BI, anxious temperament and physical therapy

“Learning to navigate the social world is a core developmental task. To do so adaptively, children must create for themselves a stable understanding of who they are as individuals and their place within the specific social context that surrounds them. One need not be a trained psychologist to note the wide individual differences displayed by children, and later adults, as they come to find their place in the world. Indeed, we have centuries of writing and debate attempting to explain why some children eagerly embrace the ambiguities and uncertainties of their environments as opportunities for discovery and surprise, while other children retreat from the world, overwhelmed by an unpredictable landscape they see as marked by signs of threat and risk. (Perez-Edgar et al 2014)”

Pediatric physical therapists often encounter children who exhibit fear related behaviors that interfere with their ability to learn new skills, as well as their ability to function well and participate fully in home, school and community life.

Difficult behaviors range from negative hyper-arousal and poor emotional regulation to fearfulness coupled with avoidance of certain tasks, meltdowns and tantrums,  strong responses to certain sensory events and separation anxiety. All of these behaviors are part of the profile of a child with a fearful temperament disposition, known as behavioral inhibition (BI), coupled with poorly developed emotion and cognitive self-regulation. In some children these behaviors may be a sign of a clinical anxiety disorder.

Recognizing the underlying biological substrates, as well as the environmental factors, that contribute to these difficult behavior patterns allows physical therapists to adopt intervention strategies that promote the child’s ability to regulate his/her fearful behaviors, take on physical challenges and improve self-esteem and self-efficacy.   

Understanding the impact of behavioral inhibition and anxiety is particularly important, as they often co-occur with developmental conditions including developmental coordination disorder,  generalized joint hypermobility, autistic spectrum disorders and ADHD.

Behavioral inhibition, dysregulated fear behaviors and anxiety may also underlie, and possibly be the root cause of many behaviors in children with a diagnosis of sensory processing disorder (SPD).  Certainly sensory over-responsivety (SOR) has been linked to anxiety in children (Lane 2012, Keuler 2011). 

SPD or dysregulated BI and an anxious temperament?

The Sensory Processing Disorder Foundation describes SPD as follows:  “Sensory Processing Disorder (SPD, formerly known as "sensory integration dysfunction")  is a condition that exists when sensory signals don't get organized into appropriate responses. Pioneering occupational therapist and neuroscientist A. Jean Ayres, PhD,  likened SPD to a neurological "traffic jam" that prevents certain parts of the brain from  receiving the information needed to interpret sensory information correctly."

"These difficulties put children with SPD at high risk for many emotional, social, and educational problems, including the inability to make friends or be a part of a group, poor self-concept, academic failure, and being labeled clumsy, uncooperative, belligerent, disruptive, or “out of control.” Anxiety, depression, aggression, or other behavior problems can follow. Parents may be blamed for their children’s behavior by people who are unaware of the child’s “hidden handicap.”   Read more 

Temperament is biologically based  

Temperament refers to biologically based behavioral and emotional tendencies.which are apparent from birth, reflect individual differences in how children and adults select, process, and respond to salient stimuli within their environments and represent a “stable profile with a presumed (also stable) physiological foundation that creates an enduring pattern of thoughts and behaviors that are early appearing and consistent across time and place. In this sense, temperament acts as the bridge between biology and personality .” (Perez Edgar 2014).

Over the past fifty years there have been numerous theories of temperament, with each proposing different constructs to best capture individual differences in emotional and behavioral tendencies. One of the most consistently included constructs is the tendency to approach or avoid novelty. This trait has been referred to as behavioral inhibition to the unfamiliar (Kagan et al.,1984) fear and distress to novelty (Rothbart, 1981), and approach/withdrawal (Thomas and Chess, 1977))

Because novel stimuli are ubiquitous, how one reacts to new people, objects, and environments forms a person's basic behavioral pattern for interacting with the world. (Claus 2015)

Behavioral inhibition as a temperament style

Extract from: Henderson 2015 

Behavioral inhibition (BI) refers to a well-studied temperament style identified reliably in infancy and early childhood. Young children with BI display heightened sensitivity to novel auditory and visual stimuli, and avoid unfamiliar situations and people (Fox et al, 2005).

Toddlers are said to exhibit BI when they are slow to approach unfamiliar stimuli and instead remain in close proximity to caregivers when confronted with novel objects or unfamiliar people.

These behaviors are thought to arise from a lowered threshold to engage neural and physiological systems associated with novelty detection, orienting, and defensive responding. Functionally, the behaviors of toddlers with BI allow an immediate, albeit relatively inflexible, source of regulation by maintaining physical distance between the child and unfamiliar stimuli. 

Infant reactivity as a precursor to BI

Individual differences in responses to novelty are observable very early in life  and observed as high motor activity and crying in response to novel olfactory, visual, and auditory stimuli as early as 4 months of age.  Although such reactive tendencies are not the same as BI, these tendencies are predictive of BI in the toddler years (Henderson et al 2015)

“When presented with benign, but novel, stimuli such as mobiles, puppets, and audio clips, negatively reactive infants at age 4 months respond with negative vocalizations, vigorous limb movements, and arching of the back. In contrast, infants displaying positive reactivity respond to the same stimuli with smiles, positive vocalizations, and limb movements that are active but not tense. Longitudinal work demonstrates that negative reactivity is linked to the later presence of BI, while positive reactivity may be a precursor to temperamental exuberance .” (Perez 2014)

BI in children

The basic underlying trait of inhibited behaviour is a tendency exhibit heightened fear responses to  a variety of situations that are interpreted by the individual as being threatening. Situations and events include:

  • Any event or situation that is new/novel, unpredictable or unexpected.
  • Events or situations that have been labeled as threatening based on previous experience.
  • Activities that the child perceives as difficult .

All children display a range of behaviors when confronted with an event or situation that they perceive as being threatening. The exact nature and strength of the response will depend on the age and experience of the child and the nature of the threat.

Toddlers and preschool children may respond in one of the following ways

  • Inhibited approach – this varies from hesitancy and taking time to approach an unfamiliar toy of person to complete refusal to approach, clinging to a parent or other familiar adult and crying.
  • Emotional displays of fear or heightened arousal
  • Refusal to participate in an activity or poor engagement in tasks
  • Shyness, social reticence, social withdrawal
  • Crying and maintaining close proximity to a parent 

Functionally, the behaviors of toddlers with BI allow an immediate, albeit relatively inflexible, source of regulation by maintaining physical distance between the child and unfamiliar stimuli. (Henderson 2015). 

Older children may display any or all of these behaviors, but may also have some added characteristics including:

  • Fear of failure and elevated monitoring of failure 
  • Intense distress when they fail at a task or make an error 
  • A tendency to not be satisfied with a result that is not perfect – children with BI of are often perfectionists.
  • Some children, in some situations display an attentional bias to threat.
  • Some children with BI also have a tendency to excessive worrying (trait anxiety)
  • BI and dysregulated emotional behavior

    The basic emotions of  anger, fear, surprise, disgust, happiness and sadness are broadly integrative systems ordering feeling, thought and action that represent the meaning or affective significance of events for the person. (LeDoux, 1989), Emotion processing networks address the questions “Is it good for me?,” “Is it bad for me?” and “What shall I do about it?”. (Rothbart 2015)

    Emotional reactions thus include, not only evaluations, but preparations for action and physiological support for those actions (Rothbart, 2011). In other words, what is important is the ability to regulate emotional reactivity in a manner that will facilitate appropriate and adaptive interaction with the environment.

    Goldsmith and Davidson define emotion regulation as the effective calibration of one’s emotional responses to the situation at hand. Failure to appropriately calibrate behavior to specific contexts, or to rigidly apply the same behavior to all types of situations, would constitute one type of dysregulation which may have important consequences for adjustment. Emotion dysregulation can be characterized by emotions that are disconnected from the incentive properties of the situation.

    There are also a group of children with higher levels of behavioral inhibition who show more extreme fear behaviors that may include signs of distress and crying, clinging, withdrawal from the situation, complete refusal to participate even in low threat situations (Buss 2015). The emotional distress is beyond what is expected from the eliciting context or may continue once removed from proximal elicitor.  This extreme fear response even in low threat situations is known as deregulated fear (DF) or high BI and is a risk factor for the development of social anxiety disorder (SAD) and generalized anxiety disorder (GAD). 

    Why would fear in low threat episodes be considered dysregulated?

    Children who do not have a fearful temperament and those with low BI are able to modulate their behavior according to the incentive properties of the situation, including:

    • perception of threat
    • novelty, predictability
    • controllability
    • whether stimulus approaches or stays at a distance
    • availability of coping resources.

     A well regulated fear response is seen when the child is able to recognize these properties in a situation and/or use the resources available to regulate fear across contexts in a flexible manner according to the changing demands of the situation (i.e., regulated fear response).

    In contrast, a dysregulated fear response under these same changing contexts would be reflected by a mismatch between the incentive properties of the situation and the response,  and the mismatch would be most observable in low-threat situations. Buss 2015 argues that  that this may constitute a maladaptive response because it represents a type of rigidity or inflexibility in response (reaction) across contexts.

    It is not the intensity of fear itself, but this type of fear dysregulation that impacts on behavior and is a risk factor for later development of anxiety disorders 

    Bottom up and top down processes interact to shape behavior

    At any given moment a child's social and emotional responses to a situation are shaped by the interaction  between bottom up and top down information processing strategies. 

    Bottom up processes -  BI and defensive responding

    Bottom up processes involve the automatic orientation towards novel stimuli, engaging a network of brain regions centered on subcortical, medial temporal structures, particularly the amygdala' insular cortex and anterior hippocampus, along with components of the ventral prefrontal cortex (PFC) that are most heavily connected to these structures (Posner, 2012). 

    Infants and children with BI show an exaggerated tendency to automatically orient towards novel stimuli, responding to such stimuli as if they are threats. Novel stimuli quickly and markedly engage neural systems supporting salience detection, rapid information processing, and defensive responding.

    "This tendency to quickly and automatically process potential threats is clearly adaptive throughout the lifespan when confronted with truly threatening situations. Nevertheless, for some children, possibly those with particularly stable forms of BI, this highly reactive and automatic style of information processing persists and develops into an over-generalized and biased style of information processing." (Henderson 2015)  

    Top down processes

    Top down information processing strategies involving more controlled, goal-directed activity start to emerge in the pre-school years and continue to mature through childhood. This control mode is described as reflective, endogenous, strategic, logical, and effortful (Hendersen 2015)

    Extract from Hendersen et al 2015

    "Whereas the automatic mode narrows attention to remain responsive to immediately present threats and rewards, the controlled mode is recruited when behavior is goal directed and dependent on the active maintenance of task-related goals, even if these goals are far removed from the immediate context."

    "The control mode incorporates information beyond that which is immediately present, supporting more planful, reasoned and goal-directed behavior in comparison with behaviors regulated by the automatic mode.  For example, engagement of controlled processing in novel contexts may allow BI children to more flexibly attend to and process novel situations and to access and implement previously learned social scripts." 

    "Moreover, controlled processing maintains a prolonged influence on behavior relative to the quick and short-acting influence of the automatic mode of processing." 

    "Controlled processes place extensive cognitive demands on the organism including working memory and self-monitoring and are therefore more resource demanding, less efficient and more slowly engaged than automatic modes of processing. Consistent with such a demanding, complex nature, this processing mode shows a later, more prolonged developmental time course, relative to automatic, reflexive modes of processing that guide behaviors from birth."

    Neural networks in top down control 

    Controlled processes engage a network centered on the dorsolateral prefrontal cortex (DLPFC). The DLPFC in turn draws on other regions that have a role in both controlled and automatic processing. These include the dorsal anterior cingulate gyrus, anterior insula with expanses onto the ventro-lateral PFC, and basal ganglia. ​

    Impact of BI on function, learning  and participation

    Learning a new motor task and improving levels of fitness require mental and physical effort, persistence and repetition in the face of failure, learning from one’s mistakes as well as control of attention to salient aspects of the task. Differences in a child’s responses to perceived threat, monitoring of performance and coping mechanisms may interfere with the engagement in motor tasks.

    Anxious temperament and anxiety sensitivity

    Anxiety sensitivity is the fear of arousal-related sensations (including increased heart rate, sweating, muscle tension, shortness of breath)  based on the beliefs that these sensations may have harmful or negative consequences. Anxiety sensitivity has been conceptualized as an anxiety amplifier; that is, when individuals with high anxiety sensitivity become anxious, they begin to fear their own anxiety-related sensations and become even more anxious (LeBouthillier et al 2014). 

    Anxiety is experienced as unpleasant sensations in the body: it may be felt as constriction in the throat, tightness in the chest with panic like feelings or unpleasant sensations arising from the intestines (butterflies in the stomach). When asked even very young children can usually identify where and how they feel scared. 

    The level of anxiety sensitivity has been shown to moderate behavioral avoidance in anxious youth (Lebowitz 2015). 

    On a clinical level high BI children often appear to be highly sensitive to the effects of effortful exercise which induce the same physiological responses (including increased heart rate, sweating, muscle tension, shortness of breath) that are associated with anxiety provoking circumstances. 

    Recent research has shown that a single bout of aerobic exercise in anxious adults reduces anxiety sensitivity by promoting exposure and habituation to anxiety-related sensations from the body (LeBouthillier et al 2014)

    Avoidance as a coping mechanism

    Children with a strong emotional response to perceived threats often use avoidance as a coping mechanism. At one level avoidance is seen as a shift in attention away from the threat and engagement in less threatening activity. Avoidance responses include attempts to shift the therapists focus of attention away from the task, clowning and chatter. Disruptive behavior in the classroom may also be a sign of avoidance of tasks that provoke anxiety. 

    Avoidance can also take the form of a parasympathetic "freeze" response with complete cessation of activity and refusal to participate in any activities until the perceived threat has been removed and the negative arousal levels have decreased.  

    Attentional bias to threat

    An attentional bias towards threat refers to differential attentional allocation towards threatening stimuli relative to neutral stimuli. 

    Selective attention to threat reflects an adaptive function to protect us from danger. Dysregulation in this adaptive process, termed threat-related attentional bias, is a feature of children with high BI and anxiety disorders.

    Some BI children will initially orient rapidly towards a threatening stimulus, followed by attentional avoidance.  Accordingly, this “vigilance-avoidance” pattern of attention has been used to explain why anxious individuals fail to habituate to threat despite enhanced processing of threat at early stages of information processing.

    Other children’s behavior is characterized by maintained attention to threat and they may find it difficult to disengage from a threatening stimulus. (Cisler 2010, Dodd et al 2015, Morales et al 2015). 

    Performance monitoring and increased sensitivity to error 

    “Learning from errors is fundamental to adaptive human behavior. It requires detecting errors, evaluating what went wrong, and adjusting behavior accordingly. These dynamic adjustments are at the heart of behavioral flexibility and  evidence suggests that deficient error processing contributes to maladaptive rigid and repetitive behavior in a range of neuropsychiatric disorders.”  (Monach 2013)

    Children with BI and an anxious temperament show an increased sensitivity to performance errors.

    Response to errors has been studied using response-locked event-related potential (ERP). Error-related negativity (ERN)  is a negative deflection in the event-related potential (ERP) that peaks at frontocentral sites approximately 50 ms following the commission of an error (Hajcak,2012). 

    "Although original conceptualizations of the ERN emphasized its role in conflict and error detection, findings that this component is moderated by affective and motivational influences suggest a more complex function (Torpey 2009). Specifically, the ERN may reflect a more affective or motivationally salient evaluation of errors and prompt  psychophysiological changes that include skin conductance and heart rate deceleration (Hajcak et al., 2003b; Hajcak, McDonald, & Simons, 2004). These peripheral responses are consistent with both a defensive and orienting response, with a larger  defensive startle reflex following errors than after correct responses (Hajcak & Foti, 2008). The amplitude of the ERN appears to relate to the significance of an error."

    "An ERN can be reliably elicited in children as young as 5–7 years of age, however the ERN response was not as responsive to motivational significance in the same way as seen in adults, in which more valuable errors were associated with a relatively more negative ERN in adults. (Torpey 2013)These differences in ERN are possibly linked to the ACC function and structure which increases with age (Casey et al., 1997). Consistent with these data, the ERN may not reach adult-like levels until the late teen years (Davies, Segalowitz, & Gavin, 2004). "

    Fear triggers in children with high BI

    Feeling physically unsafe and in danger of falling

    Some cautious/fearful children are particularly sensitive to danger and feeling physically unsafe.  In particular they are fearful of trying new activities that have an element of risk.

    Fearful children may avoid climbing on play equipment, jungle gyms, trees, walking on raised surfaces, climbing up steep slopes, playing on see-saws and roundabouts, ladders and slides.

    Riding in an elevator or on an escalator may provoke a fear response. 

    New situations 

    Highly sensitive children who are cautious/fearful children usually approach new situations or activities very hesitantly, and seem nervous or uncomfortable. 

    They get  upset at being left in new situations for the first time  and may take many days to adjust to kindergarten, preschool, or childcare. 

    Busy and noisy environments

    Cautious/fearful children often dislike situations that include lots of people moving around, unexpected noises and events. They do not like surprises. They prefer to be in control. They are also less good at predicting what is going to happen next which means that things that most children expect to happen in the normal course of events turn out to be unexpected for children with high behavioral inhibition and high fear arousal.

    When walking down the aisle of a busy supermarket with many people walking in in different directions we natural look ahead, notice who is coming directly towards us and take action to avoid a collision.  We know how to pay attention to the most important information and filter out unnecessary information and manage to walk along the aisles without bumping into people and things.

    A child with high fear arousal may not be able to filter all out unimportant noise and visual information or be able to select the most important information; they become overwhelmed and are not able to plan their path ahead, instead the child bumps into people and things and may lose sight of mom who has gone around the corner with the trolley. 

    Loud, unpredictable and unexpected noise

    Some children are very sensitive to noise levels, especially unexpected and unpredictable noises. Thunderstorms may provoke a strong fear response. 

    A child may develop a particular dislike and fear reaction to particular sounds such as sirens and when someone shouts loudly.  If a child is a worrier he may react strongly to sounds of loud sirens going off close by:  what does it mean, what has gone wrong, is there a fire, are we in danger?

    Children with high levels of arousal may find too much background noise unpleasant due to poor habituation to low level noise levels. 

    Heightened sensitivity to unexpected noises and poor habituation to even low levels of ambient noise is linked to heightened negative arousal possibly in a circular fashion:  noise in the environment increases arousal levels which in turn increases sensitivity to noise. 

    Children with noise sensitivity usually tolerate noise that they produce themselves since it is expected and anticipation of the particular sound with lead to feed forward modulation and filtering of the sensory input. 

    Fear of unfamiliar adults 

    Some children may be particularly withdrawn or fearful in the presence of strangers. The child may be very shy and refuse to engage with friendly unfamiliar adults even in a safe environment. 

    Shyness with other children 

    Cautious/fearful children may be shy when first meeting new children and reluctant to approach a group of unfamiliar children to ask to join in. They may prefer to watch other children, rather than join in their games.

    Cautiousness and reluctance to engage with other children has important implications for participation in playground activities and organized sport which impacts on the child's physical activity levels and fitness. 

    Hypersensitivity to tactile inputs

    Some children develop a dislike to the feel of clothing with certain textures or clothing that is tight and fits closely. They may also develop a dislike to the feeling of different surfaces and textures under their feet or to the feel of soft and sticky stuff on their hands. 

    The reason for the development of tactile hypersensitivity is not clear.  The argument that it is due to a sensory processing disorder does not take into account the complex nature of how the brain filters, selects and weights sensory information. 

    References and bibliography