals (see Table 1 for a description of studies on social cognition in normal ageing).

Due to the increasing prevalence of dementia with ageing, early diagnosis is important in enabling better support for these patients. The assessment of social cognition during ageing appears fundamental to this diagnostic approach. This point of view is supported by the American Psychiatric Association, which, by the intention to include impairment of social cognition in the new diagnostic criteria for “Major Neurocognitive Disorder” (i.e., former “dementia”) in the DSM-V (Diagnostic and Statistical Manual of Mental Disorders-V), demonstrates an awareness of the increased vulnerability of social cognition mechanisms with ageing and highlights the importance and necessity of addressing social cognition in patients suspected of dementia. Assessment tools in social cognition may be particularly sensitive in the diagnosis of pathological ageing and may be valuable in guiding the diagnosis toward a particular neurodegenerative disease.

The most representative mechanism of social cognition is “Theory of Mind” (ToM), which designates the ability to attribute the full range of mental states (both goal and epistemic states) to ourselves and to others, and to use these attributions to make sense of and predict behavior. The term “Theory of Mind”, was first introduced by Premack and Woodruff (1978), but there is a set of synonyms frequently employed, namely “mind reading”, “mentalizing” and “mental state attribution”. One recent model (Shamay-Tsoory et al., 2010) distinguishes cognitive (or “cold”) from affective (or “hot”) sub-processes of ToM (see Fig. 1).

Cognitive ToM refers to the ability to make inferences about the cognitive states, beliefs, thoughts, intentions and motivations of other people (Brothers and Ring, 1992, Coricelli, 2005), while affective ToM refers to the ability to infer the feelings, affective states and emotions of others (Brothers and Ring, 1992). Cognitive ToM can be assessed by a first- and second-order false belief task (see Appendix A for a task description), while affective ToM can be assessed using the Faux-Pas Test (Baron-Cohen et al., 1999) (see Appendix A for a task description). According to this model, cognitive ToM is a prerequisite for affective ToM, which also requires intact empathy processing.

ToM capacities first manifest themselves during early infancy (i.e., around 18 months of age), when children engage in shared attention and proto-declarative pointing (Baron-Cohen, 1995). Before that age, children are not able to decouple pretense from reality. Between 18 and 24 months, children begin to understand the mental state of “pretend” (Leslie, 1987), and, by age 2 years, they begin to have a firm grasp of the mental state of desire (Wellman and Woolley, 1990). Between ages 3 and 4 years, children can understand that another person may hold false beliefs (Gopnik and Astington, 1988, Johnson and Wellman, 1980, Wimmer and Perner, 1983). Prior to this age, a child does not understand that other people can hold beliefs about the world that differ from his or her own. Between ages 6 and 7 years, children begin to pass more advanced tests that examine “belief about belief” and begin to understand that other people can also represent mental states (Perner and Wimmer, 1985). Complex social skills first appear between ages 9 and 11 years, when children develop further ToM abilities, such as recognizing a social “faux-pas” or wrong behavior. Understanding that a faux-pas has occurred requires the representation of two mental states: that the person saying something does not know that he/she should not say it and that the person hearing it would feel insulted or hurt. Thus, there is both a cognitive component and an empathic affective component in this particular task (Baron-Cohen et al., 1997).

Empathy, a second component of social cognition, is mainly implicated in prosocial behavior, morality and the regulation of aggression (Eisenberg and Eggum, 2009). Moreover, the term empathy is applied to a broad spectrum of phenomena, from feelings of concern for other people that create a motivation to help them, experiencing emotions that match another's, knowing what the other is thinking or feeling, to blurring the line between self and other (Hodges and Klein, 2001). Due to the complexity of the phenomenological experience of empathy, this construct has been broken down into component processes (Decety, 2010) (see Fig. 2).

These different components are intertwined and contribute to different aspects of the experience of empathy. Affective arousal is the first component that appears during development, having evolved to differentiate automatically hostile from hospitable stimuli and to organize adaptive responses to these stimuli. Emotion understanding develops later, beginning to be mature around age 2–3 years. This component largely overlaps with ToM-like processing. Emotion regulation enables the control of emotion, affect, drive and motivation. This component develops throughout childhood and adolescence, and parallels the maturation of execution functions. Humans also have the capacity to appraise and reappraise emotions and feelings; all of goals, intentions, context, and motivation are likely to play feed-forward roles in how emotions are perceived and experienced. Thus, empathy is not only a passive affective phenomenon; empathy is not simply a resonance with the emotions of others.

The recognition of emotions in faces is an essential component of social cognition. Social cognition has been defined as “the processing of any information which culminates in the accurate perception of the dispositions and intentions of other individuals” (Brothers, 1990, Brothers, 2002). Among the information used for the recognition of dispositions and intentions are identity, category of posture, direction of movement, quality of vocalization, and facial expression (Brothers, 1990). According to this definition, emotion recognition and ToM are two core components of social cognition.

Facial expressions signal important information about the internal states of others and the external events that may have elicited those expressions (Ekman, 1997). Individuals use this information to guide their social behavior. Traditionally, the recognition of identity and emotion in human faces involves distinct processes linked by an initial visual processing. Recently, this partition has been shown to be an oversimplified model. The ability to recognize emotions from facial expressions is correlated with affective ToM, or the ability to attribute to others’ mental states, beliefs, intents, and desires. Moreover, the areas of activation of these two components of social cognition overlap.

Section snippets

Cognitive ToM

Pioneering research in 1998 addressed the modularity/domain-specificity debate in a novel way by examining, for the first time, older adults’ performance on ToM tasks (Happé et al., 1998). Two groups of participants, of mean ages 21 and 73 years, were asked to read short stories and answer questions based on their memories of each. Half of these were ToM stories involving double bluffs, mistakes, persuasions, and white lies, and half were control, or non-ToM stories. The ToM stories required

Results in animals

Animal models may provide insight into the neural mechanisms thought to be involved in social cognition and its possible decline with age in humans, although animals do not seem to possess social cognition (i.e., ToM or emotional recognition) as defined and discussed in this review. Behavioral studies in rats indicated that emotional reactivity increases with age, resulting in age-related reduction in social interactions. For example, older rats spent less time in active social interaction than

Pathological ageing and social cognition

Linking specific neurodegenerative pathologies to social cognition deficits may help in the development of a theoretical framework for age-related declines in this ability. On the one hand, the apparent decline in social cognition with normal ageing is, at least partially, independent of a more general cognitive or executive decline. On the other hand, several studies have shown that different brain areas implicated in ToM (see Section 3.2 for a description of such brain areas) are specifically

Conclusions

Several major findings have emerged from studies assessing the effects of ageing on social cognition. First, disturbances in social cognition abilities during the course of normal cognitive ageing are at least partially independent of a more general cognitive decline. Second, brain areas found crucial for the integrity of ToM are specifically affected by neurodegenerative processes in patients with age-related pathologies. Therefore, declines in social cognition in older adults can be linked to

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