The proposal Pessoa puts forward in The Cognitive-Emotional Brain (2013) sets out to counter the standard paradigm of labeling brain regions as either affective or cognitive, offering instead a framework that does justice to the complex interactions among different neural systems. Notably, Pessoa presents a host of empirical evidence in support of the connection between the amygdala – traditionally associated with fear-detection or processing of negative information – and the prefrontal cortex (PFC), which is thought to play a central role in cognition. In particular, amygdala and PFC seem to cooperate in a number of tasks connected to information gathering and salience detection, such as discriminating between threatening and neutral facial expressions (see also Lim et al. Reference Lim, Padmala and Pessoa2009). Here, I argue that the cognitive-emotional framework Pessoa proposes can be successfully applied to psychopathology and, in particular, to the reasoning of delusional subjects (DS). First, I briefly show that delusions can be characterized in terms of executive dysfunctions that affect the ability to detect relevance in a context. Second, I utilize Pessoa's notion of executive competition (Ch. 7) to offer an original explanation of the executive deficits observed in DS.
In her recent book, Bortolotti (Reference Bortolotti2009) convincingly argued that the pathological character of delusions cannot derive solely from their being irrational. Indeed, several everyday beliefs – for example, superstitious or religious – can be regarded as completely irrational without thereby qualifying as delusional (see Bortolotti Reference Bortolotti2009, p. 259). If characterizing delusions as irrational beliefs is clearly insufficient, then Bortolotti's conclusion calls for a more detailed explanation of why DS are worthy of clinical attention. One possible solution would be to qualify delusions in terms of executive dysfunctions, arising from some disturbance in the ability to detect relevance (or salience) in a context. From a phenomenological perspective, the idea that delusions may involve issues with relevance detection is supported by an analysis of case reports: indeed, DS often describe a peculiar keenness, as well as the feeling of “seeing” hidden connections between things. In particular, the prepsychotic stage corresponds to a phase of “heightened awareness and emotionality” in which specific perceptions or ideas acquire “exaggerated importance” (Kapur Reference Kapur2003, p. 15). For example, in a first-person account of his illness, Aaron Reina (Reference Reina2009) reports that he gradually became convinced that one could determine “a person's feelings, thoughts, and even their personality by the color combinations of their clothing” (p. 3).
From a cognitive perspective, the capacity to detect relevance in a context is often connected to executive functions such as shifting (i.e., switching between tasks or different aspects of the same task), updating (i.e., incorporating relevant information while removing irrelevant ones) and inhibition – for example filtering out inappropriate responses (see Miyake et al. Reference Miyake, Friedman, Emerson, Witzki, Howerter and Wager2000 for a thorough discussion). Notably, delusional patients seem to face serious challenges in every aspect of the executive domain. With respect to shifting, DS are often resistant to belief revision and find it particularly difficult to switch between different mental scenarios or interpretations, thereby displaying a peculiar fixity in their reasoning. For example, subjects affected by the Capgras syndrome would insist in claiming that their spouse has been replaced by an impostor, refusing to take other options into account (e.g., maybe my spouse looks different because she is tired). The ability to update instead requires some sort of “temporal tagging” in order to pry apart newer, more relevant information from old and no longer relevant data (Miyake et al. Reference Miyake, Friedman, Emerson, Witzki, Howerter and Wager2000, p. 57). Interestingly, one of the most common disruptions in delusional narratives concerns exactly temporal ordering: patients often experience “difficulties in indexing events in time,” and their stories are typically characterized by “a derailing of thought, constant tangents … or the compression of a temporally extended story in a single gesture” (Gallagher Reference Gallagher2007, p. 218). With respect to inhibition, some recent studies found that delusional patients fare significantly worse than controls in the Stroop Test, frequently employed to measure a subject's degree of impulsivity (see Ibanez Casas et al. Reference Ibanez Casas, De Portugal, Gonzalez, McKenney, Haro, Usall, Perez-Garcia and Cervilla2013; Rocca et al. Reference Rocca, Castagna, Marchiaro, Rasetti, Rivoira and Bogetto2006). Indeed, the test requires the ability to suppress an automatic response – that is, to read the word regardless of the color – in order to focus on a stimulus that is more relevant for the task at hand – that is, to read the color regardless of the word.
Although the correlation between executive functioning and delusions is at times considered controversial in neuropsychiatric research (see Guillem et al. Reference Guillem, Rinaldi, Pampoulova and Stip2008), more-specific studies have been recently conducted in this direction. For example, Ibanez Casas and colleagues have attempted to explore the degree of executive functioning impairment in patients affected by schizophrenia and delusional disorder. When flexibility, impulsivity, and updating were measured through standardized tests – for example, Stroop Test or Tower of London – DS tended to fare worse than controls (2013, p. 4). In a different study focused on attention and executive functioning, subjects affected by delusional disorder obtained lower scores also with respect to other psychiatric patients such as paranoid schizophrenics (see Grover et al. Reference Grover, Nehra, Bhateja, Kulhara and Kumar2011). However – interestingly enough – DS have also been found to score better than controls in some selected areas: for example, they committed fewer errors in the Wisconsin Card Sorting Test (WCST), thereby suggesting some kind of “hyper-vigilance to selectively abstracted stimuli” (Ibanez Casas et al. Reference Ibanez Casas, De Portugal, Gonzalez, McKenney, Haro, Usall, Perez-Garcia and Cervilla2013, p. 7).
The cognitive-emotional framework proposed by Pessoa offers a significant contribution to the characterization of delusions outlined above. On one hand, it describes relevance detection as an affectively laden process, in which emotions work as cues directing our attention to some elements of the context while disregarding others: in this sense, “vision is never pure, but only affective” (p. 257). On the other hand, it introduces the notion of executive competition, according to which the functions of shifting, inhibition, and updating often interact in a limited resources scenario, so that “resources devoted to one operation will not be available for other operations” (p. 161). Notably, Pessoa maintains that executive functions and emotional processing share a common pool of resources: this means that emotional content may influence executive control in various ways (although the reverse is also possible – see pp. 121 and 251). In particular, when an emotional stimulus is strong enough, task performance will often be impaired because additional resources are diverted from the executive functions in order to process the affective content (see also Mather & Sutherland Reference Mather and Sutherland2011; Pessoa et al. Reference Pessoa, Padmala, Kenzer and Bauer2012).
Applying this framework to delusional patients represents an interesting challenge. Indeed, the executive dysfunctions observed in DS may indicate that their attention is disproportionally directed toward specific – and emotionally significant – elements of the context. For example, persecutory delusions might originate from a strong feeling of anxiety that prompts patients to attend more closely to threatening stimuli in the environment. In these cases, a highly threatening emotional content causes resources to be diverted from the main task, and performance declines as a result (see Pessoa Reference Pessoa2009, p. 161). Several studies on highly anxious – although nonclinical – populations already support this point (see Fox et al. Reference Fox, Russo and Dutton2002; Norberg et al. Reference Norberg, Peira and Wiens2010). Thus, Pessoa's proposal sheds an interesting light on the pathological reasoning observed in DS, which can then be explained in terms of resources that are “taken up” in order to process complex – and often threatening – emotional items. For example, a patient affected by Capgras would direct attention to the stimuli related to his “feeling of estrangement” towards the spouse, thereby finding it hard to revise the belief that she or he has been replaced by an impostor in favor of a more “mundane” interpretation.
Connecting delusions, emotional processing, and executive functions requires a greater level of precision in determining what goes wrong in this aberrant process of relevance detection, however. What exactly makes the patient's reasoning abnormal or pathological? Here, the notion of negative distractor introduced by Pessoa may come in handy. Indeed, he argues that emotional contents can modulate attention in a way that either enhances or impairs task performance, depending on the level of strength – or arousal – of the stimulus. Roughly put, when the affective significance of a stimulus is low, performance would generally increase because the resources can be efficiently “mobilized in the service of handling the task at hand” (p. 167). On the contrary, items with sufficiently high affective significance – regardless of their relevance to the task – tend to compromise performance. In this sense, the emotionally laden items work as negative distractors that drain common pool resources from the main task (see p. 172). If this interpretation is correct, the executive competition model proposed by Pessoa would provide an interesting explanation for the specific deficits observed in DS (see Grover et al. Reference Grover, Nehra, Bhateja, Kulhara and Kumar2011; Ibanez Casas et al. Reference Ibanez Casas, De Portugal, Gonzalez, McKenney, Haro, Usall, Perez-Garcia and Cervilla2013). Indeed, the delusional content itself may work as a powerful distractor absorbing the patient's attention and directing resources away from the functions that are needed to complete the task at hand. To make this point more explicit: delusional patients may continually perceive threatening – or otherwise negative – stimuli in the environment, which force them to invest a disproportionate amount of resources that become unavailable to other cognitive functions. From a neurological viewpoint, this process need not translate to decreased activation of the relevant brain areas (e.g., amygdala, PFC), but rather reflects the fact that some common pool resources are “taken up” in dealing with delusional beliefs. This is consistent with Pessoa's findings, according to which negative distractors can at times produce increased activation of the relevant networks (see pp. 128–29). Therefore, the DS's poor outcome in executive tests may be caused by an overworking executive system, where highly significant items continuously drain resources from the current task. In this sense, the proverbial fixity associated to delusions would result from the subject's incapacity to process – or even “see” – other elements of the context as emotionally and functionally relevant.
The application of Pessoa's proposal to psychopathology also allows us to resolve an apparent inconsistency arising from one of the studies discussed above (Ibanez Casas et al. Reference Ibanez Casas, De Portugal, Gonzalez, McKenney, Haro, Usall, Perez-Garcia and Cervilla2013). Indeed, the fact that DS fared better than controls in some selected areas (e.g., WCST) indicates that their executive abilities should not be understood as impaired, but rather as dysfunctional. In other words, DS disproportionally direct their resources toward specific stimuli in the environment because they perceive them as pervasive, affectively significant, and in need of additional processing. Thus, DS can be regarded as being in a permanent – or at least frequent – condition of overload, that phenomenologically reflects the feeling of “hypersalience” observed in several patients (see Kapur Reference Kapur2003; Speechley et al. Reference Speechley, Whitman and Woodward2010). As Pessoa would put it, DS continuously face demands that exceed their available capacity of processing, causing performance to suffer when the task specifically requires attention (see pp. 89 and 98).
To sum up, the account of delusions outlined here has two main advantages. First, it offers an explanation of their pathological character that goes beyond the mere ascription of irrationality (see Bortolotti Reference Bortolotti2009). Second, it strengthens the connection between delusions and executive dysfunctions, which is still considered controversial in the neuropsychiatric literature (see Guillem et al. Reference Guillem, Rinaldi, Pampoulova and Stip2008). Notably, the executive competition model proposed by Pessoa offers an important contribution to the idea that delusions may involve both emotional and executive dysfunctions. On one hand, particularly strong emotions shape the patient's attention and direct it towards specific elements of the context (Ch. 2). Here, the guiding emotion may vary depending on the delusional content, although we can safely assume that fear would play a key role (e.g., threatening stimuli in persecutory delusions). On the other hand, affectively laden items work as negative distractors that monopolize executive functions that then become unavailable for other tasks (Ch. 7). In order to test this hypothesis empirically, I propose to extend Pessoa's studies on the relationship between emotions, attention, and executive control to delusional populations (see Pessoa Reference Pessoa2005; Reference Pessoa2008; Reference Pessoa2009). In particular, it would be interesting to see whether the regions connected to cognitive-emotional interactions (e.g., amygdala, PFC) experience an increase or decrease in activation while DS are dealing with emotionally laden interferences in executive tasks.
The proposal Pessoa puts forward in The Cognitive-Emotional Brain (2013) sets out to counter the standard paradigm of labeling brain regions as either affective or cognitive, offering instead a framework that does justice to the complex interactions among different neural systems. Notably, Pessoa presents a host of empirical evidence in support of the connection between the amygdala – traditionally associated with fear-detection or processing of negative information – and the prefrontal cortex (PFC), which is thought to play a central role in cognition. In particular, amygdala and PFC seem to cooperate in a number of tasks connected to information gathering and salience detection, such as discriminating between threatening and neutral facial expressions (see also Lim et al. Reference Lim, Padmala and Pessoa2009). Here, I argue that the cognitive-emotional framework Pessoa proposes can be successfully applied to psychopathology and, in particular, to the reasoning of delusional subjects (DS). First, I briefly show that delusions can be characterized in terms of executive dysfunctions that affect the ability to detect relevance in a context. Second, I utilize Pessoa's notion of executive competition (Ch. 7) to offer an original explanation of the executive deficits observed in DS.
In her recent book, Bortolotti (Reference Bortolotti2009) convincingly argued that the pathological character of delusions cannot derive solely from their being irrational. Indeed, several everyday beliefs – for example, superstitious or religious – can be regarded as completely irrational without thereby qualifying as delusional (see Bortolotti Reference Bortolotti2009, p. 259). If characterizing delusions as irrational beliefs is clearly insufficient, then Bortolotti's conclusion calls for a more detailed explanation of why DS are worthy of clinical attention. One possible solution would be to qualify delusions in terms of executive dysfunctions, arising from some disturbance in the ability to detect relevance (or salience) in a context. From a phenomenological perspective, the idea that delusions may involve issues with relevance detection is supported by an analysis of case reports: indeed, DS often describe a peculiar keenness, as well as the feeling of “seeing” hidden connections between things. In particular, the prepsychotic stage corresponds to a phase of “heightened awareness and emotionality” in which specific perceptions or ideas acquire “exaggerated importance” (Kapur Reference Kapur2003, p. 15). For example, in a first-person account of his illness, Aaron Reina (Reference Reina2009) reports that he gradually became convinced that one could determine “a person's feelings, thoughts, and even their personality by the color combinations of their clothing” (p. 3).
From a cognitive perspective, the capacity to detect relevance in a context is often connected to executive functions such as shifting (i.e., switching between tasks or different aspects of the same task), updating (i.e., incorporating relevant information while removing irrelevant ones) and inhibition – for example filtering out inappropriate responses (see Miyake et al. Reference Miyake, Friedman, Emerson, Witzki, Howerter and Wager2000 for a thorough discussion). Notably, delusional patients seem to face serious challenges in every aspect of the executive domain. With respect to shifting, DS are often resistant to belief revision and find it particularly difficult to switch between different mental scenarios or interpretations, thereby displaying a peculiar fixity in their reasoning. For example, subjects affected by the Capgras syndrome would insist in claiming that their spouse has been replaced by an impostor, refusing to take other options into account (e.g., maybe my spouse looks different because she is tired). The ability to update instead requires some sort of “temporal tagging” in order to pry apart newer, more relevant information from old and no longer relevant data (Miyake et al. Reference Miyake, Friedman, Emerson, Witzki, Howerter and Wager2000, p. 57). Interestingly, one of the most common disruptions in delusional narratives concerns exactly temporal ordering: patients often experience “difficulties in indexing events in time,” and their stories are typically characterized by “a derailing of thought, constant tangents … or the compression of a temporally extended story in a single gesture” (Gallagher Reference Gallagher2007, p. 218). With respect to inhibition, some recent studies found that delusional patients fare significantly worse than controls in the Stroop Test, frequently employed to measure a subject's degree of impulsivity (see Ibanez Casas et al. Reference Ibanez Casas, De Portugal, Gonzalez, McKenney, Haro, Usall, Perez-Garcia and Cervilla2013; Rocca et al. Reference Rocca, Castagna, Marchiaro, Rasetti, Rivoira and Bogetto2006). Indeed, the test requires the ability to suppress an automatic response – that is, to read the word regardless of the color – in order to focus on a stimulus that is more relevant for the task at hand – that is, to read the color regardless of the word.
Although the correlation between executive functioning and delusions is at times considered controversial in neuropsychiatric research (see Guillem et al. Reference Guillem, Rinaldi, Pampoulova and Stip2008), more-specific studies have been recently conducted in this direction. For example, Ibanez Casas and colleagues have attempted to explore the degree of executive functioning impairment in patients affected by schizophrenia and delusional disorder. When flexibility, impulsivity, and updating were measured through standardized tests – for example, Stroop Test or Tower of London – DS tended to fare worse than controls (2013, p. 4). In a different study focused on attention and executive functioning, subjects affected by delusional disorder obtained lower scores also with respect to other psychiatric patients such as paranoid schizophrenics (see Grover et al. Reference Grover, Nehra, Bhateja, Kulhara and Kumar2011). However – interestingly enough – DS have also been found to score better than controls in some selected areas: for example, they committed fewer errors in the Wisconsin Card Sorting Test (WCST), thereby suggesting some kind of “hyper-vigilance to selectively abstracted stimuli” (Ibanez Casas et al. Reference Ibanez Casas, De Portugal, Gonzalez, McKenney, Haro, Usall, Perez-Garcia and Cervilla2013, p. 7).
The cognitive-emotional framework proposed by Pessoa offers a significant contribution to the characterization of delusions outlined above. On one hand, it describes relevance detection as an affectively laden process, in which emotions work as cues directing our attention to some elements of the context while disregarding others: in this sense, “vision is never pure, but only affective” (p. 257). On the other hand, it introduces the notion of executive competition, according to which the functions of shifting, inhibition, and updating often interact in a limited resources scenario, so that “resources devoted to one operation will not be available for other operations” (p. 161). Notably, Pessoa maintains that executive functions and emotional processing share a common pool of resources: this means that emotional content may influence executive control in various ways (although the reverse is also possible – see pp. 121 and 251). In particular, when an emotional stimulus is strong enough, task performance will often be impaired because additional resources are diverted from the executive functions in order to process the affective content (see also Mather & Sutherland Reference Mather and Sutherland2011; Pessoa et al. Reference Pessoa, Padmala, Kenzer and Bauer2012).
Applying this framework to delusional patients represents an interesting challenge. Indeed, the executive dysfunctions observed in DS may indicate that their attention is disproportionally directed toward specific – and emotionally significant – elements of the context. For example, persecutory delusions might originate from a strong feeling of anxiety that prompts patients to attend more closely to threatening stimuli in the environment. In these cases, a highly threatening emotional content causes resources to be diverted from the main task, and performance declines as a result (see Pessoa Reference Pessoa2009, p. 161). Several studies on highly anxious – although nonclinical – populations already support this point (see Fox et al. Reference Fox, Russo and Dutton2002; Norberg et al. Reference Norberg, Peira and Wiens2010). Thus, Pessoa's proposal sheds an interesting light on the pathological reasoning observed in DS, which can then be explained in terms of resources that are “taken up” in order to process complex – and often threatening – emotional items. For example, a patient affected by Capgras would direct attention to the stimuli related to his “feeling of estrangement” towards the spouse, thereby finding it hard to revise the belief that she or he has been replaced by an impostor in favor of a more “mundane” interpretation.
Connecting delusions, emotional processing, and executive functions requires a greater level of precision in determining what goes wrong in this aberrant process of relevance detection, however. What exactly makes the patient's reasoning abnormal or pathological? Here, the notion of negative distractor introduced by Pessoa may come in handy. Indeed, he argues that emotional contents can modulate attention in a way that either enhances or impairs task performance, depending on the level of strength – or arousal – of the stimulus. Roughly put, when the affective significance of a stimulus is low, performance would generally increase because the resources can be efficiently “mobilized in the service of handling the task at hand” (p. 167). On the contrary, items with sufficiently high affective significance – regardless of their relevance to the task – tend to compromise performance. In this sense, the emotionally laden items work as negative distractors that drain common pool resources from the main task (see p. 172). If this interpretation is correct, the executive competition model proposed by Pessoa would provide an interesting explanation for the specific deficits observed in DS (see Grover et al. Reference Grover, Nehra, Bhateja, Kulhara and Kumar2011; Ibanez Casas et al. Reference Ibanez Casas, De Portugal, Gonzalez, McKenney, Haro, Usall, Perez-Garcia and Cervilla2013). Indeed, the delusional content itself may work as a powerful distractor absorbing the patient's attention and directing resources away from the functions that are needed to complete the task at hand. To make this point more explicit: delusional patients may continually perceive threatening – or otherwise negative – stimuli in the environment, which force them to invest a disproportionate amount of resources that become unavailable to other cognitive functions. From a neurological viewpoint, this process need not translate to decreased activation of the relevant brain areas (e.g., amygdala, PFC), but rather reflects the fact that some common pool resources are “taken up” in dealing with delusional beliefs. This is consistent with Pessoa's findings, according to which negative distractors can at times produce increased activation of the relevant networks (see pp. 128–29). Therefore, the DS's poor outcome in executive tests may be caused by an overworking executive system, where highly significant items continuously drain resources from the current task. In this sense, the proverbial fixity associated to delusions would result from the subject's incapacity to process – or even “see” – other elements of the context as emotionally and functionally relevant.
The application of Pessoa's proposal to psychopathology also allows us to resolve an apparent inconsistency arising from one of the studies discussed above (Ibanez Casas et al. Reference Ibanez Casas, De Portugal, Gonzalez, McKenney, Haro, Usall, Perez-Garcia and Cervilla2013). Indeed, the fact that DS fared better than controls in some selected areas (e.g., WCST) indicates that their executive abilities should not be understood as impaired, but rather as dysfunctional. In other words, DS disproportionally direct their resources toward specific stimuli in the environment because they perceive them as pervasive, affectively significant, and in need of additional processing. Thus, DS can be regarded as being in a permanent – or at least frequent – condition of overload, that phenomenologically reflects the feeling of “hypersalience” observed in several patients (see Kapur Reference Kapur2003; Speechley et al. Reference Speechley, Whitman and Woodward2010). As Pessoa would put it, DS continuously face demands that exceed their available capacity of processing, causing performance to suffer when the task specifically requires attention (see pp. 89 and 98).
To sum up, the account of delusions outlined here has two main advantages. First, it offers an explanation of their pathological character that goes beyond the mere ascription of irrationality (see Bortolotti Reference Bortolotti2009). Second, it strengthens the connection between delusions and executive dysfunctions, which is still considered controversial in the neuropsychiatric literature (see Guillem et al. Reference Guillem, Rinaldi, Pampoulova and Stip2008). Notably, the executive competition model proposed by Pessoa offers an important contribution to the idea that delusions may involve both emotional and executive dysfunctions. On one hand, particularly strong emotions shape the patient's attention and direct it towards specific elements of the context (Ch. 2). Here, the guiding emotion may vary depending on the delusional content, although we can safely assume that fear would play a key role (e.g., threatening stimuli in persecutory delusions). On the other hand, affectively laden items work as negative distractors that monopolize executive functions that then become unavailable for other tasks (Ch. 7). In order to test this hypothesis empirically, I propose to extend Pessoa's studies on the relationship between emotions, attention, and executive control to delusional populations (see Pessoa Reference Pessoa2005; Reference Pessoa2008; Reference Pessoa2009). In particular, it would be interesting to see whether the regions connected to cognitive-emotional interactions (e.g., amygdala, PFC) experience an increase or decrease in activation while DS are dealing with emotionally laden interferences in executive tasks.
ACKNOWLEDGMENT
I am grateful to Peter Langland-Hassan for his continuous support and thorough feedback, and to Justin Caouette for his helpful comments on earlier drafts of this commentary. This work was supported in part by a summer fellowship from the TAFT Research Center.