Rapid habituation of response to stress is a frequently reported characteristic of the HPA axis. Habituation can be defined as a decrement in responsiveness to a stimulus following repeated exposure. In the field of neuroendocrine stress research, habituation usually refers to a reduction in magnitude and/or intensity of the initial psychoneuroendocrine stress response following repeated exposure to an initially novel homotypic stressor (Grissom & Bhatnagar, 2009). Considering the metabolic cost of mounting an acute glucocorticoid response, and the potentially deleterious effects of prolonged exposure, habituation is most likely adaptive. Indeed, a failure to habituate or adjust to repeated exposure to the same stressor underpins the allostatic load state; namely repeated hits, prolonged exposure, inadequate response and lack of adaptation (McEwen, 1998a).
Rodents demonstrate decreased corticosterone responsiveness following repeated restraint (Bhatnagar, Huber, Nowak, & Trotter, 2002; Grissom, Iyer, Vining, & Bhatnagar, 2007), immobilisation (Garcia, Marti, Valles, Dal-Zotto, & Armario, 2000),
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and noise stress (De Boer, Van der Gugten, & Slangen, 1989). The cortisol response in humans has been shown to quickly habituate in a number of stress contexts including repeated parachute jumps (Deinzer, Kirschbaum, Gresele, & Hellhammer, 1997) and to psychosocial stress protocols (Federenko et al., 2004; Gerra et al., 2001; Jonsson et al., 2010; Kirschbaum, Pruessner et al., 1995; Schommer, Hellhammer, & Kirschbaum, 2003). Habituation of HPA axis mediated responses has also been shown to increase progressively with each exposure (Deinzer et al., 1997; Gomez, Houshyar, & Dallman, 2002). Habituation in response appears to be specific to the HPA axis. Biomarkers of SAM and SS activation (e.g., EPI, NE, blood pressure [BP]) tend to have comparatively uniform activation patterns across repeated stress exposures (Gerra et al., 2001; Mischler et al., 2005; Schommer et al., 2003; von Kanel, Kudielka, Preckel, Hanebuth, & Fischer, 2006; von Kanel et al., 2004).
A number of psychological characteristics, including novelty, predictability, controllability, and threats to the social-self have been identified as key psychological attributes associated with HPA axis-mediated stress responses (see Section 1.3.1). Repeated exposure to a homotypic stressor is likely to reduce the moderating influence of these psychological characteristics on the engendered response as the contextual and psychological elements of the stressor will be perceived as more familiar, predictable and controllable (Harl, Weisshuhn, & Kerschbaum, 2006; Schommer et al., 2003; Voigt, Ziegler, Grunertfuchs, Bickel, & Fehmwolfsdorf, 1990).
A number of additional factors have been shown to influence habituation of glucocorticoid stress response. Rodent models suggest the HPA axis habituates predominantly to processive (psychological) stressors, and less to physiological (physical) stressors that involve a proximate physical threat (Grissom & Bhatnagar, 2009). Indeed, different neural pathways may underpin HPA axis responses to processive and physiological stressors. Processive stressors primarily activate the PVN via limbic pathways, whilst rapid activation of the PVN via brainstem nuclei, without significant activation of limbic circuitry, has been demonstrated to underpin responses to physical stressors (Emmert & Herman, 1999).
Frequency of stressor exposure is also relevant for HPA axis habituation. In rodents, the more frequent the exposure to stress the more rapid and pronounced the habituation in corticosterone response (Deboer, Koopmans, Slangen, & Van der Gugten, 1990; Ma & Lightman, 1998). A similar effect of frequency may apply to human cortisol habituation but the relationship is less defined. A number of studies
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have exposed participants to repeated TSSTs (or modified TSST) separated by intervals of 24 hrs (Epel et al., 2000; Jonsson et al.; Kirschbaum, Pruessner et al., 1995), seven days (Engert et al., 2010; Gerra et al., 2001; von Kanel et al., 2006; Wust, Federenko et al., 2005), and four weeks (Schommer et al., 2003). Overall, mean cortisol responses habituated over repeated exposures. However, Petrowski, Wintermann, and Siepmann (2012) reported that an interval of 10 weeks was sufficient to reinstate previously habituated cortisol responses. Participants were exposed to the TSST on four occasions: time 1 and time 2 separated by 24 hrs; time 3 after an interval of 10 weeks; and time 4 completed 24 hrs after time 3. Cortisol responses to the TSST’s habituated when exposures were separated by 24 hrs (time 1 vs. time 2 and time 3 vs. time 4), but no habituation in responses was demonstrated between the TSST’s separated by an interval of 10 weeks (time 2 vs. time 3).
The considerable individual variability in HPA axis responses to stress provocation is further reflected in patterns of individual variability in habituation of response. Despite an overall mean pattern of habituation in cortisol response to repeated psychosocial laboratory stressors, a subgroup of non-habituating individuals is often reported. This subgroup usually accounts for approximately one-third of the sample (Gerra et al., 2001; Kirschbaum, Pruessner et al., 1995; Schommer et al., 2003; Wust, Federenko et al., 2005). A smaller proportion of individuals have been shown to demonstrate a sensitisation of response (approximately 16%; Wust et al., 2005). The factors underlying this non-habituation are yet to be fully elucidated. Pruessner et al. (1997) reported that a subset of non-habituators in their study were characterised by a sub- dominance, externally controlled orientation, and insecurity. Kudielka, Bellingrath, & Hellhammer (2006) reported that vital exhaustion, a sequela of chronic stress characterised by high fatigue and loss of energy, was associated with non-habituation in cortisol responses in a small subset of the sample (n = 6). Moreover, an association between heightened cortisol responsivity to psychosocial stress and vital exhaustion is yet to be consistently demonstrated (Kristenson, Kucinskiene, Bergdahl, & Orth- Gomer, 2001; Kristenson et al., 1998; Nicolson & Van Diest, 2000).
Rohleder et al. (2007) reported that the typical pattern of cortisol habituation does not necessarily occur in dancers over repeated exposure to competition stress. No significant differences between cortisol responses over three consecutive competitions or as a function of level of previous competition experience were revealed. The threat of losing social standing related to a skill intimately linked to social status and identity is proposed to underpin this apparent lack of habituation in cortisol response. The
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drive to preserve the social self in the face of social-evaluative threat may be so fundamental that, as with threats to the physical self, the cortisol response does not readily habituate. It should be noted that Rohleder et al., were unable to assess responses to competitors first ever competitions, which may well have been even greater in magnitude. However, response decrease towards abolishment over the three competitions would be expected rather than the significant cortisol excursions above baseline levels demonstrated. Further evidence of reduced habituation of cortisol responses to naturalistic stress, more intimately tied to goals and identity was reported by Schoofs, Hartmann, & Wolf (2008b). Salivary cortisol and α-amylase (sAA; a marker of sympathetic activation) responses to a statistical oral examination did not significantly habituate to repeated exposure after three weeks.