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Clinical assessment of social cognitive


function in neurological disorders
Julie D. Henry1, William von Hippel1, Pascal Molenberghs2, Teresa Lee3
and Perminder S. Sachdev3
Abstract | Social cognition broadly refers to the processing of social information in the brain
thatunderlies abilities such as the detection of others emotions and responding appropriately
tothese emotions. Social cognitive skills are critical for successful communication and,
consequently, mental health and wellbeing. Disturbances of social cognition are early and salient
features of many neuropsychiatric, neurodevelopmental and neurodegenerative disorders, and
often occur after acute brain injury. Its assessment in the clinic is, therefore, of paramount
importance. Indeed, the most recent edition of the American Psychiatric Associations Diagnostic
and Statistical Manual for Mental Disorders (DSM5) introduced social cognition as one of six
core components of neurocognitive function, alongside memory and executive control. Failures
of social cognition most often present as poor theory of mind, reduced affective empathy,
impaired social perception or abnormal social behaviour. Standard neuropsychological
assessments lack the precision and sensitivity needed to adequately inform treatment of
thesefailures. In this Review, we present appropriate methods of assessment for each of the four
domains, using an example disorder to illustrate the value of these approaches. We discuss the
clinical applications of testing for social cognitive function, and finally suggest a five-step
algorithm for the evaluation and treatment of impairments, providing quantitative evidence
toguide the selection of social cognitive measures in clinical practice.

Humans are inherently social creatures. Social behav- many neurological disorders, such as Alzheimer disease
iours emerge in the early stages of infancy1 and remain (AD), Parkinson disease and multiple sclerosis, social
critical throughout the lifespan2,3. Much of our everyday cognitive disturbances might be relatively subtle and
behaviour is motivated by social and emotional goals; harder to detect informally. Structured social cogni-
1
School of Psychology, indeed, the disproportionately large size of the human tive assessment is, therefore, useful in a wide range of
University of Queensland, brain might be the result of evolutionary pressures to neurological conditions. In patients with acute brain
StLucia, Queensland 4072, negotiate complex social systems4. For this reason, social trauma, or if a patients history or diagnosis could indi-
Australia. cognitionthe means by which we perceive, process cate social cognitive dysfunction, social cognitive assess-
2
School of Psychological
Sciences and Monash
and interpret social informationis a fundamental ment should be part of the initial standard neurological
Institute of Cognitive neurocognitive capacity. A critical role for social cog- examination. Even if no impairment is identified, such
&Clinical Neurosciences, nition in functional disability is now well established: assessment should be included in routine followup in
Monash University, social cognitive impairment has been linked to poor neurological disorders that are associated with social
Melbourne, Victoria 3800,
quality of life, mental health problems, unemployment cognitiveimpairment.
Australia.
3
Centre for Healthy Brain and loneliness57. Failures of social cognition most often present clin-
Ageing, School of Psychiatry, Nearly all neurological disorders that affect the ically in one or more of four ways: impaired theory of
University of New South brain have the potential to disrupt social cognitive mind (ToM), reduced emotional empathy, poor social
Wales, Prince of Wales function. Social cognitive impairment can be a prom- perception, and abnormal social behaviour. ToM refers
Hospital, Randwick, New
South Wales 2031, Australia.
inent clinical symptom after acute brain damage, such to our ability to understand the mental states of others,
Correspondence to J.D.H. as traumatic brain injury or stroke, and can be a core and to appreciate that these mental states might differ
julie.henry@uq.edu.au feature of the early stages of some chronic neurological from our own. Affective ToM requires an understand-
doi:10.1038/nrneurol.2015.229 disorders, such as behavioural-variant frontotemporal ing of others emotions, affective states or feelings (and
Published online 16 Dec 2015 dementia (bvFTD)8. However, in the early stages of overlaps with the construct of cognitive empathy),

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Key points deficits fundamentally disrupt the ability to make sense


of social interactions and respond appropriately. Indeed,
Social cognitive deficits are prominent in many conditions and are critical predictors impairments of social behaviour often arise as a direct
of functional outcomes because they affect the ability to form and sustain consequence of social perceptual failures, such as when
interpersonal relationships social cues have been missed or misinterpreted. Social
Assessments of social cognitive impairments typically focus on theory of mind, behavioural abnormalities include poor social tact, a
affective empathy, social perception and social behaviour, four domains that all lack of manners, interpersonal boundary infringements,
influence the management of a patient
reduced use of communicative gestures and unsolicited
Many social cognitive assessment measures that are appropriate for clinical use are affiliative contact with strangers (BOX1).
now available and should form part of a broader neurocognitive battery
In this Review, we consider the clinical contexts in
Common disorders that manifest with prominent social cognitive deficits which social cognitive dysfunction arises, and the neuro
includeschizophrenia, autism spectrum disorders, Alzheimer disease, and
biological basis for this dysfunction. We then consider
behavioural-variant frontotemporal dementia
how this dysfunction is best assessed, presenting exam-
A range of effective treatment strategies are currently available, so the nature, ple disorders in which a specific social cognitive domain
magnitude and specificity of social cognitive impairments each have important
should be tested, and the tests that can be used to meet
implications for therapeutic decision-making
the clinical needs of patients with such a dysfunction.
Finally, we consider the broader use of these tests in the
whereas cognitive ToM requires an understanding of clinic, and future directions in this area.
others cognitive states, beliefs, thoughts or intentions.
Affective empathy is ones emotional response to the Social cognition in clinical contexts
perceived situations of others. These responses can be Arguably, most psychiatric and neurological illnesses are
experienced as the same emotions that the other per- associated with some level of social cognitive impair-
son feels (an empathic response that is often referred ment that has the potential to disrupt interpersonal
to as affective resonance or experience sharing), or can relationships8. Illnesses that are known to involve social
be distinct from the experience of others, for example if cognitive impairment range from disorders in which
we feel embarrassed for someone who is overconfident9. social cognitive deficits are core diagnostic criteria, such
Emotional responses that are primarily self-oriented as bvFTD and autism spectrum disorders (henceforth
rather than other-oriented, such as personal distress, referred to as autism), to disorders in which social diffi-
are not empathic responses. By allowing us to under- culties are often a prominent concern, such as Parkinson
stand others mental states and experience their emo- disease and AD (BOX2).
tions, ToM and affective empathy have an important
role in prosocial behaviour, inhibition of aggression and Neurobiological basis
moral reasoning. Failures of social perception typically Neuroanatomical disturbances
manifest as problems with recognizing and responding Distinct disturbances of social cognition and function
to basic social and emotional cues, such as interpreting have been linked to abnormalities in specific neural
facial expressions, body language or voices, or respond- regions. For example, lesions in the orbitofrontal cortex
ing to social cues, such as eye gaze. Social perceptual (OFC) are associated with disinhibited behaviours, such
as social inappropriateness, hypersexuality and compul-
sive gambling10. This association is believed to reflect
Box 1 | Indications of social cognitive impairment
the critical role of the OFC in reinforcement-guided
Social withdrawal or avoidance of social contact decision-making11. Lesions in the anterior cingulate cor-
Loss of social graces tex (ACC) are associated with behavioural disturbances
Limited eye contact that include abulia, or its more severe form akinetic
Rude or offensive comments without regard for the feelings of others mutism, reflecting the ACCs involvement in regulat-
Loss of etiquette in relation to eating or other bodily functions ing motivational and emotional behaviour12. Damage
to thetemporoparietal junction has been shown to dis-
Extended speech that generally lacks focus and coherence
rupt the ability to view a situation from an another per-
Neglect of personal appearance (in the absence of depression)
sons perspective, and has also been linked to abnormal
Disregard of the distress or loss of others moral reasoning13,14. These disturbances are believed to
Inability to share in the joy or celebrations of others when expected or invited arise because the temporoparietal junction has a central
Failure to reciprocate socially, even when obvious social cues are given role in integrating social, attentional, memory and lan-
Poor conversational turn-taking guage processing streams to construct a social context
Overtly prejudicial or racist behaviour forbehaviour15.
Increased or inappropriate interpersonal boundary infringements The ubiquity of social cognitive difficulties among
Failing to understand jokes or puns that are clear to most people
clinical populations is unsurprising given that substan-
tial overlapping and interacting functions exist across
Failure to detect clear social cues, such as boredom or anger, in conversational
brain regions and that evidence shows that social cog-
partners
nition imposes demands on a large number of differ-
Lack of adherence to social standards of dress or conversational topics
ent brain structures and their connectivity8. Specific
Excessive focus on particular activities to the exclusion of important social or brain regions are consistently implicated in each of
occupational demands
the four social cognition networks (FIG.1), but overlap

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exists between the areas involved in the four networks. Box 2 | Disorders with social cognitive impairment
Furthermore, many other brain areas are also impli-
cated, and these areas are involved in other functions in Psychiatric disorders
addition to social cognition. Schizophrenia
Deficits of social cognition can result from damage Bipolar disorder
to the brain regions involved in such cognition or their Antisocial personality disorder
connections, and should be understood as a disrup- Major depressive disorder
tion of the interactions within and between large-scale Post-traumatic stress disorder
social cognition networks. The functional integrity Social phobia
of these networks can be disrupted by relatively mild
Anorexia nervosa
dysfunction in one structure that is involved, diffuse dys-
function or white-matter damage8. Alternative sources Personality disorders (for example, borderline,
antisocial, narcissistic, schizoid, avoidant)
provide excellent, detailed descriptions of the specific
brain regions involved in ToM 16, empathy17, social Developmental disorders
perception18, and social behaviour12. Autism spectrum disorder
Fragile X syndrome
Neurotransmitter disturbances Williams syndrome
Functional abnormalities in neurotransmitters, such Angelman syndrome
as serotonin, aminobutyric acid (GABA) and dopa- PraderWilli syndrome
mine, have also been linked to social cognitive dys- Turner syndrome
function19. The relationship between neurotransmitter
Rett syndrome
levels and cognitive functioning generally follows the
YerkesDodson law, and is best described by an inverted Attention deficit hyperactivity disorder
U: optimal function requires neurotransmitter levels to Severe conduct disorder
be neither too low nor too high. Experimental mani Fetal alcohol syndrome
pulation of neurotransmitter levels with, for example, Neurodegenerative disorders
acute tryptophan depletion (which decreases CNS lev- Frontotemporal dementia
els of serotonin) or drugs such as sulpiride (a dopamine Alzheimer disease
antagonist) or diazepam (a GABAA receptor modulator Amyotrophic lateral sclerosis
that increases the effects of GABA) influences social
Parkinson disease
cognitivefunction2022.
Huntington disease
The neuropeptides oxytocin and vasopressin, both of
which exert widespread neuromodulatory effects, have Progressive supranuclear palsy
a particularly critical role in social cognition and behav- Corticobasal degeneration
iour19,23. Behavioural studies have shown that higher Multiple sclerosis
peripheral levels of oxytocin correlate with more positive Acute brain damage
social behaviour24,25. In addition, variations in the genes Traumatic brain injury
that encode these social neuropeptides have been linked Stroke
to individual differences in aspects of social behav-
iour, such as empathy26, prosociality27 and autistic-like
traits28, and to heritable disorders, including autism29. In order to facilitate clinical decision-making, in the
Furthermore, intranasal administration of oxytocin and following sections we present four example disorders
vasopressin has been shown to influence socioemotional to illustrate the appropriate methods of assessment for
function30, a finding that underlies considerable interest impairment of each domain of social cognition: poor
in the potential therapeutic use of these agents31. ToM, reduced affective empathy, impaired social per-
ception and abnormal social behaviour. Important to
Clinical assessment of social cognition keep in mind, however, is the fact that many clinical
The clinical assessment of social cognitive function disordersincluding all four examples presented in
is important in many neurological disorders, includ- this Reviewinvolve impairment in multiple social
ing acute brain trauma, such as stroke and traumatic cognitive domains.
brain damage, and chronic neurological disorders, Measures were selected on the basis of either their
such as AD and Parkinson disease. This importance wide use in clinical practice, or their potential advan-
is now formally recognized in the fifth edition of the tages over more commonly used measures. Measures
Diagnostic and Statistical Manual for Mental Disorders that are known to have good reliability and clinical
(DSM5)32, which includes social cognition as one of sensitivity were prioritized. The inclusion of an appro-
six core neurocognitive domains. Standardized tests priate control was also an important consideration in
are essential for objective quantification of the extent test selection because deficits of social cognition can
and severity of impairment and for the identification of be secondary to other cognitive deficits rather than the
the strongest residual abilities that can be used to com- result of a primary disturbance; fully understanding
pensate for deficits, yet the DSM5 does not name any the origin and specificity of the deficit is necessary for
proprietarytests. making appropriate therapeutic decisions. Most clinical

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a Theory of mind b Empathy relationships with family and friends, disengagement


Dorsomedial Dorsal anterior
from socially important activities, such as work and
prefrontal cingulate cortex study, and poor selfcare. These clinical symptoms
cortex and behavioural abnormalities are believed to reflect a
Temporoparietal
junction disorder of brain network organization, or functional
dysconnectivity34.
Impairment of social functioning is not only critical
to the initial diagnosis of schizophrenia, but is also one of
the most important predictors of long-term prognosis35.
However, social functioning is only moderately related to
Anterior insula clinical symptomatology and the outcomes of standard
neurocognitive assessment. Instead, a patients ability to
c Social perception d Social behaviour infer what others are thinking and feeling, and to rea-
Ventromedial son about how their thoughts and feelings will influence
prefrontal their behaviour, seems to be central to understanding
cortex the poor occupational and social functioning evident in
Posterior many people with schizophrenia36. Assessing a patients
superior
temporal capacity for ToM is, therefore, critical for treatment
sulcus andrehabilitation.
Falsebelief tasks37 are extensively validated meas-
ures of ToM that assess the ability to disregard ones own
knowledge about the world and consider that someone
Fusiform face area Amygdala Orbitofrontal else might have a different, erroneous belief. Relative to
cortex healthy controls, people with schizophrenia often exhibit
Figure 1 | Brain regions that are consistently involved in the four social cognition a reduced capacity for false-belief understanding38,39.
networks. a | The dorsomedial prefrontal cortex integrates social Nature Reviews | Neurology
information across When engaged in false-belief reasoning, these patients
time and enables reflection and cognitive representation of traits and norms, whereas also exhibit less recruitment of neural circuitry that has
the temporoparietal junction represents temporary goals and intentions113. b | The dorsal been related to ToM than do healthy controls; these
anterior cingulate cortex is often involved in the cognitive aspects of empathy, whereas neural abnormalities seem to relate to a patients level of
the anterior insula is more often involved in the affective aspects of empathy114. social adjustment40. Most evidence indicates that difficul-
Bothareas are often active when watching others in pain115. c | The posterior superior
ties with false-belief understanding in schizophrenia are
temporal sulcus is often activated in response to real or implied biological motion,
not simply related to secondary cognitive task demands,
specifically in relation to social cues116. The fusiform face area is critical in the face
perception network117. The amygdala is often associated with the social perception such as working memory38,39, but instead reflect more
network because it attributes either a positive or negative emotional valence to stimuli. fundamental problems with mental statereasoning.
d | Activation in the orbitofrontal cortex and ventromedial prefrontal cortex is not Measures that assess social inference, such as the
essential for affective responses, but is critical for the attribution of meaning to an ability to detect faux pas and to interpret speech with
affective stimulus118. Activation in the lateral part of this prefrontal region is often hidden meanings, such as sarcasm, also provide insight
associated with a feeling of displeasure and inhibits behaviour, whereas activation in into when and why ToM difficulties are expected to
more medial parts typically reinforces behaviour through feelings of pleasure119. Damage disrupt social interaction. For instance, Parts2 and 3 of
to these areas often leads to inappropriate social behaviour. The Awareness of Social Inference Test (TASIT)41a
video-based measure that depicts actors in different
studies of social cognition have focused on adults33, social scenariosassess the understanding of sincere
so this Review focuses primarily on measures that are and sarcastic interpersonal exchanges. Studies that used
suitable for use in adult populations. The false-belief the TASIT have shown that people with schizophrenia
understanding task, however, was developed to charac- can understand sincere social exchanges but struggle to
terize developmental changes in preschool children and comprehend sarcasm42,43. Social inference can also be
in middle childhood, so is appropriate for use in young assessed with the Strange Stories test44, which involves
cohorts. Child-appropriate versions of several other of patients reading a series of written stories. People with
the tasks discussed are available, and we provide details schizophrenia are impaired in their ability to understand
where this is the case. stories in which a characters behaviour is best explained
by assuming that they have knowledge of another char-
Theory of mind: schizophrenia acters underlying mental state45. The Faux-Pas Test46 also
Schizophrenia is a clinically heterogeneous disorder that involves a series of written stories but assesses a more
is characterized by positive symptoms (such as delusions specific aspect of social inference: the ability to iden-
and hallucinations), negative symptoms (such as anhe- tify social gaffes. As in the Strange Stories test, people
donia, avolition and affective flattening) and disorgan- with schizophrenia can understand the factual content
ized speech and behaviour. Severe impairments of social of the stories, but their ability to identify social fauxpas
interaction and associated abnormalities are also key isimpaired47.
features: evidence of social or occupational dysfunction In addition to profound impairments of high-level
is a prerequisite for diagnosis32. Specific impairments social inferences and mental state reasoning, people
of social function include difficulty in maintaining with schizophrenia often exhibit deficits in more-basic

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mental-state decodingthe ability to make infer- One of the most extensively validated of these measures
ences on the basis of observable features, such as facial is the Empathic Concern subscaleof the Interpersonal
expression and eye gaze, for example. The Reading the Reactivity Inventory (IRIEC)57. When administered
Mind in the Eyes Test (RMET)48 is the most commonly alongside the Perspective-Taking subscale of the IRI
used and extensively validated method of assessing (IRIPT), the IRIEC can distinguish between affective
this behavioural deficit. The test involves asking par- abnormalities that reflect a lack of caring and those that
ticipants to infer the mental state of a person on the reflect a lack of understanding. For a broader under-
basis of a photograph of their eyes and the surrounding standing of empathic difficulties, the Empathy Quotient
area. People with schizophrenia have greater difficulty (EQ)58 should also be considered, as this measure pro-
than do healthy controls in using these eye gaze cues vides insight into both affective and cognitive empathy.
to determine what another person is thinking or feel- Most, but not all, studies that have used the measures
ing45. An important clinical strength of the RMET is described above have found self-rated empathy to be
that it imposes minimal demands on higher level cog- lower in people with autism than in controls54,59,60.
nitive control operations, such as working memory and Nevertheless, self-report requires emotional insight
abstract reasoning, that are commonly required in other and a willingness to self-disclose personal informa-
measures of ToM. However, visual and verbal demands tion, so in most clinical groups, self-report measures
of the RMET mean that apparent deficits can, in fact, be should be supplemented with other assessments of
a consequence of broader visuoperceptual impairment affective empathy. These other assessments are par-
or aphasia. ticularly important for specific clinical groups, such
As already noted, ToM deficits are not unique as people with autism, which is highly comorbid with
to schizophrenia: a large body of literature on the alexithymia61, a personality construct characterized by
topic demonstrates that ToM is disrupted in a wide difficulties in identifying and describing emotions and
range of neuropsychiatric, neurodegenerative and in distinguishing feelings from the physical sensations
neurodevelopmental disorders8, and is often impaired of emotional arousal. Many individuals with autism also
after acute brain damage49. In many of these disorders, have intellectual impairments32.
as in schizophrenia, ToM deficits are not simply attrib- Although observation during a clinical interview
utable to secondary task demands, and have been linked can provide potentially valuable insights into affective
to important functional outcomes. However, the liter- empathic disturbances, in highly structured situations,
ature also shows that considerable heterogeneity exists patients might behave similarly to controls62, meaning
between and within different clinical populations that empathic deficits might not be evident during brief
with respect to the nature, severity and specificity of observations. For these reasons, informantrated and
ToM impairments, an observation that reinforces the emotion-relevant performance tasks might provide
need for objective measures to inform therapeutic the clearest clinical insights into the affective empathic
decision-making on a casebycase basis (TABLE1). disturbances associated with autism, particularly when
combined with self-report.
Affective empathy: autism The most widely used informant-rated measures
Autism is one of the most common neurodevelop- of affective empathy are simple modifications of self-
mental disorders: the estimated prevalence is 1 in 132 report measures, such as the IRIEC or EQ. Several
people50. The condition is characterized by a restricted studies that have used these measures have revealed
repertoire of interests and activities, and deficits in autism-related deficits; in some cases, they identified
communication skills and social interaction32. It has greater impairments than did the corresponding self-
been linked to a range of neural abnormalities, includ- report versions of these scales63. In emotion-relevant
ing aberrant functional connectivity51. Maladaptive performance tasks, emotionally arousing videos 64
emotional reactions are common among people with orphotographs59,65 are presented to participants, who
autism, and include a reduced affective empathic are asked to rate their emotional response. One such
response52. Reduced distressresponse measures in measure is the Multifaceted Empathy Test (MET)59,
infants as young as 12months are predictive of a later which differentiates between mental state understand-
autism diagnosis53. However, some studies indicate that ing (cognitive empathy) and subjective emotional
emotional empathic responses can be intact54, or even response (affective empathy). This test has been used to
heightened, in people with autism, indicating a more identify abnormalities of affective empathic responding
general affective imbalance55. This heterogeneity could in people withautism65.
indicate that some atypical emotional reactions in peo- Affective empathy is impaired in many other dis
ple with autism reflect problems with understanding orders that present with relatively diffuse brain dam-
the perspectives of others rather than a lack of care or age, including traumatic brain injury and dementia66,
concern perse56. and in many personality disorders. For instance, the
Valuable clinical insight into the social cognition of affective empathic response is dysfunctional in nar-
people with autism can be gained from self-report meas- cissistic personality disorder67, and a lack of affective
ures of affective empathy (BOX3). Such measures typi- empathy is a defining feature of antisocial personality
cally involve a series of simple statements that directly disorder. Moreover, people with psychopathic personal-
enquire about the degree to which a person experiences ity disorders exhibit a specific breakdown of the neural
warm, concerned or compassionate feelings for others. processes that support the ability to experience others

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Table 1 | Descriptions of stimuli from theory of mind measures


Measure Experimental task Control task(s)
False-belief Tasks 37
Participants are told a story that involves two characters, Non-mental reality
Sally and Anne. In one example, Sally has a basket and Anne control questions that
has a box. Sally puts a marble in her basket, then goes for a assess participants
walk. While Sally is away, Anne moves the marble to the box. understandingofthe situation
Sally comes back and wants to play with her marble. At the and/or a series oftrue belief
end of this story, participants are asked where Sally will look scenarios
for her marble. The task measures whether a participant can
understand that Sally holds a belief that is different to their
own, and which is contrary to reality (a false belief)
The Awareness Questions focus on the ability to detect sarcasm in a Questions focus on the ability
ofSocial socialinteraction to detect sincerity in a social
InferenceTest41 interaction
Strange Stories Participants are asked to demonstrate their understanding Identical to the experimental
Test44,120 of a written story in which a characters behaviour can be task, except a characters
best understood by attributing to them a specific underlying behaviour can be explained
mental state without any need for mental
inference
Faux-Pas Test46 Participants are read a story that contains a faux pas and Identical to the experimental
subsequently asked questions that focus on their ability to task, except participants are
detect the faux pas, and to understand beliefs, intentions asked questions that focus on
andinappropriateness a protagonists behaviour and
do not require mental inference
toanswer
Reading the Mind Participants are shown photographs of the eye regions of No standard control task exists;
in The Eyes Test48 peoples faces, and asked to select one of four alternatives in some studies, participants are
describing what the person in the photograph is thinking shown the same photographs as
orfeeling in the experimental task, but are
asked to select which age range
or gender is correct for each
person in the photographs

emotions68. Such difficulty in identifying with the dis- in other neurocognitive domains become increasingly
tress of others should be regarded as particularly clin- evident. Deficits in social cognition have also emerged
ically important, as it has been linked to premeditated as an important aspect of the disease. Evidence has
and goal-directed acts of aggression69. shown that such deficits explain aspects of patients
functional dependence that are independent of the
Social perception: Alzheimer disease effects of deficits in general cognition72, and are related
AD is the most common cause of dementia. The dis- to problems with managing treatment and behaviour73,
ease involves gradual and progressive neurodegener- increased agitation,74 and poor interpersonal relation-
ation that initially affects the hippocampi, entorhinal ships75. Inparticular, social difficulties and behavioural
cortex and posterior cingulate cortex, and subsequently abnormalities related to AD have been linked to deficits
the entire temporal, parietal and frontal cortices70. Mild in interpreting cues to emotional states. Consequently,
episodic memory impairment is often the earliest cog- basic social perceptual functioning should be consid-
nitive marker of AD71, but with disease progression, ered when modelling the effects of AD on important
memory deficits become more severe, and impairments clinical and behavioural outcomes, such as mental
health and socialfunctioning.
Social perceptual failures often manifest as diffi-
Box 3 | Measures of affective empathy
culties with identifying others emotions, and many
measures are available that assess this ability through
Empathic Concern57 the presentation of static photographs of high-intensity
Self-rated or informant-rated facial expressions (TABLE2). The most extensively vali
Participants are asked about feelings of warmth, compassion and concern for others dated stimuli are the Ekman Faces76, which are black
Empathy Quotient58 and white photographs that depict the six basic emo-
Self-rated or informant-rated tions (disgust, anger, fear, surprise, sadness and happi-
This measure assesses the ability to understand and predict others behaviour, and the ness) and neutral faces. Most studies that have used the
nature of any emotional response to other people Ekman Faces to assess patients with AD have identified
impairments in patients when compared with healthy
Multifaceted Empathy Test59
controls7779. ADrelated deficits have also been identi-
Performance task
fied when different sets of photographs79, schematic line
The empathic responses of participants to emotionally intense photographic images drawings of faces73 or 3D virtual actors have been used80.
are assessed
However, most standard measures of facial expression

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Table 2 | Descriptions of stimuli from social perception measures


Measure Experimental task Control task(s)
Ekman Faces Emotion Participants are shown a picture of a face and Executive control and language tasks
Labelling76 asked which emotion is depicted; emotion labels
are typically provided, and participants are asked
to choose between them
Ekman Faces Emotion Participants are shown two faces concurrently Facial recognition
Discrimination76 andasked whether they show the same or
different emotions
Facial Expressions Uses the Ekman Faces; photographs can depict Depends on whether the task involves
of Emotion Stimuli expressions with 100% intensity (as in the standard emotion labelling (in which case
andTests81 EkmanFaces), but computerized morphing and executive control and language control
caricaturing procedures are also available to tasks should be used) or emotion
modulate emotion intensity discrimination (in which case a facial
recognition control task should be used)
Comprehensive Affect Subtest 1: Ekman 3faces task Subtest 2: Identity matching
Testing System82 Subtest 3: Affect matching Subtest 8: Non-emotional prosody
Subtest 4: Affect discrimination discrimination
Subtest 5: Affect naming
Subtest 6: Prosody identification
Subtest 7: Prosody naming
Subtest 9: Emotional prosody discrimination
Subtest 10: Match emotional prosody to face
Subtest 11: Match emotional face to prosody
Subtest 12: Conflicting facial emotion and
prosodyrespond to face
Subtest 13: Conflicting facial emotion and
prosodyrespond to prosody
Florida Affect Battery83 Subtest 2: Facial affect discrimination Subtest 1: Facial identity
Subtest 3: Facial affect naming discrimination
Subtest 4: Facial affect selection Subtest 6: Non-emotional prosody
Subtest 5: Facial affect matching discrimination
Subtest 7: Emotional prosody discrimination
Subtest 8: Name the emotional prosody
Subtest 9: Match emotional prosody to an
emotional face
Subtest 10: Match emotional face to the
emotional prosody
The Awareness of Participants are shown videos in which an actor Executive control and language tasks
Social Interference portrays one of seven basic emotions, sometimes
Test Part 1: Emotion with ambiguous dialogue, sometimes without any
Evaluation Test41 dialogue. Participants are asked to identify the
emotional expression depicted

recognition present extreme emotional intensities, so impaired in AD but some are not84,85, indicating that
when assessment of subtle social perceptual impairment patients have residual strengths with implications for
is required, measures that present less intense facial individualizedinterventions.
expressions should be used. The Facial Expressions of Evaluation of the ability to integrate social percep-
Emotion: Stimuli and Tests81 includes images that vary tual cues with contextual information that forms part of
in their emotional intensity, enabling clinicians to create normal social encounters can also be clinically useful.
tasks that are graded in difficulty. A study that used this One measure that can be used for such an assessment
measure showed that ADrelated deficits in identifying is the Emotion Evaluation Test41, which forms part of
emotions were greater when expressions with an inten- the TASIT and assesses the ability to recognize emotions
sity of 75% were presented than when those with an from dynamic, multimodal stimuli that are embed-
intensity of 100% werepresented5. ded into specific social scenarios. ADrelated deficits
The breadth and specificity of difficulties in recog- detected by this measure are minimal or absent77,84. This
nizing emotions can be assessed with batteries of tests finding might be explained by greater redundancy that
such as the Comprehensive Affect Testing System82 results from multiple channels of information, help-
and the Florida Affect Battery83, which use not only ing to attenuate declines in the speed or efficiency of
visual stimuli, but also auditory. Both of these bat- processing social perceptual cues in patients with AD.
teries incorporate multiple subtasks that assess the As previously noted, an important consideration in
ability to process visual (facial expressions), auditory the development of any treatment plan for impairments
(prosody) and visualauditory (simultaneous facial of social cognition is establishing the specificity and
expressions and prosody) emotional information. Use potential causes of the impairment. Impairments of per-
of these measures has shown that some subtasks are ception, language, and executive function often cooccur

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Box 4 | Measures that assess social behavioural abnormalities progressive degeneration of the prefrontal and anterior
temporal neocortex90. Individuals with bvFTD often
Frontal Systems Behaviour Scale93 exhibit deficits in executive function that can be detected
Self-rated or informant-rated with neuropsychological tests, but they often perform
Assesses behaviour that is related to frontal lobe dysfunction normally on other standard neurocognitive assessments.
Focuses on apathy, disinhibition and executive dysfunction Mood and behavioural disturbances are often the ear-
Frontal Behavioural Inventory96 liest presenting symptoms of bvFTD, so the condition
Informant-rated is clinically under-recognized and often misdiagnosed.
In the early stages and in young patients in particular,
Assesses behaviour that is related to frontal lobe dysfunction
bvFTD is often mistaken for a psychiatric rather than
Assesses behavioural symptoms that include aspontaneity, indifference or emotional
neurodegenerative disease91. Misdiagnosis as AD or
flatness, inflexibility, disorganization, inattention, personal neglect, loss of insight,
perseveration and stereotypy, inappropriateness, excessive jocularity, poor
other types of dementia is also relatively common.
judgement, impulsivity and hypersexuality Simple tools that are designed to detect abnormal
interpersonal behaviour often provide an effective
Socioemotional Dysfunction Scale100
way to distinguish bvFTD from other psychiatric and
Informant-rated
neurodegenerative disorders92. Patients self-report data
Provides a global score of social competency might be distorted owing to a lack of emotional insight,
Focuses on a range of social behaviours, including extraversion, warmth, social known as frontal anosodiaphoria, that is often present
influence, insight, openness, appropriateness and maladjustment in this condition. As a consequence, informants such
PeerReport Social Functioning Scale101 as a close confidant, a caregiver, or a spouse are widely
Informant-rated regarded as the best source of clinical data in patients
Assesses socially appropriate and inappropriate behaviour, as well as the tendency to with bvFTD. A range of informant-rated measures are
engage in stereotyping or prejudicial behaviour towards others now available to gain insight into abnormalities of social
Social Impairment Rating Scale103 behaviour(BOX4).
Clinician-rated The Frontal Systems Behaviour Scale (FrSBe)93 was
developed specifically to quantify the behavioural distur-
Assesses specific domains of social impairment
bances associated with frontoexecutive dysfunction. The
Domains are: lack of attention or response to social cues, inappropriate trusting or
scale provides a total score and separate scores for three
approach behaviour, lack of adherence to social norms, difficulty with recognizing
people, social withdrawal and socioemotional detachment behavioural domains: apathy, disinhibition and executive
dysfunction. Scores obtained with the FrSBe are higher
for patients with bvFTD than for patients with AD94, and
with impairments of social cognition and contribute to increase with greater prefrontal and temporal grey matter
poor social functioning in many clinical groups, includ- loss95. Similarly, the Frontal Behavioural Inventory (FBI)96
ing patients with AD. In particular, ADrelated deficits quantifies changes in personality and behaviour that are
that are detected by measures of facial affect labelling associated with frontoexecutive dysfunction. Scores on
(in which explicit choices must be made between differ- the FBI can distinguish bvFTD from other dementias97,98,
ent affective labels) are partially explained by difficul- and are sensitive to diseaseprogression99.
ties with language79 and executive control5. By contrast, The FrSBe and FBI each include items that assess
difficulties with facial affect discrimination (which social behavioural symptoms, but also assess patients for
requires participants to decide whether two faces dis- a broader range of nonsocial behavioural disturbances,
play the same or differing emotions) are predicted by such as executive dysfunction and stereotyped move-
face processing ability5,79. ments. If a more focused and nuanced understanding
The use of similar tests to establish the specificity of social impairment is required, the informant-rated
and cause of impairment is important for many clinical Socioemotional Dysfunction Scale (SDS)100 should
populations that present with social perceptual failures, be considered. The SDS focuses on interpersonal
including patients with common neurodegenerative phenomena, such as social inappropriateness, social dis
disorders other than AD, such as Huntington disease86, engagement and personal warmth, and can differentiate
and demyelinating disorders, such as multiple sclero- between earlyonset AD and bvFTD100. Another prom-
sis87. Social cognitive difficultiesincluding broad- ising informant-rated measure that focuses on inter
based social perceptual failuresare also regarded as personal function is the Social Inappropriateness Scale101,
core impairments in traumatic brain injury49, and are which can identify increased levels of socially insensitive
common in many psychiatric illnesses88. behaviour in people with dementia102.
A clinician-rated measure, the Social Impairment
Social behaviour: bvFTD Rating Scale (SIRS)103, has been developed to system-
bvFTD is a chronic neurodegenerative disorder that is atically grade the severity of social behavioural symp-
characterized by changes in personality and interper- toms across seven domains, including social withdrawal
sonal conduct, loss of empathy, increased stereotypical and inappropriate trusting or approach behaviour. In
behaviours, disinhibition, apathy and emotional dys- people with bvFTD, deficits in specific SIRS domains
regulation89. Sociopathic acts, including unsolicited differentially relate to atrophy in distinct corticolimbic
sexual acts and physical assaults, are also common. networks. Systematic observation of patients during
These behavioural changes have been associated with everyday socialactivities can also provide valuable

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History or presentation indicates


Clinical potential social cognitive dysfunction Diagnosis associated with
case nding social cognitive impairment

Self or informant raises concerns


Clinical assessment
Theory of mind Unusual social behaviour
Aective empathy observed in the clinic
Social Social perception
cognitive Social behaviour
assessment Ideally a combination of standardized
self-report, informant rating and ability-based
assessments, in addition to clinical observation

Social cognitive decit(s) identied

Specicity of impairment?
Dierential Interpret in relation to appropriate matched control tasks
diagnosis where available, and to broader neurocognitive function,
particularly perceptual, language and executive function

Primary impairment Secondary impairment

Interventions that Interventions that


Treatment directly target social target the underlying
cognitive symptoms impairment

Key outcome variables include quality of life,


Follow-up mental health, employment status, loneliness
and social relationships and/or support

Figure 2 | Algorithm for the evaluation and treatment of social cognitive impairments. If patient
Nature history
Reviews or| clinical
Neurology
presentation indicates social cognitive dysfunction, each of the four domains should be assessed with at least one measure.
Results of these assessments should be supplemented with formal clinical observation. If specific social cognitive deficits
are identified, a more comprehensive assessment that focuses on the domain(s) in question should be conducted. Before
recommendations for treatment can be made, establishing the specificity of any impairments, particularly whether the
difficulties reflect a primary social cognitive deficit or a secondary consequence of broader neurocognitive impairment,
iscritical. Upon completion of treatment, followup should focus on community integration and mentalhealth.

insight intosocial behaviour. For example, in one study, rehabilitation plan, treatment efforts should be directed
recorded segments of mealtimes revealed consistent dif- towards managing such difficult behaviour, andensur-
ferences between the behaviour of patients with different ing the availability of appropriate educationand support
forms of dementia104. Patients with bvFTD used fewer forcaregivers.
phrases that contained the word you than did caregivers
or individuals with AD, and they also exhibited less tact Clinical application and the future
and manners. Such data highlight the fact that clinical Social cognitive deficits rarely occur in isolation, so all
observation of a patients spontaneous social behaviour four domains should routinely be assessed in clinical
can provide valuable insight into the level and nature of practice when a patient presents with a neurological
social impairment, even when high-quality informant disorder and indications of social cognitive impairment
reports are available. (BOX1). In the context of a broader neurocognitive assess-
Abnormal interpersonal behaviour is commonly seen ment, such clinical data can be used to clarify the nature,
in clinical practice, and it forms part of the core diag- magnitude and specificity of social cognitive impair-
nostic criteria for many clinical disorders in addition ment, with important implications for therapeutic deci-
to bvFTD, including schizophrenia, autism, Williams sion-making. We present here a five-step algorithm for
syndrome and social phobia32. Acute brain damage can evaluation and treatment (FIG.2) that includes details
also precede profound changes in social behaviour. For of how to approach the assessment of social cognition
instance, people with traumatic brain injury often exhibit in clinical practice, starting with data gathering and
a range of behaviours that are difficult to deal with and proceeding through treatment to followup.
cause distress and burden among family caregivers, When social cognitive dysfunction is suspected, we
thereby directly contributing to poor social relation- recommend that at least one measure of each of the four
ships105. Given the critical role of family and friends in any domains is administered. Selection of these assessments

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REVIEWS

should be guided by their reliability, clinical validity and also exists in the potential benefits of pharmacotherapy.
population norms (see Supplementary TablesS1S4). Peripheral administration of exogenous oxytocin has
Clinical validity is judged according to whether a meas- already been shown to augment social cognitive skills
ure has shown appropriate sensitivity and specificity, training in schizophrenia110, and might help people with
where these data are available, for disorders that are char- other disorders, such as autism andbvFTD31,111.
acterized by social cognitive dysfunction, with particular
reference to autism and bvFTD. The variation in these Conclusion
aspects demonstrates the challenge in assessing social For neurologists, assessment of social cognitive defi-
cognitive function. In particular, many measures have no cits in many disorders associated with brain dysfunc-
formal, or only modest, population norms. The interpre- tion is now recognized to be as important as traditional
tation of clinical data depends on an appropriate match neurocognitive assessment. Problems with memory or
between the individual being assessed and the normative language might affect a patients ability to work or live
data with which their test performance is compared; a independently, but the negative impact of such disabili-
concerted effort is now needed to gather normative data ties on mental health and wellbeing can be ameliorated
for assessments for which such data are currently unavail by strong social networks. Social cognitive deficits, how-
able or limited. The availability of norms will become ever, impair the ability to form and sustain interpersonal
increasingly important as this field of research grows. relationships, thereby eliminating the benefits that social
Social cognitive intervention is a relatively new area of interactions have for patients with other neurocognitive
research, but many promising inroads have already been impairments. Indeed, social isolation has long been
made. Progress has included the development of targeted known to be a major risk factor for morbidity and mor-
training programmes that have been associated with tality7,112. A comprehensive assessment of social cogni-
improvements in some functional domains106 andwith tive dysfunction in patients with acute brain trauma, as
changes in the neural systems that support social cog- well as in patients with either a history or diagnosis that
nitive processes107. Several available interventions focus points to social cognitive dysfunction, should therefore
on individual social cognitive skills, such as facial affect be central in planning any neurorehabilitation effort. We
recognition108; a common strategy among such interven- have detailed the four key domains of social cognitive
tions is to direct a patients attention to specific aspects function that should be assessed in such patients, and
of a facial expression, and to provide verbal descriptions some of the best validated assessment tools that can be
of distinguishing perceptual characteristics. Other inter- used to meet the clinical needs of patients with such dys-
ventions target social behaviour and communication function. When used in combination with more stand-
skills more broadly, often via role-play or social cognitive ard neurocognitive assessments to inform treatment
training batteries that encompass repeated practice of a efforts, these measures have the potential to substantially
range of social cognitive tasks109. Considerable interest enhance treatment decision-making and outcomes.

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