Prefrontal cortex (PFC) has been implicated in affect generation and regulation (e.g. Ochsner and Gross, 2005
). However, empirical support for this claim is heterogeneous at both conceptual and methodological levels. Affective experience encompasses a complex set of processes that vary both in time course (transient vs
dispositional) and in content (e.g. fear, happiness). Furthermore, individual affective episodes include subjective sensations, objective behaviors and autonomic responses (Russell, 2003
). Studies of the neural basis of affect have variously operationalized affect as a mood-like trait (e.g. Zald et al.
), as a relatively transient emotional state (e.g. Schaefer et al.
), or as a disorder (e.g. Mayberg et al.
), and each of these constructs has been measured in a variety of ways. Perhaps unsurprisingly, the result is a patchwork of findings that resists easy interpretation.
Notwithstanding this conceptual and experimental heterogeneity, many studies have suggested that PFC is somehow involved in affective experience. Some of the most compelling data in this area come from clinical observations of the effects of PFC damage, which typically have captured affective experience at a fairly general level, whether in early descriptions of emotional changes after PFC damage (as in the case of Phineas Gage; Damasio, 1994
) or of the effects of frontal lobotomy on mood and mood disorders (Valenstein, 1986
), or in more recent questionnaire-based observational studies of patients with PFC damage (e.g. Barrash et al.
). While such work supports a role for PFC in emotion, the specific emotional processes and their relation to specific subregions within PFC remain ill-defined.
More recently, functional imaging has been applied to explore the neural basis of many facets of affective experience. Such experiments in the burgeoning field of affective neuroscience have led to increasingly detailed, component-level models of how emotion is generated and regulated in the healthy brain, and in mood disorders. This work suggests that particular regions within PFC, including ventromedial [VMF, encompassing orbitofrontal and adjacent ventromedial prefrontal cortex (vmPFC)] and dorsal and ventral lateral frontal (LF) cortex, may be playing distinct roles (for reviews see Barrett et al.
; Kober et al.
; Lee and Siegle, in press).
VMF areas have been implicated in the experience of transient affect (Damasio et al.
) and in longer-term affective states (Zald et al.
). VMF also has been implicated in depression (e.g. Davidson et al.
), with ‘over-activity’ within subgenual anterior cingulate (a subregion of VMF) proposed to be a critical pathophysiological mechanism (e.g. Mayberg et al.
). LF regions also have been implicated in the experience of transient affect (e.g. Goldin et al.
), as well as in dispositional affect, particularly during depressed states (e.g. Mayberg et al.
). However, these findings are not simple to interpret in a component process account of affective experience, given that low mood is not an essential criterion for depression.
It has been proposed that LF activations—particularly those seen in transient emotional perturbations—may reflect the regulation of emotional experience. Transient emotional states represent a balance between emotional perturbation and regulation, with top–down regulation of emotion plausibly present even during the onset of an emotional state. Several researchers have reported an inverse association between LF activity and in brain regions thought to be important in negative affect (e.g. Ochsner et al.
), suggesting that LF regions act to dampen transient emotional changes mediated by limbic and subcortical structures. However, similar patterns have also been reported for VMF regions (e.g. Hariri et al.
Although this functional imaging work provides a more detailed view of the role of PFC in emotional experience, models that derive from neuroimaging data require converging support from other methods. Given the complex processes that comprise emotions (e.g. facial expression, subjective experience; see Russell, 2003
), it is difficult to know which of these components is reflected in the various activations observed in neuroimaging studies. Furthermore, as discussed above, observed activations may represent reactivity, regulation, or both.
Studies of patients with focal brain injury can help to answer two questions: (i) does a particular brain region play a necessary role in a given process and (ii) are putative component processes of affective experience in fact dissociable? There are remarkably few loss-of-function studies that address the roles of PFC in emotional experience at the component process level. Transient emotion, in particular, has been little studied. Rule et al.
) and Roberts et al.
) found a diminished ability among individuals with damage to orbitofrontal cortex (OFC; a region within VMF) to ‘filter’ responses to aversive stimuli such as shock and loud noises. OFC damage also has been reported to impair more complex transient emotional experiences, such as regret (Camille et al.
), pride and embarrassment (Beer et al.
). Even these few studies are difficult to reconcile, in that they report enhancement of one transient emotional response and blunting of others.
Questionnaire-based studies of patients with focal VMF injury have identified general changes in emotion (e.g. ‘blunted emotional experience’) by informant report (Barrash et al.
) and self-reported changes in emotional experience for certain cardinal emotions (Hornak et al.
). The latter study reported that damage to medial frontal and OFC areas was associated with changes in emotional experience, but the specific pattern of change (affected emotions, direction of change) varied widely across individuals. Finally, despite the plausibility of LF involvement in affective experience based on neuroimaging studies, there have been few lesion studies examining LF contributions to affective processes.
In sum, the existing loss-of-function literature provides insufficient evidence to conclude that the PFC plays a necessary role in either transient emotional experience and regulation or longer-term mood, much less to specify what this role might be. Here we report a study of the effects of PFC damage affecting either VMF or LF lobes on three aspects of affective experience: short-term induced emotion, spontaneous recovery from emotional states and long-term ‘dispositional’ affect. This exploratory work aimed to begin to disentangle the component processes of affective experience supported by these two regions of PFC. We focused on sad and happy emotional states because of the relevance of these emotions to understanding the neural substrates of depression.