Neuronal Correlates of Social Cognition in BPD
Neuronal Correlates of Social Cognition in BPD
Patients with borderline personality disorder (BPD) have severe problems in social interactions that might be caused by deficits in social cognition. Since the findings about social-cognitive abilities in BPD are inhomogeneous, ranging from deficits to superior abilities, we aimed to investigate the neuronal basis of social cognition in BPD. We applied a paradigm with three social cognition tasks, differing in their complexity: basal processing of faces with a neutral expression, recognition of emotions, and attribution of emotional intentions (affective ToM). A total of 13 patients with BPD and 13 healthy matched controls (HCs) were included in a functional magnet resonance imaging study. BPD patients showed no deficits in social cognition on the behavioral level. However, while HCs showed increasing activation in areas of the mirror neuron system with increasing complexity in the social-cognitive task, BPD patients had hypoactivation in these areas and hyperactivation in the amygdala which were not modulated by task complexity. This activation pattern seems to reflect an enhanced emotional approach in the processing of social stimuli in BPD that allows good performance in standardized social-cognitive tasks, but might be the basis of social-cognitive deficits in real-life social interactions.
Borderline personality disorder (BPD) is a psychiatric disorder characterized by prominent deficits in affect regulation (Putnam and Silk, 2005) and social functioning (Skodol et al., 2002; Hill et al., 2008). Patients with BPD and persons with BPD traits distinguish themselves from individuals without BPD-traits by negative perception (Benjamin and Wonderlich, 1994; Meyer et al., 2004) and expectations of others (Barnow et al., 2009). These impairments in social settings might be conceptualized as deficits in the domain of social cognition.
The term social cognition refers to the processing of all information that culminates in the perception of the intentions and dispositions of an individual (Brothers, 1990). According to Brothers (1990), social cognition comprises different processing stages that are all related to social interactions, starting from the perception of an interaction partner, via the recognition of emotions, to the recognition of intentions. In light of this model, one might ask whether the impairments of BPD patients observed during social interactions can be linked to dysfunctions in one particular processing stage or occur at all levels, in terms of a generalized alteration in the processing of social information.
Although studies on emotion recognition constitute the main area of research in social cognition in BPD their number is still small and their results are heterogeneous, ranging from findings of deficits (Levine et al., 1997; Bland et al., 2004; Guitart-Masip et al., 2009; Unoka et al., 2011), comparable performance with healthy controls (HCs; Minzenberg et al., 2006; Domes et al., 2008; Dyck et al., 2009) to increased sensitivity (Lynch et al., 2006). Results from studies on the attribution of emotion to neutral or ambiguous facial expressions range from no deficit (Levine et al., 1997; Bland et al., 2004;) to a tendency to attribute negative emotions to neutral faces or ambiguous emotional expressions (Wagner and Linehan, 1999; Domes et al., 2008; Dyck et al., 2009).
The ability to recognize mental states, such as intentions, wishes, and desires of oneself and of others can be conceptualized as theory of mind (ToM; Premack and Woodruff, 1978). A concept very close to ToM is mentalizing: the capacity to implicitly and explicitly understand oneself and others through subjective states and mental processes (Fonagy and Bateman, 2008). It is supposed that in BPD the ability to mentalize develops insufficiently due to an insecure attachment style and an insufficiently marked mirroring of the emotional state by the caretaker during the early development of the patients (Fonagy and Bateman, 2008). However, studies on ToM in BPD point towards no deficit (Murphy, 2006; Harari et al., 2010), or only a subtle one (Preissler et al., 2011), or even a superiority in BPD (Arntz et al., 2009; Fertuck et al., 2009; Franzen et al., 2011). Especially, interesting is a study, by Harari et al. (2010), showing that patients with BPD are superior in affective ToM (the ability to recognize affective mental states), while showing equal performance in cognitive ToM (the ability to recognize mental states without the aid of emotional information).
From a neurobiological perspective, several brain structures have been discussed as being substantially involved in social cognition. While the perception of faces in general is mainly based on the inferior occipital lobe, the fusiform gyrus and the superior temporal suclus (STS), emotion recognition additionally recruits the amygdala and the insula (Haxby et al., 2000; Fusar-Poli et al., 2009). If the recognition of intentions is required as in ToM, prefrontal areas, such as the anterior cingulate and the inferior prefrontal gyrus are recruited for task solving (Gallese and Goldman, 1998; Frith and Frith, 2006). One network that seems to be especially important for the recognition of intentions is the mirror neuron system (MNS). The MNS is the place where the matching of one's own motor representation and the motor representation of others seem to coincide by a simulation mechanism (Gallese and Goldman, 1998). Areas that belong to the human MNS are the inferior prefrontal gyrus, specifically Brodmann area 44 (BA 44), the inferior parietal lobe and associated the superior temporal sulcus (STS) (Iacoboni et al., 2001; Rizzolatti and Craighero, 2004). However, it was demonstrated recently that neurons with mirror properties can also be found outside of these areas, such as in the medial temporal lobe, in the somatosensory cortices, and in the anterior cingulate cortex (Keysers and Gazzola, 2010; Keysers et al., 2010; Mukamel et al., 2010). In addition, if intentions are linked to affective states, as in affective ToM, intention recognition also seems to be associated with an activation in the amygdala (Baron-Cohen et al., 1999; Castelli et al., 2000; Gallagher and Frith, 2004) that exceeds the already observed activation during emotion recognition (Mier et al., 2010).
Several brain imaging studies concordantly point to a particular importance of the amygdala for social-cognitive deficits in BPD. Hyperactivation in the amygdala in BPD was found during the presentation of negative scenes (Herpertz et al., 2001; Koenigsberg et al., 2009a, 2009b) as well as during the processing of neutral and emotional facial expressions (Donegan et al., 2003; Minzenberg et al., 2007). To the best of our knowledge, there are no studies investigating the neuronal bases of ToM in BPD, until now. However, there are some studies giving evidence for alterations in BPD in the MNS. Koenigsberg et al. (2009a) found increased STS-response to negative pictures in BPD, Dziobek et al.(2011) reported decreased STS-activation in BPD associated with cognitive empathy, and Juengling et al.(2003) investigating metabolism during resting-state demonstrated decreased inferior prefrontal glucose consumption.
Taken together, while the results about social cognition in BPD on the behavioral level are rather inconclusive, functional imaging studies point more homogeneously to a hyperactivation of the amygdala in response to social stimuli. Thereby alterations are reported on different stages of social cognition. However, in none of the studies, different stages of social cognition were investigated together in one paradigm and, in none of these studies, ToM was assessed. As a first attempt to study neural correlates of ToM in BPD, we applied a paradigm, including affective ToM-, emotion recognition-, and basal face processing-tasks (Mier et al., 2010a, b). This enabled us to investigate whether possible alterations in affective ToM are specific to the intention recognition process or rather based on a global deficit in the processing of social stimuli. Based on the literature, we did not assume finding performance deficits in BPD, but alterations in the neuronal activation associated with the tested social-cognitive tasks. We hypothesized that patients with BPD show hyperactivation in the amygdala already at the lowest stage of processing i.e. the processing of neutral faces without the necessity to attribute an emotional state. In addition, it was hypothesized that the more complex social cognition processes, i.e. emotion recognition and affective ToM, are associated with additional aberrations in cortical structures. Especially, we were interested in alterations regarding structures linked to the simulation of intentions, namely areas of the MNS, such as the STS and BA 44 (Rizzolatti and Craighero, 2004; Iacoboni et al., 2005; Mier et al., 2010a).
Abstract and Introduction
Abstract
Patients with borderline personality disorder (BPD) have severe problems in social interactions that might be caused by deficits in social cognition. Since the findings about social-cognitive abilities in BPD are inhomogeneous, ranging from deficits to superior abilities, we aimed to investigate the neuronal basis of social cognition in BPD. We applied a paradigm with three social cognition tasks, differing in their complexity: basal processing of faces with a neutral expression, recognition of emotions, and attribution of emotional intentions (affective ToM). A total of 13 patients with BPD and 13 healthy matched controls (HCs) were included in a functional magnet resonance imaging study. BPD patients showed no deficits in social cognition on the behavioral level. However, while HCs showed increasing activation in areas of the mirror neuron system with increasing complexity in the social-cognitive task, BPD patients had hypoactivation in these areas and hyperactivation in the amygdala which were not modulated by task complexity. This activation pattern seems to reflect an enhanced emotional approach in the processing of social stimuli in BPD that allows good performance in standardized social-cognitive tasks, but might be the basis of social-cognitive deficits in real-life social interactions.
Introduction
Borderline personality disorder (BPD) is a psychiatric disorder characterized by prominent deficits in affect regulation (Putnam and Silk, 2005) and social functioning (Skodol et al., 2002; Hill et al., 2008). Patients with BPD and persons with BPD traits distinguish themselves from individuals without BPD-traits by negative perception (Benjamin and Wonderlich, 1994; Meyer et al., 2004) and expectations of others (Barnow et al., 2009). These impairments in social settings might be conceptualized as deficits in the domain of social cognition.
The term social cognition refers to the processing of all information that culminates in the perception of the intentions and dispositions of an individual (Brothers, 1990). According to Brothers (1990), social cognition comprises different processing stages that are all related to social interactions, starting from the perception of an interaction partner, via the recognition of emotions, to the recognition of intentions. In light of this model, one might ask whether the impairments of BPD patients observed during social interactions can be linked to dysfunctions in one particular processing stage or occur at all levels, in terms of a generalized alteration in the processing of social information.
Although studies on emotion recognition constitute the main area of research in social cognition in BPD their number is still small and their results are heterogeneous, ranging from findings of deficits (Levine et al., 1997; Bland et al., 2004; Guitart-Masip et al., 2009; Unoka et al., 2011), comparable performance with healthy controls (HCs; Minzenberg et al., 2006; Domes et al., 2008; Dyck et al., 2009) to increased sensitivity (Lynch et al., 2006). Results from studies on the attribution of emotion to neutral or ambiguous facial expressions range from no deficit (Levine et al., 1997; Bland et al., 2004;) to a tendency to attribute negative emotions to neutral faces or ambiguous emotional expressions (Wagner and Linehan, 1999; Domes et al., 2008; Dyck et al., 2009).
The ability to recognize mental states, such as intentions, wishes, and desires of oneself and of others can be conceptualized as theory of mind (ToM; Premack and Woodruff, 1978). A concept very close to ToM is mentalizing: the capacity to implicitly and explicitly understand oneself and others through subjective states and mental processes (Fonagy and Bateman, 2008). It is supposed that in BPD the ability to mentalize develops insufficiently due to an insecure attachment style and an insufficiently marked mirroring of the emotional state by the caretaker during the early development of the patients (Fonagy and Bateman, 2008). However, studies on ToM in BPD point towards no deficit (Murphy, 2006; Harari et al., 2010), or only a subtle one (Preissler et al., 2011), or even a superiority in BPD (Arntz et al., 2009; Fertuck et al., 2009; Franzen et al., 2011). Especially, interesting is a study, by Harari et al. (2010), showing that patients with BPD are superior in affective ToM (the ability to recognize affective mental states), while showing equal performance in cognitive ToM (the ability to recognize mental states without the aid of emotional information).
From a neurobiological perspective, several brain structures have been discussed as being substantially involved in social cognition. While the perception of faces in general is mainly based on the inferior occipital lobe, the fusiform gyrus and the superior temporal suclus (STS), emotion recognition additionally recruits the amygdala and the insula (Haxby et al., 2000; Fusar-Poli et al., 2009). If the recognition of intentions is required as in ToM, prefrontal areas, such as the anterior cingulate and the inferior prefrontal gyrus are recruited for task solving (Gallese and Goldman, 1998; Frith and Frith, 2006). One network that seems to be especially important for the recognition of intentions is the mirror neuron system (MNS). The MNS is the place where the matching of one's own motor representation and the motor representation of others seem to coincide by a simulation mechanism (Gallese and Goldman, 1998). Areas that belong to the human MNS are the inferior prefrontal gyrus, specifically Brodmann area 44 (BA 44), the inferior parietal lobe and associated the superior temporal sulcus (STS) (Iacoboni et al., 2001; Rizzolatti and Craighero, 2004). However, it was demonstrated recently that neurons with mirror properties can also be found outside of these areas, such as in the medial temporal lobe, in the somatosensory cortices, and in the anterior cingulate cortex (Keysers and Gazzola, 2010; Keysers et al., 2010; Mukamel et al., 2010). In addition, if intentions are linked to affective states, as in affective ToM, intention recognition also seems to be associated with an activation in the amygdala (Baron-Cohen et al., 1999; Castelli et al., 2000; Gallagher and Frith, 2004) that exceeds the already observed activation during emotion recognition (Mier et al., 2010).
Several brain imaging studies concordantly point to a particular importance of the amygdala for social-cognitive deficits in BPD. Hyperactivation in the amygdala in BPD was found during the presentation of negative scenes (Herpertz et al., 2001; Koenigsberg et al., 2009a, 2009b) as well as during the processing of neutral and emotional facial expressions (Donegan et al., 2003; Minzenberg et al., 2007). To the best of our knowledge, there are no studies investigating the neuronal bases of ToM in BPD, until now. However, there are some studies giving evidence for alterations in BPD in the MNS. Koenigsberg et al. (2009a) found increased STS-response to negative pictures in BPD, Dziobek et al.(2011) reported decreased STS-activation in BPD associated with cognitive empathy, and Juengling et al.(2003) investigating metabolism during resting-state demonstrated decreased inferior prefrontal glucose consumption.
Taken together, while the results about social cognition in BPD on the behavioral level are rather inconclusive, functional imaging studies point more homogeneously to a hyperactivation of the amygdala in response to social stimuli. Thereby alterations are reported on different stages of social cognition. However, in none of the studies, different stages of social cognition were investigated together in one paradigm and, in none of these studies, ToM was assessed. As a first attempt to study neural correlates of ToM in BPD, we applied a paradigm, including affective ToM-, emotion recognition-, and basal face processing-tasks (Mier et al., 2010a, b). This enabled us to investigate whether possible alterations in affective ToM are specific to the intention recognition process or rather based on a global deficit in the processing of social stimuli. Based on the literature, we did not assume finding performance deficits in BPD, but alterations in the neuronal activation associated with the tested social-cognitive tasks. We hypothesized that patients with BPD show hyperactivation in the amygdala already at the lowest stage of processing i.e. the processing of neutral faces without the necessity to attribute an emotional state. In addition, it was hypothesized that the more complex social cognition processes, i.e. emotion recognition and affective ToM, are associated with additional aberrations in cortical structures. Especially, we were interested in alterations regarding structures linked to the simulation of intentions, namely areas of the MNS, such as the STS and BA 44 (Rizzolatti and Craighero, 2004; Iacoboni et al., 2005; Mier et al., 2010a).
