Lindquist et al. offer an outstanding compilation, organization, and presentation of the results of human neuroimaging studies related to emotion. Their study is of great interest as a review and summary of empirical data from this burgeoning area of research. The interpretation of these data, however, is flawed. It criticizes a so-called locationist model that specific brain regions are consistently associated with specific emotion categories, and reports little evidence for such associations. However, no one holds the simplistic view of brain–emotion relationships illustrated in the target article's Figure 1. It is a “straw man.” Views such as those of Panksepp (Reference Panksepp1998) linking specific emotion categories with brain networks are not inconsistent with the pattern of results summarized in this article. Indeed, the pattern illustrated in Figure 3 of the target article supports the classic view of the brain and emotion dating from Papez (Reference Papez1937) and MacLean (Reference MacLean, Lewis and Haviland1993): richly interconnected limbic structures associated with subjective emotional experience, and connected with many other brain areas. Indeed, the differentiation of core limbic, lateral limbic, and medial prefrontal cortex (PFC) subsystems in Figure 3 is not unlike MacLean's differentiation of subcortical-reptilian, selfish-paleomammalian, and prosocial-paleomammalian subsystems.
The quest to find specific brain locations associated with the primary affects – happiness, sadness, fear, anger, and disgust – is off the mark because the primary affects exist at an ecological rather than a bio/physiological level of analysis (Buck Reference Buck1984; Reference Buck2010). They are properly measured at the level of communication – display and pre-attunement – as they traditionally have been in research on facial displays.
The favored alternative “psychological constructionist” view assumes that emotions “emerge out of more basic psychological operations that are not specific to emotion” (target article, sect. 3, para. 1). However, the nature of these mechanisms is unclear. The notion of core affect, that all affect can be reduced to dimensions of valence and arousal, is not helpful.
However, the conclusion that emotions emerge from more basic processes may be on the mark. There are specific neurochemical systems underlying primary motivational-emotional systems or primes (Buck Reference Buck1985; Reference Buck1999). These include neurotransmitter molecules and receptors that vary in number and sensitivity. The activation of many primes is associated with specific, subjectively experienced feelings and desires, as demonstrated by the effects of psychoactive drugs on animals, including humans (Buck Reference Buck1999). Many such transmitter molecules are peptides, direct products of genes in sending neurons. Specific peptides are associated with specific subjectively experienced feelings and desires (Pert Reference Pert1997), and as the origin of the peptides is the genes, subjectively experienced affects function as “voices of the genes.” The genes are always murmuring and whispering, generating a complex background of feelings and desires, but like the feel of our shoes on our feet, we rarely pay attention. Of course, sometimes the genes scream and shout, and our feelings and desires dominate consciousness. The genes do not control us through these feelings and desires, but they do cajole us.
Primes constitute modules, as it were, which, although dissociable in principle, are highly interactive, and combine to contribute to complex subjective experiences such as those associated with primary affects. For example, the subjective experience associated with fear might be composed of a variable neurochemical “cocktail” that might combine diazepam-binding inhibitor (DBI: the “anxiety peptide”), corticotrophin-releasing hormone (CRH: stress), cholecystokinin (CCK: panic), among others (Buck Reference Buck2010). Similarly, love is arguably a primary affect at the ecological level, associated with intimate displays (contact comfort, pheromones). The subjective experiences associated with love may be associated with a neurochemical cocktail including high endorphins (euphoria), gonadotropin-releasing hormone (GnRH: eroticism), dopamine (DA: excitement), oxytocin (OXY: nurturance); vasopressin (AVP: protectiveness), CRH (stress); and low serotonin (5-HT: submission) (see Ortigue et al. Reference Ortigue, Bianchi-Demicheli, Patel, Frum and Lewis2010; Panksepp Reference Panksepp1998). Understanding of these systems, their evolutionary and genetic bases, their complex interrelationships, and their communicative role in social interaction is proceeding apace.
Therefore, the contention that emotion requires a constructionist account may be accurate, but it is a neurochemical, biomolecular construction: arguably, “cocktail” is a better term. Also, this version of the locationist position is squarely on the mark: specifiable neurochemical systems, or primes, are constituent elements of the affective cocktail.
There is a 500-pound gorilla lurking largely unacknowledged in this article, and more generally in the literature on the brain and emotion: that is, cerebral lateralization. Right- and left-sided brain mechanisms are distinguished in the presentation of the empirical results of Lindquist et al., and there are many such differences, including an apparently larger neural reference space associated with emotions in the right than in the left hemisphere in the ventral view in their Figure 4. However, there is little discussion of the meaning of these differences. The discussion of the amygdalae and fear does not note evidence of amygdala lateralization, including sex differences. Whereas the right amygdala has been particularly associated with fear, there are suggestions that the left amygdala may be involved in socio-emotional functioning. There is evidence of left amygdala hypoactivation in Asperger Syndrome (AS: Ashwin et al. Reference Ashwin, Baron-Cohen, Wheelwright, O'Riordan and Bullmore2007) and hyperactivation in Borderline Personality Disorder (BPD: Donegan et al. Reference Donegan, Sanislow, Blumberg, Fulbright, Lacadie, Skudlarski, Gore, Olson, McGlashan and Wexler2003; Koenigsberg et al. Reference Koenigsberg, Sievera, Lee, Pizzarello, Newa, Goodman, Cheng, Flory and Prohovnika2009). Although these conditions have, historically, rarely been compared with one another, the evidence that they are related to the same brain area highlights the fact that in many ways their symptoms are opposite. Major AS symptoms include an obliviousness to other persons: a lack of empathy and socio-emotional reciprocity, and a preference for solitary activities. In contrast, BPD involves a kind of socio-emotional hypervigilance, often including frantic efforts to avoid real or imagined separation, rejection, or abandonment. These findings are in turn consistent with the observed sex differences: males tend to be emotionally oblivious and females emotionally hypervigilant. Hence, “the battle of the sexes.”
This evidence, that the left amygdala is involved in the functioning of what might be termed a “social brain,” is consistent with suggestions that the left hemisphere is associated with prosocial emotions (Buck Reference Buck2002; Ross et al. Reference Ross, Homan and Buck1994). The evidence in the target article, that anger experience is often associated with left-sided processing, is not inconsistent with this, as anger often functions as a prosocial emotion.
Lindquist et al. offer an outstanding compilation, organization, and presentation of the results of human neuroimaging studies related to emotion. Their study is of great interest as a review and summary of empirical data from this burgeoning area of research. The interpretation of these data, however, is flawed. It criticizes a so-called locationist model that specific brain regions are consistently associated with specific emotion categories, and reports little evidence for such associations. However, no one holds the simplistic view of brain–emotion relationships illustrated in the target article's Figure 1. It is a “straw man.” Views such as those of Panksepp (Reference Panksepp1998) linking specific emotion categories with brain networks are not inconsistent with the pattern of results summarized in this article. Indeed, the pattern illustrated in Figure 3 of the target article supports the classic view of the brain and emotion dating from Papez (Reference Papez1937) and MacLean (Reference MacLean, Lewis and Haviland1993): richly interconnected limbic structures associated with subjective emotional experience, and connected with many other brain areas. Indeed, the differentiation of core limbic, lateral limbic, and medial prefrontal cortex (PFC) subsystems in Figure 3 is not unlike MacLean's differentiation of subcortical-reptilian, selfish-paleomammalian, and prosocial-paleomammalian subsystems.
The quest to find specific brain locations associated with the primary affects – happiness, sadness, fear, anger, and disgust – is off the mark because the primary affects exist at an ecological rather than a bio/physiological level of analysis (Buck Reference Buck1984; Reference Buck2010). They are properly measured at the level of communication – display and pre-attunement – as they traditionally have been in research on facial displays.
The favored alternative “psychological constructionist” view assumes that emotions “emerge out of more basic psychological operations that are not specific to emotion” (target article, sect. 3, para. 1). However, the nature of these mechanisms is unclear. The notion of core affect, that all affect can be reduced to dimensions of valence and arousal, is not helpful.
However, the conclusion that emotions emerge from more basic processes may be on the mark. There are specific neurochemical systems underlying primary motivational-emotional systems or primes (Buck Reference Buck1985; Reference Buck1999). These include neurotransmitter molecules and receptors that vary in number and sensitivity. The activation of many primes is associated with specific, subjectively experienced feelings and desires, as demonstrated by the effects of psychoactive drugs on animals, including humans (Buck Reference Buck1999). Many such transmitter molecules are peptides, direct products of genes in sending neurons. Specific peptides are associated with specific subjectively experienced feelings and desires (Pert Reference Pert1997), and as the origin of the peptides is the genes, subjectively experienced affects function as “voices of the genes.” The genes are always murmuring and whispering, generating a complex background of feelings and desires, but like the feel of our shoes on our feet, we rarely pay attention. Of course, sometimes the genes scream and shout, and our feelings and desires dominate consciousness. The genes do not control us through these feelings and desires, but they do cajole us.
Primes constitute modules, as it were, which, although dissociable in principle, are highly interactive, and combine to contribute to complex subjective experiences such as those associated with primary affects. For example, the subjective experience associated with fear might be composed of a variable neurochemical “cocktail” that might combine diazepam-binding inhibitor (DBI: the “anxiety peptide”), corticotrophin-releasing hormone (CRH: stress), cholecystokinin (CCK: panic), among others (Buck Reference Buck2010). Similarly, love is arguably a primary affect at the ecological level, associated with intimate displays (contact comfort, pheromones). The subjective experiences associated with love may be associated with a neurochemical cocktail including high endorphins (euphoria), gonadotropin-releasing hormone (GnRH: eroticism), dopamine (DA: excitement), oxytocin (OXY: nurturance); vasopressin (AVP: protectiveness), CRH (stress); and low serotonin (5-HT: submission) (see Ortigue et al. Reference Ortigue, Bianchi-Demicheli, Patel, Frum and Lewis2010; Panksepp Reference Panksepp1998). Understanding of these systems, their evolutionary and genetic bases, their complex interrelationships, and their communicative role in social interaction is proceeding apace.
Therefore, the contention that emotion requires a constructionist account may be accurate, but it is a neurochemical, biomolecular construction: arguably, “cocktail” is a better term. Also, this version of the locationist position is squarely on the mark: specifiable neurochemical systems, or primes, are constituent elements of the affective cocktail.
There is a 500-pound gorilla lurking largely unacknowledged in this article, and more generally in the literature on the brain and emotion: that is, cerebral lateralization. Right- and left-sided brain mechanisms are distinguished in the presentation of the empirical results of Lindquist et al., and there are many such differences, including an apparently larger neural reference space associated with emotions in the right than in the left hemisphere in the ventral view in their Figure 4. However, there is little discussion of the meaning of these differences. The discussion of the amygdalae and fear does not note evidence of amygdala lateralization, including sex differences. Whereas the right amygdala has been particularly associated with fear, there are suggestions that the left amygdala may be involved in socio-emotional functioning. There is evidence of left amygdala hypoactivation in Asperger Syndrome (AS: Ashwin et al. Reference Ashwin, Baron-Cohen, Wheelwright, O'Riordan and Bullmore2007) and hyperactivation in Borderline Personality Disorder (BPD: Donegan et al. Reference Donegan, Sanislow, Blumberg, Fulbright, Lacadie, Skudlarski, Gore, Olson, McGlashan and Wexler2003; Koenigsberg et al. Reference Koenigsberg, Sievera, Lee, Pizzarello, Newa, Goodman, Cheng, Flory and Prohovnika2009). Although these conditions have, historically, rarely been compared with one another, the evidence that they are related to the same brain area highlights the fact that in many ways their symptoms are opposite. Major AS symptoms include an obliviousness to other persons: a lack of empathy and socio-emotional reciprocity, and a preference for solitary activities. In contrast, BPD involves a kind of socio-emotional hypervigilance, often including frantic efforts to avoid real or imagined separation, rejection, or abandonment. These findings are in turn consistent with the observed sex differences: males tend to be emotionally oblivious and females emotionally hypervigilant. Hence, “the battle of the sexes.”
This evidence, that the left amygdala is involved in the functioning of what might be termed a “social brain,” is consistent with suggestions that the left hemisphere is associated with prosocial emotions (Buck Reference Buck2002; Ross et al. Reference Ross, Homan and Buck1994). The evidence in the target article, that anger experience is often associated with left-sided processing, is not inconsistent with this, as anger often functions as a prosocial emotion.