One of the most noteworthy functions of the neurocircuitry reviewed above is that these areas and pathways have been shown to have extensive connections with peripheral physiological functioning (Critchley, 2005
; Levenson, 2003
), and specifically to have strong reciprocal connections with the endocrine system (Liberzon et al., 2007
). Though the hypothalamus is clearly important in connecting the brain with the periphery, most of the limbic structures receive peripheral inputs as well as centrally stimulating HPA axis activity (Herman & Cullinan, 1997
; Herman et al., 2003
; Herman, Prewitt, & Cullinan, 1996
), including extensions from the insula and the amygdala to the nucleus of the hypothalamus responsible for triggering the cascade which will cause cortisol release (Risold, Thompson, & Swanson, 1997
). Based on the strength of these connections and the review above which suggests that limbic and paralimbic structures are implicated in empathy-related processes or are altered in callous individuals, individuals who were particularly empathic or callous would be expected to have a corresponding physiological signature in their peripheral physiology.
The limbic system sends and receives several types of peripheral input, including both branches of the stress response. The stress response (e.g., the fight or flight response) is characterized most immediately by sympathetic activity, including release of epinephrine (adrenaline) from the middle of the adrenal gland as a part of the autonomic nervous system (ANS); the release of the parasympathetic brake can also characterize ANS activity (Porges, 1995
). The slower track involves the HPA axis which releases cortisol from the outside of the adrenal gland (Gunnar & Quevedo, 2007
There is a longstanding literature demonstrating ANS associations (both sympathetic and parasympathetic measures) with empathy and related behaviors (see review by Hastings et al., 2006
). Heightened ANS activity is often associated with the experience of personal distress and internalizing of emotions and consequently reduced expression of empathy and prosocial behaviors. Often, however, heightened ANS activity sets the stage for the experience of sufficient amounts of emotional distress to trigger prosocial behavior and caring for others. There is a parallel literature that focuses on the expression of callousness. Several studies from Raine's work highlights low ANS activity in children and adults with callous or antisocial behavior (Blair et al., 1997
; Brennan & Raine, 1997
; Raine, 2002
; Raine, Lencz, Bihrle, LaCasse, & Colletti, 2000
; Raine, Venables, & Mednick, 1997
). A full review of the ANS correlates of empathy and callousness is beyond the scope of this review (and has been done by Hastings et al., 2006
; Raine, 2002
). This next section will focus on the stress hormone cortisol and the Hypothalamic-Pituitary-Adrenal (HPA) axis for several reasons. While cortisol is just one physiological marker, it is an important endpoint of the HPA axis and index of limbic activity.
Peripheral Physiological Signature: A focus on Cortisol
Our focus is on cortisol because the hormonal cascade of the HPA axis begins in the limbic system. While this may be obvious for limbic structures like the hypothalamus, connections of the HPA axis with limbic areas are inclusive and extensive. Vazquez (1998)
and others (Gunnar & Vazquez, 2001
) have changed the terminology to be LHPA (limbic-hypothalamus-pituitary-adrenal) to emphasize that this peripheral endproduct begins and ends largely in emotion-related neurocircuitry. While both the ANS and the HPA have reciprocal connections with the limbic systems, cortisol (much more easily than epinephrine) crosses the blood brain barrier and consequently the brain is a major target organ for cortisol (Gunnar & Quevedo, 2007
). Moreover, cortisol has been shown to be a key modulator of several emotion-related neural functions, including empathy-related or prosocial behaviors as well as emotion-related learning and memory; cortisol has extensive connections with the social brain and those areas that relate to affiliation and social stress (Taylor et al., 2000
). Cortisol maintains strong connections with limbic structures like the hippocampus which facilitates learning and memory, particularly emotion-related memory (Roozendaal, 2000
). Taken together, this raises the possibility that cortisol may serve as a partial mechanism for the deficits in emotional learning and memory evidenced in developmental aspects of psychopathy.
Another reason our focus is on cortisol is because its response profile is slow compared to the nearly immediate reactivity of ANS measures. Likewise, it takes substantially more time for the HPA axis to return to baseline following a stressor, and this recovery is largely a result of negative feedback of peripheral cortisol release on limbic activity, including hypothalamic activity. Consequently, cortisol reactivity or hypoactivity has physiological implications (and by extension, brain activation patterns) across periods of minutes to hours, not milliseconds to seconds (Sapolsky, Romero, & Munck, 2000
). On the other hand, circulating cortisol (i.e., basal levels) or fast-acting nongenomic stress-responsive cortisol levels can have nearly immediate implications for brain activation patterns by changing membrane excitability (Falkenstein, Tillmann, Christ, Feuring, & Wehling, 2000
; Losel et al., 2003
). Thus, cortisol levels are potentially important as both immediate modulators of brain activation as well as potentially responsible for mediating long-term genomic alterations (De Kloet, 2004
; Liberzon et al., 2007
). Cortisol's unique properties also enable it to directly change gene expression. Thus, it not only enters target cells more easily than other hormones but is also able to induce a more dramatic and longer-lasting effect when it arrives. Combined with the observation that cortisol activity and reactivity impact physiology for hours to days and that this impact is largely on limbic neurocircuitry, it is possible that HPA functioning is a major peripheral mechanism to explain how emotion-related neurocircuitry can get disrupted for long periods of time or is permanently altered across development. The long-term and possibly permanent duration of cortisol's effects is important to demonstrate (Gottlieb, 1991
) because disorders of empathy (e.g., psychopathy) are developmental disorders in which symptoms generally persist throughout the life span (Blair, 1995
; Hastings et al., 2000
; Salekin & Frick, 2005
Cortisol's Role in the Neurociruitry of Empathy and Callousness
There are relatively few studies which have directly linked insula activity with the HPA axis. Liberzon and colleagues (2007)
found insula activity in response to traumatic stimuli was associated with adrenocorticotropic hormone (ACTH) responsivity. ACTH from the pituitary gland stimulates the release of cortisol, but this study did not observe direct associations of the insula with cortisol levels or responsivity.
There are several studies which have found associations between cortisol and ACC functioning. This literature is complicated because different indices of HPA activity are frequently employed. Cortisol Reactivity can be thought of as a consequence of brain activation starting in the limbic system, triggering the hypothalamus (Gunnar & Vazquez, 2006
). Emotions should increase activity in the limbic system at the level of stress-appraisal (Eisenberger, Taylor, Gable, Hilmert, & Lieberman, 2007
), while failing to appraise an event as stressful would trigger less HPA axis reactivity. In support, cortisol reactivity to a laboratory stressor has been associated with increased ACC activity later when participants were scanned during a social stressor (Eisenberger et al., 2007
). In a subset of individuals with greater social support, diminished cortisol responses were also associated with reduced ACC activation. In studies by Wang and colleagues (2007
), ACC responses to a laboratory stressor were positively correlated with cortisol reactivity, particularly in females. Electrical stimulation of the ACC results in cortisol increase (Eisenberger et al., 2007
). Cortisol also enhanced ACC activity in response to pain in a fear conditioning task (Stark et al., 2006
). Pretask laboratory cortisol levels (which likely reflect responsivity to laboratory arrival) and ACTH responsivity to traumatic stimuli were positively associated with ACC responsivity (Liberzon et al., 2007
). These studies generally fit with the idea that ACC responsivity is associated positively with HPA responsivity.
A different pattern emerges if negative feedback functioning is analyzed. The administration of cortisol does not parallel a stress response as there is no activation of the HPA axis in the brain. Rather, it indexes the negative feedback of cortisol from the periphery back to the brain. This is parallel to HPA axis activity several minutes/hours after stress reactivity. As expected, these studies show that ACC activity is generally reduced when individuals display dysregulated negative feedback. Males receiving a placebo showed enhanced activity in the ACC during fear conditioning, but sensitivity to fear conditioning was absent when participants received cortisol (Stark et al., 2006
). Another study found individuals who had high cortisol levels despite being given a potent synthetic cortisol (e.g., failed the dexamethasone suppression test) structurally had smaller ACCs than individuals who suppressed the dexamethasone (MacLullich et al., 2006
Basal cortisol is also distinct from stress-reactive cortisol in its basic physiology (de Kloet, 2003
), and the direction of effects on the emotion neurocircuitry (Gunnar & Quevedo, 2007
). Circulating cortisol is more likely to have effects on the brain (i.e., bottom-up effects), whereas reactive cortisol indexes the downstream effects of limbic activation on the periphery. Two studies that examine basal HPA activity (integrated across several time points) show that basal cortisol is associated with reduced ACC functioning. Basal ACTH levels were associated with smaller ACCs in younger and older men (Wolf, Convit, de Leon, Caraos, & Qadri, 2002
). Also, some of our work shows basal cortisol was associated with less ACC activity during emotion regulation in adolescents (Mazzulla et al., 2008
In sum, basal and negative feedback functioning of HPA axis activation appears to reduce ACC activity whereas stress reactive cortisol is more frequently associated with enhanced ACC functioning. If reduced ACC activity is also associated with callousness, it would be expected that callous individuals would have low basal cortisol. Given that they generally have reduced ACC activity, we would in turn expect that their hypoactive ACC (and other limbic structures) would be less able to stimulate a stress response. Consequently, callous individuals would be expected to have reduced cortisol reactivity. Given the relative infrequency of a HPA response, it would further be expected callous individuals would have impaired negative feedback because the bottom-up component of the HPA axis is weakened and untested; negative feedback dysregulation would be further enhanced by hypoactivity of the ACC directly. In short, the expected HPA axis profile of the callous individual mirrors the profile of an individual with a hypoactive ACC.
Animal studies have demonstrated the importance of the amygdala for stimulating HPA axis activity (Hsu, Chen, Takahashi, & Kalin, 1998
; Kalin, Shelton, & Davidson, 2004
), particularly in reference to fear (Kalin, 1993
). Like the ACC, the amygdala enhances HPA activity; it also has many cortisol receptors, suggesting that cortisol in turn helps regulate amygdala activity (Herman & Cullinan, 1997
; Herman et al., 1996
). The amygdala also connects with the hypothalamus, suggesting that its control over the HPA axis is direct (Risold et al., 1997
The human literature reveals that greater amygdala functioning enhances the cortisol stress response. van Stegeren and colleagues (2008
) found that viewing emotional pictures enhanced amygdala activity, and this heightened amygdala functioning was largest in participants with high cortisol levels. Drevets and colleagues (2002)
found that heightened amygdala activity was associated with higher stressed cortisol levels. Finally, Urry and colleagues (2006)
found individuals with a dysregulated diurnal rhythm (shallow declines across the day) had heightened amygdala activity when regulating their emotions. Taken together, these results suggest that stress enhances amygdala functioning which in turn enhances HPA functioning and elevates cortisol levels. Given that callous individuals are expected to have reduced amygdala functioning, it would be predicted that they would likewise show reduced stress responsivity. This prediction parallels that predicted by ACC functioning.
OFC and vmPFC
While the limbic structures like the insula, ACC and amygdala are thought to enhance HPA axis functioning (Herman & Cullinan, 1997
; Herman et al., 1996
), the PFC is more frequently implicated in the inhibition or regulation of the HPA axis (Liberzon et al., 2007
). The distinction between stress reactivity and the bottom-up effects of cortisol on the brain again has bearing on the interpretation of the findings. The top-down role of cortisol is to index stress activation. Since the PFC generally inhibits limbic activity (Goldin, McRae, Ramel, & Gross, 2008
) including hypothalamic release of hormones (Hoover & Vertes, 2007
), one would expect that enhanced PFC activity would be associated with reduced cortisol reactivity. Yet cortisol also feeds back into the brain and has receptors on many key regulatory areas, including the PFC (Lupien & Lepage, 2001
). This feedback is negative, so the anticipated direction of the effect of cortisol on regulatory areas is opposite that of stress reactive cortisol (Liberzon et al., 2007
). If PFC activation reduces the stress response and consequently diminishes the availability of cortisol to effect the brain, then the long-term effects of enhanced PFC activation may lead to aberrant cortisol negative feedback and a reduction in the ability of circulating cortisol to reduce limbic activation. These two opposite predictions are not mutually exclusive because they are differentiated by the timing of the stress response.
There is some ambiguity in the literature about the role of the PFC in relation to cortisol. Negative associations have been reported with the vmPFC (Eisenberger et al., 2007
). Stark and colleagues (2006)
found that the administration of cortisol reduced fear conditioning responsivity in the mPFC and the OFC in males, a well as reduced habituation to the fear conditioned response in other prefrontal areas. Urry and colleagues (2006)
reported greater vmPFC activation with concomitant reduced amygdala activation in individuals with normative declines in cortisol across the day. These studies support an inhibitory role of the PFC on the L-HPA axis.
Opposite findings are also reported. Kern et al (2008)
found that heightened PFC functioning was associated with lower and higher cortisol responses to psychosocial stressors. Wang and colleagues (2007
) found increases in responsivity of the PFC and OFC were positively associated with stress reactivity, particularly in males. ACTH response to traumatic stimuli was associated with mPFC activation in addition to the observed insula and ACC activation (Liberzon et al., 2007
). This positive link between PFC functioning and stress reactivity may be due to anatomical distinctions between subareas of the PFC (ie., the OFC may be behaving as a part of the limbic system rather than a part of the PFC) or may be due to long-term implications of reduced negative feedback on PFC functioning.
Summary and Implications
Peripheral neurobiology is not anticipated to be as straightforward as “low cortisol relates to callousness”. This is due to the HPA axis interaction with neural functioning under basal, reactive and feedback states and these states differentially reflect top-down and bottom-up processes. Predictions for the neurobiology of empathic or callous individuals will focus on limbic activity (especially the predictions based on the ACC and amygdala). The PFC findings are more complex and generally make sense only in terms of the consequences of reduced HPA activation failing to feed back on the PFC.
The first implication of this model is that low basal cortisol may relate to CU traits primarily through bottom-up processes or a failure to prime limbic and paralimbic structures like the ACC or amygdala. The second implication is that hypoactivity in emotion-related neurocircuitry is expected to fail to trigger a stress response or cross a callous individual's threshold for stress activation, so the L-HPA axis (through top-down hypoactivity) produces a diminished stress response. The third expectation is that, over time, negative feedback functioning would be dysregulated, reflecting hypoactivity of the adrenal. Unfortunately, few empirical studies have examined negative feedback functioning.
The next section examines whether the peripheral physiology of empathy fits with a profile of high basal, highly reactive and well-regulated cortisol negative feedback. Conversely, it will be considered whether those with CU or psychopathic traits display HPA axis hypoarousal and, if cortisol reactivity is actually triggered, impaired negative feedback. This section will focus on the literature in children and adolescents because (a) psychopathy is considered a developmental disorder (Frick, 2006
); (b) both empathy and callousness have their roots in early childhood (Frick, Cornell, Bodin et al., 2003
; Zahn-Waxler, 2000
); and (c) because the neurobiology model reviewed above sets forward different predictions for the development vs. the expression of adult psychopathy (Blair, 2007b
). The HPA axis's utility as a peripheral marker depends on its ability to track the emergence of psychopathy and consequently must differentiate empathy or callousness relatively early in childhood.
Cortisol's Role in the Expression of Empathy
Theoretical implications for cortisol's modulatory role on the expression of social and prosocial behavior have been suggested (Swain et al., 2007
; Taylor et al., 2000
), and there is some empirical support. High cortisol reactivity to social novelty was associated with outgoing behavior in socially competent, well-liked preschoolers (Gunnar, Tout, de Haan, Pierce, & Stansbury, 1997
). High cortisol was related to child-initiated social interaction, social competence, popularity, and social affiliation at school (Tennes & Kreye, 1985
; Tennes, Kreye, Avitable, & Wells, 1986
). Evidence for good social skills in high cortisol youth, especially girls, extends across family and peer domains (Booth, Granger, & Shirtcliff, 2008
), and is especially true when adolescents are in social settings (Adam, 2006
). This parallels findings in adult females (Adam & Gunnar, 2001
). Another study highlighted gender differences in that empathic males and systematizing females had higher cortisol levels than those with typical cognitive styles (Nakayama, Takahashi, Wakabayashi, Oono, & Radford, 2007
). Finally, Sethre-Hofstad and colleagues (2002)
found mothers who were more attached with their children showed heightened cortisol responses to watching their child during a stressor, but only when their children also showed stress reactivity; when children were not especially challenged, neither mothers nor children exhibited cortisol reactivity. These findings indicate cortisol may promote social and prosocial behavior, as well as matched or attuned physiological functioning in stressful circumstances.
It is difficult to come to strong conclusions regarding the literature on cortisol and empathy because there is no definitive work on the topic. It is also complicated because cortisol is often associated with anxiety symptoms and other internalizing problems (Stansbury & Gunnar, 1994
). Similar to the ANS literature, it may be that empathic/prosocial behaviors are supported by an optimal level of arousal reflected in moderately high cortisol levels and corresponding level of internal distress that facilitates empathy (Eisenberg, 2007
Cortisol's Role in the Expression of Callousness or Antisocial Behavior
There is a fairly consistent literature that children and adolescents with low basal cortisol have more callous symptoms or antisocial behaviors. HPA hypoactivity extends across a broad range of symptom levels and types, suggesting that this physiological correlate is indexing a continuum of risk rather than a unique signature of psychopathy. Compared to healthy controls, clinic-referred disruptive children (Oosterlaan, Geurts, Knol, & Sergeant, 2005
; Popma et al., 2007
; Scerbo & Kolko, 1994
; van de Wiel, van Goozen, Matthys, Snoek, & van Engeland, 2004
), disruptive children with persistent and early onset aggression (McBurnett, Lahey, Rathouz, & Loeber, 2000
), and children with oppositional defiant or conduct disorder (Kariyawasam, Zaw, & Handley, 2002
; Pajer, Gardner, Rubin, Perel, & Neal, 2001
) have all been found to have low cortisol levels; it is particularly the subgroup of disruptive children with callous symptoms (as opposed to the highly anxious children) who show the greatest evidence of hypoarousal. The link between CU symptoms and low basal cortisol extends to at-risk populations (Granger et al., 1998
; Pajer, Gardner, Kirillova, & Vanyukov, 2001
; Vanyukov et al., 1993
). Low cortisol levels have also been correlated with antisocial behavior across the normal range of externalizing symptoms, especially in boys (Cicchetti & Rogosch, 2001
; Flinn & England, 1995
; Loney, Butler, Lima, Counts, & Eckel, 2006
; Shirtcliff & Essex, 2008
; Shirtcliff, Granger, Booth, & Johnson, 2005
; Smider et al., 2002
; Tennes & Kreye, 1985
). The diurnal rhythm of children with antisocial symptoms may also be dysregulated or blunted, suggestive of an overall impairment in HPA functioning (Fairchild et al., 2008
; Popma et al., 2007
; Shirtcliff & Essex, 2008
; Susman et al., 2007
). While no studies claim a causal link between CU traits and HPA axis hypoactivity, some studies stress that the strong hormonal correlates of conduct or oppositional defiant disorder have clinical applications for use in the assessment of symptom severity and treatment effect in adolescents with externalizing behavior disorders (van de Wiel et al., 2004
; van Goozen, Fairchild, Snoek, & Harold, 2007
A few studies have not found low cortisol in individuals with more externalizing symptoms (van Bokhoven et al., 2005
), but these studies had small sample sizes (Kruesi, Schmidt, Donnelly, Hibbs, & Hamburger, 1989
), or focused on populations characterized by attention and inhibitory externalizing symptoms rather than CU traits or antisocial behavior (de Haan, Gunnar, Tout, Hart, & Stansbury, 1998
; Gunnar et al., 1997
; Sondeijker et al., 2007
). While attention problems are within the disruptive behavior spectrum, they do not define CU traits as core symptoms and they do not necessarily show continuity with adult psychopathy. This gulf between subgroup criteria led some studies to compare subgroups within the disruptive behavior spectrum (McBurnett et al., 2005
). In one such study only the oppositional defiant youth (with or without comorbid attention problems) showed weaker cortisol responsive relative to controls; the attention problem group paralleled control youth (van de Wiel et al., 2004
). This implies that not only does low cortisol serve as a good predictor of externalizing behavior, but it can also help to distinguish between subtypes as well.
Attenuation in cortisol reactivity is also evident in children with CU traits or antisocial behavior (Susman, 2006
). Children with oppositional defiant or conduct disorder had smaller cortisol responsivity to a frustration task (Fairchild et al., 2008
; Snoek, Van Goozen, Matthys, Buitelaar, & van Engeland, 2004
; Van Goozen, Matthys, Cohen-Kettenis, Buitelaar, & Van Engeland, 2000
; Van Goozen et al., 1998
); this was most evident when problems persisted during treatment (van de Wiel et al., 2004
). Within at-risk youth, the magnitude of stress hyporesponsivity was associated with aggressive and impulsive symptoms (Moss, Vanyukov, & Martin, 1995
). Cortisol reactivity was likewise blunted in normally developing youth with more concurrent and subsequent aggressive and disruptive behavior symptoms (Granger, Stansbury, & Henker, 1994
). Interestingly, Brotman and colleagues (2007)
found at-risk youth (who had an adjudicated sibling) also demonstrated an attenuated stress response, but this pattern normalized as they received a therapeutic family-based intervention. Contrarily, higher cortisol reactivity was associated with externalizing symptoms in normally developing youth in two studies (Susman, Dorn, Inoff-Germain, Nottelman, & Chrousos, 1997
; Tout, de Haan, Campbell, & Gunnar, 1998
), and one study involving youth with conduct problems (McBurnett et al., 2005
). Nevertheless, the overall pattern is for low basal and blunted reactivity to stress in youth with CU symptoms.
Given that psychopathy is considered a developmental disorder, the above literature review on reduced HPA functioning in children and adolescents may have bearing on the development of psychopathy (van Honk & Schutter, 2006
). Burke and colleagues (2007)
found that cortisol in adolescents predicted callousness when the youth were young adults. Other studies have found basal cortisol was lower in individuals with more psychopathic traits (Holi, Auvinen-Lintunen, Lindberg, Tani, & Virkkunen, 2006
; van Honk, Schutter, Hermans, & Putman, 2003
). Relatedly, cortisol's diurnal rhythm was blunted within a subsample of psychopathic criminals compared to incarcerated non-psychopaths (Cima, Smeets, & Jelicic, 2008
). Finally, individuals scoring higher on psychopathy measures show reduced cortisol responsivity to laboratory (Dishman, Wallace, Crawford, Grant, & Hinton, 1982
; O'Leary, Loney, & Eckel, 2007
) and pharmacological stressors (Netter, Hennig, & Rohrmann, 1999
), suggesting that the overall pattern of blunted HPA levels and reactivity in children and adolescents with antisocial behavior has developmental extensions and unique predictive value with psychopathic characteristics in adults.
Summary and Integration: What does not stress me should not stress another
The neurocircuitry involved in both empathy and callousness and in their overlap promotes prosocial and empathic concern, and by extension moral decision-making, by co-opting brain areas that instantiate physical and social distress. Activation in response to distress extends to witnessing distress cues/contexts and the expression of distress in others. These brain areas receive substantial peripheral input and are responsible for integrating peripheral signals with concurrent neural processes. Cortisol levels and HPA responsivity are implicated in the functioning of these brain areas through bottom-up modulation and top-down activation, respectively. Peripheral signals like cortisol enhance activation in this neurocircuitry. Contrarily, diminished HPA activity reduces the potential degree of activation in empathy-related neurocircuitry, further reducing the potential for stress reactivity to begin in the L-HPA axis. The hypoactivity of the stress system is expected to perpetuate itself over time. The involvement of peripheral physiology at multiple levels suggests a basic mechanistic impairment in CU individuals.
Our suggestion is not that social information processing in CU individuals (or the heightened sociality in empathic individuals) is due to deficits in sociality or impairment in the representation of self. If it were, then callous individuals would have substantially greater difficulty in finding adequate alternative strategies, such as manipulating others' emotions (Pardini et al., 2003
; Waschbusch, Walsh, Andrade, King, & Carrey, 2007
). Also, it would not be expected that cortisol would relate to empathy or callousness because cortisol is associated with neural activation in areas that fire regardless of whether pain or distress is signaled by the self vs. other. Yet, HPA hypoactivity is not expected to be specific to the distress of another because cortisol modulates neural activity regardless of the object of distress. Individuals with reduced basal and reactive HPA axis are expected to fail to respond to emotional or stressful experiences that they themselves experience as well as fail to respond to similar stimuli experienced by another.
Especially with areas like the insula or ACC, this neural network illustrates how an individual feels the emotions/ stressors of another as though they experienced those emotions/ stressors themselves. The appearance of a lack of empathy is that individuals with CU traits consistently have a blunted stress response and hypo-responsive physiological input to the neurocircuitry described above. If the callous individual were in the same social context as a distressed conspecific, the callous individual would not trigger a stress response. Their representation of another's stress or emotion would be similarly blunted and they would fail to feel distress. The appearance of callousness is a consequence of a brain with a high threshold for detecting stress or registering arousal. It is not a mismatch between the representation of the self vs. other but rather a mismatch between what any two people experience as stressful.
Support for the hypoarousal model in populations with high thresholds
Is there evidence that people who under-represent emotion, pain or stress show impairments in empathy? A handful of studies have explored this question outside of populations defined as CU (so as to avoid a circular argument) (Hein & Singer, 2008
). Individuals with a congenital insensitivity to pain (CIP), who presumably do not have a strong representation of pain in self, show reduced emotional responses to pain eliciting stimuli and impairments in inferences about the amount of pain experienced by others based on facial expressions or event descriptions (Danziger, Prkachin, & Willer, 2006
). Underestimations were especially large when other emotional cues were lacking, suggesting CIP patients used alternative strategies to empathy. Individuals with lower physical pain thresholds also have lower sensitivity to social pain and distress (Eisenberger, Jarcho, Lieberman, & Naliboff, 2006
). Individuals who have difficulty expressing their emotions (i.e., alexithymia patients) also under-estimate the experience of pain in themselves and others, and have low empathy scores (Moriguchi et al., 2007
). Interestingly, individuals with alexithymia also showed reduced neural activation to painful situations in the ACC, suggesting this under-representation of distress may be instantiated in the empathy-related neurocircuitry as well as the periphery.
That individuals scoring higher on psychopathy scales likewise appear less responsive to stress or pain (Errico, Parsons, King, & Lovallo, 1993
; O'Leary et al., 2007
) raises the possibility that callous individuals display a similar mechanistic impairment in pain or emotion processing as opposed to a self vs. other impairment. That psychopaths also are reported to use alternative strategies to empathy (like the congenital insensitivity to pain patients) to process social information supports a mechanistic link 1
. Hallmark symptoms of psychopathic individuals include the ability to manipulate others' emotions and are conscious of impression management (Forth, Kosson, & Hare, 2003
). Psychopaths appear aware of the emotions of others without viscerally feeling the emotions of others.
Support for the hypoarousal model in contexts which are no longer stressful
Another way to distinguish whether the impairment in CU individuals is at the level of stress appraisal/activation as opposed to the self vs. other distinction is to ask whether individuals in specific contexts that they do not consider stressful show alterations in empathy-related processes. This context-specific perspective was initially criticized because empathy was considered a fast, automatic response (Preston & de Waal, 2002
). It was difficult to theorize how something involuntary could be modulated by context, yet familiarity and fairness are frequent modulators of empathy-related neural processing and the personal distress one feels for another (Hein & Singer, 2008
; Singer, 2007
; Singer et al., 2006
). Indeed, past experience with an unfair person can change neural activation patterns from an empathic distress signal to activation in reward areas in response to observing their pain (Fehr & Rockenbach, 2004
). Thus, past experience with a person or event as well as stress appraisal modulates empathic neuronal responses (de Vignemont & Singer, 2006
; Hein & Singer, 2008
There has been additional support for the hypoarousal model from another perspective. Cheng and colleagues (2007)
found that acupuncture physicians activated regulatory brain areas in response to viewing needles being inserted into body parts; nonphysicians activated the empathy-related neurocircuitry like the ACC and insula. Cheng (2007)
and others (de Vignemont & Singer, 2006
) suggest that behavioral responses in these types of contexts would be limited to cognitive forms of mentalizing rather than empathizing, again suggesting that alternative strategies are employed when empathizing is not supported by physiological arousal.