4. Chapter four: Rationale for the current research
4.1. The rationale for the current research
As previously outlined, TBI is a major cause of death and disability (Dinsmore, 2013; Maas et
al., 2008). The high prevalence of TBI creates a serious burden on public health services
(Fineberg et al., 2013), as well as physical, emotional, and financial strains on the survivor and
their families. Indeed, some authors have documented that social cognition impairments are
the greatest barrier to life adjustment and rehabilitation after brain injury (Grattan &
Ghahramanlou, 2002; Ponsford & Schönberger, 2010; Yates, 2003). The extant literature
illustrates that many TBI survivors and their families report that changes in emotional and
social abilities were more disabling and difficult to deal with than cognitive or physical changes
(Kelly et al., 2008; Koskinen, 1998; Marsh et al., 2002). Individuals who have sustained a TBI
often do not return to full-time employment (Grauwmeijer, Heijenbrok-Kal, Haitsma &
Ribbers, 2017) and experience decreased social relationships and material difficulties
(Ponsford et al., 2014). This deleterious sequela more than likely exacerbates pre-existing
mental health conditions that include depression, anxiety, and substance abuse (van der Horn,
Spikman, Jacobs & van der Naalt, 2013; Kreutzer, Seel & Gourley, 2001).
As human beings are social creatures, interpersonal relationships are important for both
physical and mental health (Heinrich & Gullone, 2006). Exclusion from or inadequate
participation in the social community through core social roles (e.g. having a job, being part of
a family or hobbies) can lead to poor self-regulation and poor self-esteem (Siegrist, 2000).
Human loneliness is a risk factor for the decline in cognitive function, depression, and social
anxiety (Cacioppo & Hawkley, 2009). Social cognition, the skill which enables people to
understand the social world (Cassel et al., 2019), is a prerequisite of social integration (Brother,
documented (May et al., 2017; McDonald, 2013). It has been acknowledged that the prevailing
nature of socioemotional impairments post-TBI makes them one of the most challenging and
deliberating of all TBI sequelae (Brooks et al., 1986; Kinsella et al., 1991; Ubukata et al., 2014).
It has been noted that social cognition impairments occur on an implicit and automatic level
(Barker & Andrade, 2006; Morton & Barker 2010, Barker, Andrade & Romanowski 2004),
strongly correlating with frontal lobe pathology (Barker, et al., 2004; Frith and Frith 2001;
Siegal and Varley, 2002). Due to the brains position within the skull and the biomechanical
and pathophysiological factors associated with TBI, the frontal lobes and the connecting
pathways often sustain an injury during trauma (Bigler, 2007). One of the most prevalent
impairments associated with frontal lobe damage is facial affect recognition (Drapeau,
Gosselin, Peretz & McKerral, 2017; Neumann et al., 2016; Spikman et al, 2013), yet the
underlying mechanisms of this deficit are not well understood.
It is estimated that up to 39% of individuals with a moderate-severe TBI could present with
significant facial affect identification impairments (Babbage et al., 2011), with experts
suggesting that this particular impairment could be one of the main barriers to successful
community re-integration (Croker & McDonald, 2005). Nevertheless, formal assessments of
facial expression recognition post-TBI are often overlooked in clinical practice (Kelly et al.,
2017a, 2017b). Current experimental treatment-outcome research has indicated that
rehabilitation programmes can be successful in improving social behaviour post-TBI (Barman,
Chatterjee & Bhide, 2016; Flanagon, McDonald and Togher, 1995; Williamson & Isaki, 2015).
Indeed, there are positive reports of facial affect recognition interventions post-TBI (Bruhns,
2017; Neumann, Babbage, Zupan & Willer, 2015; Williamson & Isaki, 2015), but more success
could be gained if the underlying impairment mechanisms were fully understood, potentially
allowing clinicians to target specific deficits rather than resorting to a global intervention
Social perception, that is the ability to detect social stimuli or social cues, is pivotal for social
functioning. Social interactions rely on several visual processes, including action observation and the ability to read others’ feeling and intentions through body language and facial
expressions (Matsumoto et al., 2015). A range of brain networks orchestrates social perception;
central to this is the perception network (Bickart, Dickerson & Barrett, 2014). This network is
thought to process information rapidly and automatically (Whalen, 2007). Appropriate eye
movements are critical for social perception (Gobel et al., 2015; Freeth et al., 2013) and
aberrant eye scan patterns are associated with low social adaption and high social disability
(Klin et al., 2002), as well as impairments in deciphering mental states (Grynszpan & Nadel,
2015; Itier & Batty, 2009).
Residing within the frontal lobes are critical eye movement regions that mediate saccades and
fixations, namely the FEF, SEF, DLPFC. Intracortical white matter pathways also connect the
frontal lobes to other critical eye movement centres within the brain, such as the PEF and the
occipital cortex (Stanton, Bruce & Goldberg, 1995; Vernet et al., 2014). These networks often
incur some degree of pathology during trauma due to the compressive forces of the skull on
soft brain tissue (Bigler, 2013), yet there is a dearth of research exploring the impact this has
on social cognition. There are a limited number of studies which have investigated eye scan
patterns in response to social stimuli after TBI (Adolphs et al., 2005; Douglas et al., 2010;
Mancuso et al., 2015; Vassallo et al., 2010; Vassallo et al., 2011; Wolf et al., 2014), but the
methodologies are constrained by small sample sizes and static stimuli. Nevertheless, what
these findings underscore is that impairments in social perception after TBI may be associated
with the inability to direct attentional resources to salient social information, rather than
damage to specific areas (e.g. the face perception network) or aberrant upstream cognitive
Eye movement abnormalities are well established in several disorders associated with frontal
lobe dysfunction, notably schizophrenia (Bortolon et al., 2016) and autism (Wang et al., 2015).
In fact, aberrant eye scan patterns are used as a classifier and trait marker in both schizophrenia
(Benson et al., 2012) and autism (Carette et al., 2019). This information is pertinent for the TBI
research field as common behavioural symptoms shared by the conditions (e.g. apathy, lack of
motivation, lack of spontaneity, and disinterest in social interactions) might be related with
atypical eye movements. For example, Schwab, Würmle, Razavi, Müri and Altorfer (2013)
developed a visual peripheral recognition task that required participants to coordinate both eye
and head movements. A visual target was first presented in the centre of the screen and then in
the periphery and the participant had to decide if the two targets were equal or not. There were
two different tasks, a simple colour recognition task and a more challenging Landolt-C
orientation task. Two tasks were implemented to explore the hypothesis that tasks of varying
difficulty may induce differences between participants with schizophrenia and controls
concerning eye-head coordination. There were differences between individuals with
schizophrenia and controls where the control group displayed long latencies during the colour
task and short latencies during the Landolt task while individuals with schizophrenia had
similar latencies across both tasks. The individuals with schizophrenia also displayed more
head movements and increased eye-head offsets. As head movements and visual strategies are
both used during social interactions to pick up social cues and to display engagement (e.g. joint
attention), abnormalities within these systems are bound to have a negative effect of social
integration. The researchers suggested that the individuals with schizophrenia may have
displayed a specific oculomotoric attentional dysfunction as they demonstrated difficulty in
adapting to the two different tasks, compared to the control group. Furthermore, the
uneconomic over-performance of head-movements may have been due to poor inhibition,
individuals with schizophrenia have difficulty determining the relevance of stimuli which could
extend to social interactions. This hypothesis is supported by a published literature review
which concluded that restricted scanning behaviour, often documented in schizophrenic studies,
could be linked with the negative symptoms of the condition, specifically in terms of face
viewing (Beedie, Clair & Benson, 2011). Research has demonstrated that individuals with TBI
frequently display very similar behaviours to the negative symptoms of schizophrenia (e.g.
apathy, anhedonia difficulty in determining the relevance of social stimuli – Damasio, Tranel
& Damasio, 1990; Worthington & Wood, 2018), so it may be the case that aberrant visual
strategies lead to difficulty determining the relevance of social stimuli, but this hypothesis is
currently untested. An emerging theory within the autism literature is that abnormal social
reward processing may underlie social impairments in autism (Bottini, 2018), and this has been
linked to pupillary responses to faces. Sepeta et al., (2012) reported that children with autism
did not show typical pupillary sensitivity to gaze direction in response to happy faces compared
to typically developed children. The authors proposed that the findings supported the
hypothesis that individuals with autism displayed reduced sensitivity to the reward value of
social stimuli. This theory has also been supported by subsequent research (Gale, Eikeseth &
Klintwall, 2019; Ruta et al., 2017) and could potentially explain why individuals with TBI
often appear apathetic and disinterested in the social environment (Worthington & Wood,
2018) (i.e. pupillary sensitivity indicates appeal/attention/preference but if visual strategies are
aberrant after TBI then the individuals affected may not be picking up relevant
cues/appropriately reacting to cues). Again, this hypothesis is currently untested.
Therefore, the negative symptoms of schizophrenia (e.g. apathy, anhedonia) and the principal
characteristics of autism (e.g. finding it hard to understand others, finding it hard to make
friends or preferring to be on their own, seeming blunt, rude or not interested in others), are all
mediated by aberrant low-level visual processing abilities, but eye-tracking research within the
TBI field is significantly lacking.
From reviewing the existing literature base, it is clear that the mechanisms underpinning social
cognition post-TBI are poorly understood. Research suggests that upstream cognitive processes,
as well as co-morbid effects and pre-morbid personality traits, could affect social cognition
impairments post-TBI. Correlational analyses have reported that poor performance on social
cognition tasks is generally not related with cognitive deficits post-TBI (e.g. memory,
executive function and attention – Spikman et al., 2012), suggesting that other factors must
mediate the social cognition deficits consistently reported in the literature. TBI is often
associated with co-morbid conditions such as post-traumatic stress disorder (PTSD; Tanev,
Pentel, Kredlow & Charney, 2012), substance abuse (Weil, Corrigan & Karerlina, 2016),
psychiatric disorders (Rogers & Read, 2007) and mood disorders (Spitz, Always, Gould &
Ponsford, 2017). These post-TBI comorbidities interplay with social cognition deficits, for
example, a general impairment in memory may lead to an individual with TBI forgetting key
dates resulting in relationship breakdowns. Furthermore, PTSD, mood disorders and other
psychiatric disorders may stop an individual with a TBI from leaving their home, harming
social relationships and general mental health. Premorbid personality characteristics have also been proposed as a moderator for ‘reserved’ social cognition following TBI. Sela-Kaufman,
Rassovsky, Agranov, Levi and Vakil (2013) reported that premorbid personality characteristics
provided the most robust moderator of occupational outcome (which could be considered as a
good measure of social reintegration). Frank (2011) also proposed that certain premorbid
personality traits may have implications regarding the way the individual copes with post-TBI
changes. High levels of neuroticism, ineffective problem solving, and avoidance coping have
been associated with poor adaption, while characteristics such as optimism and positivity are
public (Salminen, Saarijärvi, Aärelä, Toikka & Kauhanen, 1999) and is hypothesised to be a
risk factor for several medical and psychiatric disorders associated with affect regulation
(Luminet, Bagby & Taylor, 2018). Individuals who experience this ‘organic alexithymia’ are
likely to have a lower social reserve if they experienced a TBI compared to individuals who do
not have alexithymia. Although the literature suggests that these comorbid factors are not the
underpinning mechanisms driving social cognition impairments post-TBI, the factors
mentioned above, plus other factors (e.g. employment status, social/culture/economic status),
are likely to exacerbate the already deleterious emotional and social sequelae of TBI and
partially determine psychosocial outcome post-TBI (Williams et al., 2020).
Existing attempts to elucidate the underlying mechanisms of social cognition post-TBI have,
so far, been unsuccessful. Existing research tends to employ imaging techniques with findings
indicating a general brain dysfunction, with particular abnormalities within the frontal circuits.
However, the specific mechanisms underpinning these impairments are still unknown and
findings are univocal. For instance, Neumann, McDonald, West, Keiski and Wand (2016)
proposed that post-TBI brain dysfunction may lead to impaired holistic face processing while
Rigon, Voss, Turkstra, Mutlu and Duff (2019) hypothesised that facial affect recognition was
comprised of subcomponents that depend on distinct neural substrates and that individuals with
TBI were impaired in some, but not all, subcomponents. Other schools of thought for
explaining the potential mechanisms underpinning impaired social cognition include impaired
simulation (McDonald et al., 2011), impaired physiological responsivity and dulled emotional
experience (Croker & McDonald, 2005; Hornak et al., 1996). However, none of these theories
presents a complete account for the underlying mechanisms of social cognition deficits post-
TBI. One downfall of the pre-existing explanations is that they tend to focus on mid to high-
Individuals perceive what they attend to, or fixate on, so recording fixations in response to
social stimuli can offer objective indices of typical or aberrant visual scanning patterns. If there
is variability between the TBI and control groups, then this might underpin the reported
upstream social cognition deficits in the TBI literature. Few studies have explored these basic
visual processes and the experiments which do have only implemented very basic static stimuli
which lack ecological validity. It appears that one of the reasons for this deficiency in
understanding the low-level social cognition processing of individuals with TBI is due to a lack
of published research. For example, when a targeted literature search was conducted using
Scopus, an abstract and citation database, with the terms ‘eye-tracking’ and ‘traumatic brain injury’ only 86 documents were found. When ‘social cognition’ was added to the search terms,
only three papers were found. These figures are extremely low in comparison to a similar search when the terms ‘eye-tracking’ and ‘autism’ were inputted, generating 761 documents or ‘eye-
tracking’, ‘autism’ and ‘social cognition’ which generated 122 articles. Indeed, while the
research fields of autism and schizophrenia have explored, in-depth, visual strategies in
response to social stimuli, the TBI research field is lagging. One reason for this may be that
higher-level ‘classic’ cognitive impairments have been the focus of investigation following
TBI. This is supported by a Scopus review using the terms ‘cognitive impairment’ and ‘traumatic brain injury’ which generated a list of 3,087 articles. It has been established that
social cognition is not well understood by experts in the TBI field and that social cognition
deficits are rarely ever assessed during clinical practice (Kelly et al., 2017a, 2017b). Commonly,
practice-based evidence feeds into research, for instance, clinicians consistently feedback that ‘classic’ cognitive functions are impaired post-TBI. However, if clinicians are not assessing
social cognition post-TBI, probably due to a lack of education, assessments and rehabilitation
interventions, then this cross-talk between clinicians and researchers is naturally going to
When referring back to the three stages of social cognition (Ostrom, 1984; Penn et al., 1997),
there is a wealth of evidence focusing on stages two and/or three (interpretation of social
information and processing of social information) while very little exploration is given to the
very initial perception of social cues. This dearth could be associated with the fact that, in the
past, eye-tracking technology was limited (not many models available, difficult to use, i.e. chin
rest and head restrictions, and varying accuracy) and costly or because other areas of post-TBI
impairments appeared more pertinent. As the research field of eye-tracking and social cognition
post-TBI is scant, very few efforts have been made to create reliable and valid assessments.
Indeed, to the best of the researcher’s knowledge, only two dynamic tasks have been validated
with TBI populations; TASIT (McDonald et al., 2002) and CAVEAT (Rosenberg et al., 2016),
neither of which have been implemented with eye-tracking technology. This also supports the
fact that the deficiency in understanding the role of low-level processing in social cognition
post-TBI is due to a general paucity of investigation. Hence, the current research, and similar
projects, are needed to fill the gap in the literature and to shed light on the deficient
understanding of the role of low-level processing in social cognition post TBI.
The innovative aspect of the current research is the implementation of ‘real world’ dynamic
and contextual stimuli. The denouncement of static stimuli in the neuropsychology literature is
gaining traction, with scholars arguing that static stimuli lack ecological validity and mundane
realism (Blais et al., 2017; Feldman-Barrett, 2011; Ibañez & Manes, 2012; Juslin et al., 2018;
Knox & Douglas, 2009; Leigh & Zee, 2016; Namba et al., 2018; Recio, Sommer and Schacht,
2011). There are clear disparities between static laboratory-based social cognition tasks and
everyday social interactions. For instance, experimental paradigms often lack motion and depth
cues (Alves, 2013; Mccamy et al., 2014; McDonald et al., 2003) as well as the absence of
contextual cues (Feldman-Barrett et al., 2011; Ibañez & Manes, 2012). Furthermore, evidence
Stoesz and Jakobson, 2013). Social interactions demand the tracking of emotions and mental
states through complex cues, such as facial expressions, body language, and eye gaze. This
dynamic process requires a constant shift in attentional processing. The currently available
dynamic social cognition assessments are still flawed in that they include posed expressions
(Juslin et al., 2018; Namba, et al., 2018) and are administered in experimental settings
(Feldman-Barrett et al., 2011; Ibañez & Manes, 2012). Nevertheless, they offer a vast
improvement on static stimuli yet are not as widely implemented in the existing evidence base,
particularly within the TBI research field.