Social neuroscience and theory of mind.

Original Paper Folia Phoniatr Logop 2014;66:7–17 DOI: 10.1159/000362877

Published online: November 14, 2014

Social Neuroscience and Theory of Mind Carol E. Westby Bilingual Multicultural Services, Albuquerque, N.Mex., and Brigham Young University, Provo, Utah, USA

Key Words Social neuroscience · Theory of mind · Empathy · Social communication disorders · Epigenetics

This information provides an important framework for assessing ToM deficits in persons with social and communication impairments and developing interventions that target the specific dimensions of ToM deficits. © 2014 S. Karger AG, Basel

© 2014 S. Karger AG, Basel 1021–7762/14/0662–0007$39.50/0 E-Mail [email protected] www.karger.com/fpl

The Diagnostic and Statistical Manual of Mental Disorders, fifth edition [1], included a new diagnostic category, ‘social communication disorder’. Persons with social communication disorder exhibit persistent difficulties in pragmatics or the social use of verbal and nonverbal communication. They exhibit impairments in changing communication to match context or the needs of the listener, difficulties taking turns in conversation, rephrasing when misunderstood, knowing how to use verbal and nonverbal signals to regulate interaction, and difficulty making inferences and understanding figurative language. Effective and appropriate social communication/pragmatic language skills require a theory of mind (ToM). Premack and Woodruff [2] introduced the term ‘theory of mind’, defining it as the ability to impute mental states to oneself and others and to use these observations to make predictions about behaviors of others. The term was rapidly adopted by developmental psychologists. By the late Carol E. Westby, PhD 1808 Princeton NE Albuquerque, NM 87106 (USA) E-Mail mocha @ unm.edu

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Abstract Background: The role of theory of mind (ToM) in autism spectrum disorders and other communication impairments has been an active area of research in the last 30 years. Advances in neuroimaging in the last 10 years have led to the rise of the field of social neuroscience, which has markedly increased the understanding of the neurophysiological/ neuroanatomical and neurochemical nature of ToM functioning and deficits in typically developing individuals and in children and adults with a variety of social and communication impairments. Objective: The goal of this paper is to (a) describe the current concepts of ToM based on neuroscience research, and (b) present a framework for the dimensions of ToM that have been identified, which can be used to guide assessment and intervention for persons with deficits in ToM that affect social interactions. Summary: This article presents neuroscience research that has documented the neurophysiological/neuroanatomical bases for cognitive and affective ToM and interpersonal and intrapersonal ToM as well as neurochemical and epigenetic influences on ToM.

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Folia Phoniatr Logop 2014;66:7–17 DOI: 10.1159/000362877

ronmental, dietary, behavioral and medical experiences can significantly affect the development of an individual (including ToM understanding) and sometimes their offspring. Until the early 2000s, most of the research on ToM was at the behavioral, psychological or cognitive level – how persons performed when given tasks that required them to reflect on the knowledge, thoughts and beliefs of others. With the advent of social neuroscience and epigenetics, an increasing number of studies have investigated the neurophysiological/neuroanatomical and neurochemical functions associated with these behavioral activities and how environmental factors may influence neuroanatomical and chemical functioning. This research has revealed that ToM is not a unitary construct [15–17]. Electroencephalography/event-related potentials, functional magnetic resonance imaging and transcranial magnetic stimulation have provided insights into neural mechanisms underlying the reading of facial and body cues, understanding others, interacting with others, and reflecting on one’s own thoughts and emotions – all components essential for ToM [18, 19]. Results of these studies have documented that variations in ToM activities depend on differing neurophysiological/neuroanatomical and neurochemical underpinnings [20–23]. In investigating ToM, researchers have studied how differing individuals perform a variety of ToM tasks: neurotypical individuals; individuals who have had circumscribed brain insults (strokes, tumors, penetrating wounds); individuals with different diagnoses (autism, schizophrenia, behavioral disorders), and persons of different ages. This research provides evidence for the distinctions among several types or dimensions of ToM. Although there can be overlap in regions of the brain involved in the different types of ToM, specific brain areas are critical for performance of particular types of ToM. This article will describe the dimensions of ToM that have been identified through these studies and the neuroanatomical areas associated with them, and explain the significance of this information for SLPs. See figure 1 that shows a framework for the dimensions of ToM.

Cognitive versus Affective ToM

Over the years, the majority of studies have focused on performance in cognitive ToM tasks. These have investigated a person’s ability to attribute mental states – beliefs, intents, desires, pretending, knowledge, etc. – to oneself Westby


1980s to early 1990s, deficits in ToM became associated with autism [3]. ToM deficits and delays in developing ToM are not limited to those with autism and social communication disorder, however. Deficits in ToM may underlie many of the social communication/pragmatic difficulties exhibited by persons with communication disorders for a variety of reasons (e.g. language impairment, deafness, attention deficit hyperactivity disorder, traumatic brain injury, Parkinson’s disease, dementia), behavioral disorders and psychiatric conditions, as well as children who have experienced abuse and neglect [4–12]. Because social interactional and inferring skills related to ToM deficits are commonly associated with most instances of language impairment in a variety of communicative disorders, it is imperative that speech-language pathologists (SLPs) recognize the dimensions or behavioral variations in ToM and understand the possible neurological underpinnings for these variations. This knowledge can be used to guide assessment and intervention for persons with deficits in ToM that affect social interactions. The majority of studies on ToM have used the definition of Premack and Woodruff [2], developing activities to assess persons’ ability to reflect on what others know, think and believe. ToM, however, extends beyond mentalizing about cognitive processes of knowing, thinking and believing. ToM also involves reflecting on the emotions of oneself and others and appropriately responding to or empathizing with the emotions of others [13]. In the last 20 years, advances in neuroscience have markedly influenced our understanding of the nature of ToM and the fact that there are different types or dimensions of ToM. The field of social neuroscience has emerged in just the last few years. The first issue of the journal Social Neuroscience was published in 2006. The term ‘social neuroscience’, as it is used today, first appeared in an article by Cacioppo and Bertson [14] who proposed that social psychology and neuroscience represent two ends of a continuum of levels of organization studied in psychology. Understanding social behaviors must acknowledge research demonstrating both that (a) neurophysiological/ neuroanatomical/neurochemical events influence social processes and (b) social processes influence neurophysiological/neuroanatomical/neurochemical events. Recent work in epigenetics is demonstrating how environmental factors influence gene expression. Epigenetics is the study of heritable changes in gene activity that are not caused by changes in the DNA sequence. The first issue of Epigenetics and Chromatin was published in 2008. Epigenetic discoveries reveal that social factors such as envi-

ToM

Recognizing thoughts and emotions of others

Cognitive

Affective Affective cognitive Affective empathy

Interpersonal/ social

Interpersonal/ reflective

Making inferences about behaviors, thoughts and emotions of others

Responding empathically to others

Reflecting on one‘s own thoughts and emotions

Planning and regulating one‘s own behaviors/ emotions

and others and to understand that others have beliefs, desires and intentions that are different from one’s own. Neuroscience studies have shown that attributing emotional states to oneself and others involves some different neuroanatomical areas than attributing mental states to oneself and others. The ability to attribute or understand the emotions of oneself and others and share affective states is termed affective ToM [16]. Affective ToM has two components: an affective cognitive component (sometimes termed cognitive empathy) that involves an awareness or recognition of the feelings of others and an affective empathy (emotional empathy) component that involves the ability to experience the emotions of others. Affective empathy is elicited by the perceived, imagined or inferred affective state of another and includes some cognitive appreciation of the other’s affective state comprising perspective taking, self-other distinction and knowledge of the causal relation between the self and the other’s affective state [23]. Affective empathy includes some metaknowledge about self and the other that distinguishes it from emotional mimicry and emotional contagion. Emotional mimicry is defined as automatic synchronization of emotional behavior, for example affective expressions, vocalizations, postures and movements with those of another person [23]. Emotional contagion occurs when people experience emotions similar to those of others by mere association, for example when you feel happy because others around you feel happy, or when you are

panicking because you are in a crowd of people feeling panic [23]. Emotional mimicry and contagion require neither perspective taking nor an explicit self-other distinction. It can be difficult to know whether a person is really experiencing affective empathy or is instead displaying emotional mimicry or emotion contagion. Both cognitive and affective ToM have several levels of development. First-order ToM, which develops between 4 and 5 years of age, involves thinking about what someone else is thinking or feeling. Second-order ToM, which in typically developing children develops shortly after first order, involves thinking about what someone is thinking or feeling about what someone else is thinking or feeling. Beyond second-order ToM, higher-order cognitive and affective ToM involve tasks that require recognizing that what is said is not what is literally meant (e.g. lies, sarcasm, figurative language, idioms) or following multiple embeddings (e.g. he thinks that she hopes that they believe she loves the gift). These skills are typically developing between 8 and 12 years of age [24]. Evidence for the neural bases of cognitive and affective ToM has come from two sources: functional imaging studies of normal participants and patients with brain injuries. Shamay-Tsoory and colleagues [20, 25–27] have probably the most extensive set of studies on the neuroanatomical bases of cognitive and affective ToM. In several studies they have asked participants to judge mental or emotional states based on verbal and eye gaze cues of

Social Neuroscience


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Fig. 1. Types of ToM.

TPJ IFG er Lat

ulc al s

us

STS

OFA

TP

PCun

PCC MCC

dACC

dMPFC

vACC vMPFC FFA

OFC

Fig. 2. Brain areas involved in ToM. Cognitive ToM is associated with: dACC (dorsal anterior cingulate cortex); dLPFC (dorsal lateral prefrontal cortex); dMPFC (dorsal medial prefrontal cortex); STS (superior temporal sulcus); TPJ (temporal parietal junction). Affective ToM is associated with: IFG (inferior frontal gyrus); OFA (occipital facial area); OFC (orbital frontal cortex); vMPFC (ventromedial prefrontal cortex). Intrapersonal ToM is associated with: PCun (precuneus); PCC (posterior cingulate cortex); MCC (middle cingulate cortex); vMPFC (ventromedial prefrontal cortex); vACC (ventral anterior cingulate cortex). Facial processing is associated with: OFA (occipital facial area); FFA (fusiform facial area); STS (superior temporal sulcus).

a cartoon figure. The task consists of 64 trials, each showing a cartoon outline of a face (named ‘Yoni’) and 4 colored pictures of objects belonging to a single category (e.g. fruits, chairs) or faces, one in each corner of the computer screen. The participant’s task is to point to the image to which Yoni is referring, based on a sentence that appears at the top of the screen and available cues, such as Yoni’s eye gaze, Yoni’s facial expression or the eye gaze and facial expression of the face to which Yoni is referring. There are two main conditions: ‘cognitive’ and ‘affective’, requiring either a first-order or a second-order inference. In the cognitive conditions, both Yoni’s facial expression and the verbal cue are emotionally neutral, whereas in the affective conditions, both cues provide af10


Westby


dLPFC

fective information [i.e. Yoni is thinking of (cognitive condition) vs. Yoni loves (affective condition)]. While the cognitive condition requires understanding beliefs about others’ beliefs and desires (Yoni is thinking of the toy that ... wants), the affective condition involves understanding of one’s emotions in regard to the others’ emotions (Yoni loves the toy that ... loves). Shamay-Tsoory et al. [27, 28] have also developed a variety of vignette tasks that require participants to employ cognitive or affective ToM. For example, participants respond to questions about vignettes that require them to interpret sarcasm (e.g. cognitive ToM – a man walks into a very messy office and says: ‘You’re office is so tidy.’ – or affective ToM – a father forgets to pick up his son after school, leaving him in the rain for some time. When the father and son finally get home, the mother says to the father: ‘You are such a good father.’). Performing tasks that require participants to mentalize about people’s thoughts and beliefs (cognitive ToM) consistently result in activation of the temporal parietal junction (TPJ), the dorsal lateral prefrontal and dorsal medial prefrontal cortex (PFC), and the dorsal anterior cingulate cortex [20, 29–32]. When mentalizing about people’s emotions (affective cognitive ToM), the TPJ is also involved, but in addition, the orbital frontal cortex, the inferior lateral frontal gyrus, the ventral medial PFC and ventral anterior cingulate cortex are activated [13, 16, 20, 25–27, 33] (fig. 2). These areas have direct connections into the insula cortex (which is folded deeply within the lateral sulcus), the midcingulate cortex and the amygdala which are involved in affective or emotional empathy. The ventral medial PFC is an important relay station between cognitive and affective processing [13]. Affective cognitive ToM and affective empathy ToM involve somewhat different neuroanatomical structures. To explore this, Shamay-Tsoory et al. [32] compared the performance of persons with lesions in the ventral medial PFC or the IFG with two control groups – a healthy group and a group with lesions outside the frontal lobes – on tasks measuring emotion recognition, second-order false belief, and affective cognitive and emotional empathy. The researchers administered the Interpersonal Reactivity Index [34] which measures both components of empathy. Participants rated each item of the Index in terms of how well it described them. Examples of affective cognitive items are ‘When I am reading an interesting story or novel I imagine how I would feel if the events in the story were happening to me’ or ‘I try to look at everybody’s side of a disagreement before I make a decision’. Examples of affective empathy items are ‘I am often quite

touched by things that I see happen’ or ‘When I see someone being taken advantage of, I feel kind of protective towards them’. The researchers found subjects with lesions in the ventral medial PFC to be specifically impaired in affective cognitive ToM (cognitive empathy) whereas patients with inferior frontal gyrus lesions were specifically impaired in affective empathy and emotion recognition. Experimental evidence suggests that motor simulation may be a trigger for the simulation of associated feeling states or affective empathy. Researchers have hypothesized that the mirror neuron systems may be involved in emotional mimicry or contagion which can then trigger empathic emotional experiences [35]. The discovery of mirror neurons [36, 37] provided new insights into possible explanations for the ability to imitate and to empathize. A mirror neuron is a neuron that fires both when an animal acts and when the animal observes or hears the same action performed by another; hence, it acts as a bridge between the self and the other. Mirror neurons respond not just to the motor properties of an action but also to the goal of the action. If an action is the same (e.g. grasping), but the goal is different (to put food into a container or to eat the food), different mirror neurons respond [38]. Thus, the neuron ‘mirrors’ the behavior or intent of the other, as though the observer were itself acting. There are both visual and auditory mirror neurons [39]. Researchers who support a simulation theory explanation of ToM maintain that mirror neurons can explain the early development of affective ToM [40–43]. Mirror neurons have been interpreted as the mechanism by which we simulate others in order to better understand them, and therefore their discovery has been taken by some as a validation of simulation theory. According to simulation theory, ToM is activated because we subconsciously empathize with the person we are observing and, accounting for relevant differences, imagine what we would desire and believe in that scenario. Researchers [35, 40, 41] have argued that the mirror neuron system is involved in empathy. A large number of experiments using functional MRI, electroencephalography and magnetoencephalography have shown that the anterior insula, anterior cingulate cortex and inferior frontal cortex are active when people experience an emotion (disgust, happiness, pain, etc.) and when they see another person experiencing an emotion [44–46]. Keysers and Gazzola [42, 43] have shown that people who are more empathic according to self-report questionnaires have stronger activations both in the mirror system for hand actions and the mirror system for emotions, providing more direct support for the idea that the mirror system is linked to empathy.

Although mirror neurons may have a role in empathy, they are not necessary for empathy. Walter [23] suggested that there are two possible roads to affective empathy, a low road and a high road. For the low road, features indicating affective states or suffering (facial expressions, body movements, blood or injuries) might trigger emotional contagion and mimicry (via the mirror neurons) and lead more or less to automatic empathic responding in a bottom-up manner. With the high road to empathy, empathic responses are induced topdown by higher cognitive processes. The observer draws inferences about the thoughts and feelings of another, based on contextual or situational information, for example knowing that a friend wrecked his new car or that your brother just won a scholarship. The cognitive understanding of the situation (dependent on the TPJ, superior temporal sulcus, dorsal lateral and dorsal medial PFCs) can lead to affective empathy (dependent on the inferior frontal gyrus, amygdala and insula) via the ventromedial PFC.

Social Neuroscience


Facial Processing

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Interpersonal ToM, particularly affective ToM, makes use of reading faces and bodies when making inferences about others. Three regions of the brain are involved in this: the occipital face area, the fusiform face area and the superior temporal sulcus [47]. The occipital face area is located in the inferior occipital gyrus. It is an early stage in perceptual analysis of faces that sends inputs to the fusiform and superior temporal regions. It shows greater functional MRI response to faces relative to other categories. The occipital face area activity is sensitive to any physical change in the stimulus [48]. The fusiform face area responds to faces more than other stimuli and is particularly important for recognizing familiar faces [49]. The superior temporal sulcus responds to changeable aspects of a face, particularly poses and gaze directions, whereas the fusiform face area responds to stable aspects of the face (the person’s identity) [47]. These changeable aspects are particularly important for extracting social cues that are likely to be fleeting [50]. Lesions in these areas disrupt facial processing. Although dozens of studies have reported that face and emotion recognition are impaired in people with autism spectrum disorders [51], these deficits do not appear to be due to functioning of these visual areas. Some reports have indicated that persons with autism have less activation of the fusiform area when processing faces, but this

Table 1. Interpersonal and intrapersonal ToM

Interpersonal ToM

Intrapersonal ToM

Cognitive

Mary plays a trick on Sam, whose favorite snack is M&M’s. Mary puts M&M’s in a toothpaste box and puts the box on Sam’s table. What will another kid think is in the box before opening it? What did Sam think was inside the toothpaste box before opening it?

Ask child if he/she prefers for a snack M&M’s or toothpaste. C. says M&M’s and is then handed a wrapped box. C. unwraps and sees toothpaste box. C. opens box and finds M&M’s. What does it look like is in the box? What is really in the box? What did you think was inside the toothpaste box before opening it?

Affective

How did Sam feel about what was inside the box before opening it?

How did you feel about what was inside the box before opening it?

Interpersonal versus Intrapersonal ToM

Cognitive and affective ToM can be either interpersonal, which involves recognizing thoughts and emotions of others and making inferences about them, or intrapersonal, which involves having a sense of self, reflecting on one’s own thoughts and emotions, regulating one’s emotions, and using this information to learn and plan. Lucariello et al. [55] compared the development of interpersonal and intrapersonal ToM by asking children to respond to vignettes that required cognitive and affective reflection on others or on oneself (table 1). 12


Researchers have used neural imaging to investigate neural functioning in a variety of self-referential tasks involving verbal, spatial, social, emotional or memory processing [22]. For example, persons see single words describing personality traits (e.g. lazy, talkative, ambitious) and judge if the trait is true of a famous person or of themselves [56]. For example, Jenkins and Mitchell [57] had participants evaluate adjectives for how well they described either themselves or the then-current US President, George W. Bush. Three different sets of adjectives referred to (a) stable personality traits (e.g. in general, how brave?); (b) current mental states (e.g. at the moment, how bored?), and (c) stable physical attributes (e.g. physically, how tall?). Kana et al. [54] had high functioning adults with autism and neurotypical adults make yesno decisions about whether visually presented adjectives (e.g. smart, unhappy) described themselves (self-judgment) or their favorite teacher (other-judgment). British researchers Lombardo et al. [58] had neurotypical adults make mental reflections about themselves or the Queen. On the self task, participants judged on a scale from 1 (not at all likely) to 4 (very likely) how likely they themselves would personally agree with opinion questions (e.g. ‘How likely are you to think that keeping a diary is important?’). On the other task, the same mentalizing judgments were made, except this time they were in reference to how likely the British Queen would agree with the opinion questions (e.g. ‘How likely is the Queen to think that keeping a diary is important?’). Vogeley et al. [59] asked participants to count the number of balls seen from the perspective of an avatar in a scene or from their own perspective. There is considerable overlap of neural areas that process both self- and other-reflection, but there is also some specificity. A meta-analysis of imaging studies on self-reflection provided significant support that cortical midline Westby


appeared to be related to the fact that they were not attending to eyes in the stimuli. When compelled to visually scan faces, functioning of the fusiform area normalized [52]. Instead, these facial processing deficits in autism spectrum disorders seem more likely to be due to underconnectivity between the posterior facial recognition areas and anterior frontal areas, particularly the medial prefrontal area responsible for interpretation of the facial information. There is evidence from diffusion tensor imaging that children with autism show areas of decreased white matter integrity [53]. Specifically, reduced white matter connectivity has been found between the fusiform face area and frontal area and the posterior superior area and medial frontal area [54]. This underconnectivity between frontal and posterior cortical areas constrains the psychological processes that rely on integrated functioning of frontal and posterior brain networks. Thus, it may be that persons with autism spectrum disorder perceive the visual information similarly to those without autism spectrum disorder, but that they fail to interpret the information appropriately.

Neurochemistry and Genetics

Abu-Akel and Shamay-Tsoory [20] maintain that neuroanatomical models for ToM cannot fully explain how various pathologies that present with differing neurobiological abnormalities such as autism or reactive attachment disorder (autistic-like problems in social relatedness found in children who experienced neglect or maltreatment in infancy [61]) exhibit similar ToM dysfunctions or how persons with a single disease such as parkinsonism exhibit differing profiles of cognitive and affective ToM impairments [62, 63]. To explain these variations, Abu-Akel and Shamay-Tsoory [20] suggest considering the neurochemical basis of ToM. It has been hypothesized that the dopaminergic-serotonergic system has a role in ToM. This is based on the observations that ToM dysfunctions are frequent consequences of disorders that are associated with deficits in the dopaminergicserotonergic system such as autism [64, 65] and schizophrenia [66] and that the dopaminergic-serotonergic system innervates the PFC, the TPJ and the anterior cingulate cortex, regions that are critical for ToM. Genetic variation influences production and metabolism of neurotransmitters, which in turn affects ToM performance. The dopamine receptor DRD4 gene variation predicts preschoolers’ developing ToM [67] and it moderates infants’ sensitivity to maternal affective communications [68]. Neurotypical children with the short allele Social Neuroscience

variant of the DRD4 gene perform better on ToM tasks than children with the long allele variant. However, infants with the short variant of the DRD4 gene were more affected by disrupted maternal communication, having more disorganized attachments that could potentially later result in lower ToM. Oxytocin plays a role in how we perceive our own and other’s emotional states. Oxytocin increases sociability and emotional empathy [69]. In contrast to persons with 1 or 2 copies of the G allele for the oxytocin receptor gene (OXTR), persons with 1 or 2 copies of the A allele have exhibited lower dispositional empathy as measured by their ratings on the Interpersonal Reactivity Index [34] and lower behavioral empathy as measured by their scores on ‘Reading the Mind in the Eyes’ test that required them to interpret emotions from eyes [70]. Variants of the OXTR gene have been associated with autism [71, 72]. Monoamine oxidases are enzymes that are involved in the breakdown or inactivation of neurotransmitters such as serotonin and dopamine and are, therefore, capable of influencing feelings, mood and behavior of individuals. The monoamine oxidase A gene (MAOA) is involved in neural circuitry between the ventromedial frontal cortex and the amygdala, regions implicated in social behavior, ToM and empathy. The low-activity MAOA genotype has been associated with antisocial behavior, particularly in persons who have experienced abuse during childhood [73]. Maltreated children with genotypes causing high levels of MAOA are less likely to develop antisocial behavior [74]. Environmental factors can affect neurochemical functioning and, as a consequence, neuroanatomical development. For example, neglected and maltreated children are exposed to high stress levels in infancy and early childhood, and as a result, tend to have high ongoing levels of cortisol. Chronic high levels of cortisol affect brain functioning and development [75]. Maltreated children have been found to have smaller brain volumes in the orbital frontal cortex [76], critically important in affective ToM. Children who have been reared in institutions in their early years have a significantly smaller cortical gray matter volume [77]. Recent work in developmental neuroscience and epigenetics is offering suggestions for how early life experiences and environmental influences interact directly with genes in the developing brain. Epigenetics is the study of heritable changes in gene activity that are not caused by changes in the DNA sequence. Studies are showing how epigenetic mechanisms that regulate gene activity in the central nervous system are modified by experiences, particularly those occurring within the context Folia Phoniatr Logop 2014;66:7–17 DOI: 10.1159/000362877

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structures, a set of regions in the midline of the cortex arching around the corpus callosum, are involved in intrapersonal ToM activities (self-referential processing) [22]. The cortical midline structures (constituting the medial PFC, the anterior, middle and posterior cingulate cortices, and the precuneus) are thought to functionally integrate self-related thought and planning [22]. The cortical midline structures may mediate the evaluative and self-reflective aspects of the self, ToM may help understand the mental states of oneself and others, and the mirror neuron system may help to self-simulate the actions of the other to understand goals and intentions. Ramachandran [60] speculated that mirror neurons may provide the neurological basis of human self-awareness or intrapersonal ToM. He hypothesizes that these neurons can not only help simulate other people’s behavior, but can also be turned inward to create metarepresentations of your own earlier brain processes. This could be the neural basis of introspection, and of the reciprocity of self-awareness and awareness of others.

Implication/Conclusions

ToM deficits lie at the heart of autism and are major contributors to social communication/pragmatic language difficulties exhibited by children and adults with a wide variety of conditions. ToM is not a unitary construct. In the last 15 years, neuroimaging studies have provided evidence of distinctive dimensions of ToM. Cognitive ToM, affective cognitive ToM and affective empathy have differing neuroanatomical foundations. Furthermore, thinking about the thoughts or emotions of others (interpersonal ToM) and reflecting on one’s own thoughts and emotions (intrapersonal ToM) involve differing neuroanatomical structures. McPartland and Pelphrey [79] suggest that findings from social neuroscience could be used to define subgroups of persons with disabilities with particular profiles. Researchers and clinicians could then work together to determine which profiles respond best to particular interventions. Using the cognitive and affective ToM framework, Baron-Cohen [4] has described ToM profiles in persons with a variety of psychiatric disorders as well as classic autism and Asperger syndrome. Clinicians working with persons with social communication/pragmatic communication disorders should consider evaluating these dimensions of ToM in their clients and developing a ToM profile for each client so they are better able to implement specific interven14


tion strategies to target the linguistic and cognitive/affective foundations for ToM development. Hutchins and Prelock [80] are developing a standardized assessment for children for some aspects of first-order and second-order cognitive and affective ToM. The Awareness of Social Inference Test, developed by Rollins, Flanagan and McDonald for adolescents and adults who have experienced traumatic brain injury, assesses primarily higher-order affective ToM [81, 82]. Although a number of tests that assess pragmatics and emotional understanding incorporate tasks that do require ToM, none of these tests distinguish among the dimensions of ToM nor do they link test items to levels of ToM processing. This information is critical if SLPs and educators are to design effective programs to promote social communication/ pragmatic development. The goal is not to teach students to pass ToM tasks but to use the information from the assessment of ToM to teach the interactional, linguistic and social/emotional cognitive skills that underlie ToM performance. Teaching skills underlying cognitive ToM may have little effect on the development of a person’s skills underlying affective ToM, and developing skills for intrapersonal cognitive ToM (such as learning strategies and decision making) may have little effect on intrapersonal affective ToM skills (such as awareness of one’s own emotional states and regulation of those states). SLPs can make use of protocols that are described in research articles to assess cognitive ToM [83, 84] and affective ToM [27, 85]; then using the data gathered, they can review materials designed to develop social communication/ pragmatic skills, selecting those activities that address clients’ specific needs. For example, to promote interpersonal cognitive ToM, one would want to ensure that students comprehend and use a variety of mental state words (think, remember, forget, believe, decide, plan, intend, predict) and complement structures (Gracee thought she had turned in her homework. She forgot she had given it to her mother to check) [86], and one might use thought bubbles over characters showing what they are saying, but also what they are really thinking [87]. To promote interpersonal affective ToM, one might use computer programs that have been shown to improve emotion recognition [88] or strategies using situational contextual cues, visual body cues and knowledge of the persons involved to interpret the emotions of others [89]. To promote intrapersonal affective ToM, one can teach strategies for emotion regulation – identifying one’s body cues for positive and negative emotions and employing strategies to change one’s emotions [90]. The think-aloud strategy can promote cognitive intrapersonal ToM as students are Westby


of caregiving [78]. Environmental experiences can result in special chemicals called tags (epigenomes) becoming attached to our genes, and, depending on the nature of these tags, specific genes can either be silenced (prevented from being expressed as protein) or pushed to become more active. These epigenetic changes may last through cell divisions for the duration of the cell’s life and may be inherited for multiple generations. When these epigenomic chemicals become attached to genes controlling neurotransmitters, ToM abilities can be disrupted. These epigenetic changes in combination with particular genotypes may explain why some children reared in abusive or neglectful backgrounds appear to develop relatively well, while others exhibit deficits in ToM and social skills and are at greater risk for a variety of health problems. Children with the short variant of the DRD4 dopamine receptor gene, the low-activity MAOA gene, or the AA or AG allele of the oxytocin gene are likely to have significant social and behavioral difficulties if they experience maltreatment in early childhood but not if they are reared in healthy, supportive environments.

taught to reflect on whether they are understanding or not what they are reading and what they could do to promote comprehension [91]. The developing research in genetics and epigenetics along with the documented neuroanatomical and behavioral effects of early abuse and neglect provide SLPs with data to influence social policy. Children who live in neglectful/abusive environments are at risk for having ToM deficits and behavioral and social communication difficulties related to these deficits. These deficits are especially likely if children carry particular genotypes. In many states in the USA, young children are only eligible for free preschools or intervention services if their performance in standardized tests is markedly below the mean for children their age. This requirement results in their receiving services only after the damage has been done.

Although some epigenetic changes may be reversed, Perry [92], director of the Child Trauma Academy (http:// childtrauma.org/), claims that children who have experienced abuse and neglect are malleable – they can change – but they will never be the children they would have become if they had not had these negative experiences. Research shows that the brain has a critical window for language development between the ages of 2 and 4. Brain circuits associated with language are more flexible before the age of 4, and environmental influences have their biggest impact before the age of 4. Consequently, early intervention for children should be initiated before this critical age [93]. SLPs can be in position to advocate for policy changes to promote the mental health and language development of at-risk children.

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The social neuroscience and the theory of integrative levels.

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Loneliness and social neuroscience.

Executive functions and theory of mind as predictors of social adjustment in childhood traumatic brain injury.

Theory of Mind, Social Desirability, and Unlikely Symptom Reporting in Offenders With and Without Psychopathy.

Action mechanisms for social cognition: behavioral and neural correlates of developing Theory of Mind.

Children's strategic theory of mind.

The neural basis of theory of mind and its relationship to social functioning and social anhedonia in individuals with schizophrenia.

Psychiatry and social nutritional neuroscience.

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How cognitive theory guides neuroscience.

Theory of mind and social functioning in patients with temporal lobe epilepsy.

Social anxiety disorder exhibit impaired networks involved in self and theory of mind processing.

Social cognition in ADHD: irony understanding and recursive theory of mind.

In others' shoes: do individual differences in empathy and theory of mind shape social preferences?

Deconstructing and reconstructing theory of mind.

Insight and theory of mind in schizophrenia.

Plans, Habits, and Theory of Mind.

Hot baths and cold minds: neuroscience, mind reading, and mind misreading.

Green Mind Theory: How Brain-Body-Behaviour Links into Natural and Social Environments for Healthy Habits.

A teacher-centered exploration of the relevance of social factors to theory of mind development.

Autistic social dysfunction: some limitations of the theory of mind hypothesis.

A decade of theory of mind research on Cayo Santiago: Insights into rhesus macaque social cognition.