Amygdala involvement in human avoidance, escape and approach behavior Page: 2
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Schlund and Cataldo Page 2
avoidance-escape motivated by negative emotional states. For example, chronic coping in
posttraumatic stress disorder often involves avoidance of uncontrollable intrusive memories
(Brewin and Holmes, 2003). Features of panic disorder have been linked to avoidance of
Z catastrophic appraisals of panic sensations (Clark, 1986). Obsessive-compulsive disorder is
associated with avoidance-escape strategies designed to reduce negative cognitions or
emotions, particularly in fear-contamination. Chronic avoidance-escape coping emerges in
borderline personality disorder as nonsuicidal, deliberate self-harm to deal with negative
thoughts or emotions. High levels of negative emotion (e.g., hostility, guilt, sadness) or anxiety
o may also prompt deliberate self-harm in nonclincial populations (Brown et al., 2007; Klonsky
et al., 2003). Within substance abusing populations, negative affect (anxiety), social (potential
loss of using friends), stress and aversive biological states associated with drug withdrawal can
similarly motivate avoidance-escape in the form of drug seeking and facilitate drug relapse
(Blume, 2001; Downs and Woods, 1975; Koob, 2009; Sinha, 2007). Such examples highlight
how avoidance-escape commonly functions to control or modify aversive or threatening
aspects of the environment or internal states (i.e, thoughts, emotions, bodily sensations), thus
working as a basic emotion regulation strategy (Gross and Thompson, 2009; Hayes et al
Although avoidance-escape behavior is a recognized feature of many clinical disorders, our
understanding of the neurocircuitry supporting adaptive human avoidance-escape remains
poor. Consequently, progress has been limited in understanding transitions from adaptive to
Z chronic forms of avoidance-escape and differences in avoidance neurocircuitry among clinical
disorders. Neurophysiological research on adaptive forms of avoidance has implicated the
amygdala in nonhuman (Poremba and Gabriel, 1997, 1999; Roozendaal et al., 1993; Werka et
al., 1978) and human avoidance learning (Mobbs et al., 2009). There is also evidence linking
amygdala dysfunction to mood disorders characterized by avoidance behavior (Etkin and
" Wager, 2007). The amygdala's role in avoidance has been hypothesized to be limited to fear-
-conditioning, where a conditioned cue/threat signals the delivery of an aversive event (e.g.,
shock) (Cain and LeDoux, 2008; Werka et al., 1978). This view is consistent with two-factor
theories of avoidance that propose threatening fear-conditioned cues motivate avoidance and
removal of cues and fear-reduction serve to negatively reinforce avoidance (Miller, 1948;
Mowrer, 1947; but also see Bolles, 1972, Herrnstein, 1969). Considerable evidence shows
avoidance is also associated with increased reported fear and catastrophic thoughts (Eifert and
Heffner, 2003) and increased skin conductance responses (Jensen et al, 2003; Mobbs et al.,
2009; Rose et al., 1995; Solomon et al., 1980). Clinical research also suggests avoidance, such
as the intentional suppression of undesirable or distressing emotions, can be counterproductive
and can paradoxically enhance, or at least maintain, self-reported negative experiences, anxiety
and physiological responses (Campbell-Sills et al., 2006; Cioffi and Holloway, 1993; Feldner
Z et al., 2006; Spira et al., 2004). While such results suggest ties among the amygdala, avoidance
and fear/anxiety, other investigations have shown that learned avoidance in nonhumans is not
dependent upon the amygdala (Andrzejewski, et al., 2005; Lehmann et al., 2000; Poremba and
> Gabriel, 1997, 1999; Roozendaal et al., 1993), avoidance learning in humans is associated with
Declines in skin conductance responses to fear-conditioned cues (Lovibond et al., 2008) and
avoidance cues fail to elicit amygdala activation in humans, but consistently prompts activity
o in the striatum (Jensen et al, 2003; Kim et al., 2006).
SThe relative paucity of research on the neurocircuitry supporting adaptive forms of human
Savoidance-escape and the mixed findings within the avoidance literature represent important
gaps in our knowledge. In this functional magnetic resonance imaging investigation, our
primary aim was to examine amygdala reactivity to threatening cues when avoidance
responding consistently prevents contact with an upcoming aversive event, a process which
models central features of many forms of psychopathology. Our secondary aim included
Examining reported amygdala contributions to escape from a proximal aversive event (Gold
Neuroimage. Author manuscript; available in PMC 2011 November 1.
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Schlund, Michael W. & Cataldo, Michael F. Amygdala involvement in human avoidance, escape and approach behavior, article, November 1, 2010; [Amsterdam, Netherlands]. (digital.library.unt.edu/ark:/67531/metadc77178/m1/2/: accessed March 23, 2017), University of North Texas Libraries, Digital Library, digital.library.unt.edu; crediting UNT College of Public Affairs and Community Service.