This is the first study to examine the neural correlates of three cardinal symptoms of acute grief (grief occurring within 3 months of a loss). We found that unique patterns of brain activity indexed attention toward reminders of the deceased, grief styles involving distinct cognitive strategies for coping with thoughts of the deceased, and sadness and yearning induced by memories of the deceased.
In the incentive salience model of grief (7
), excessive attention toward an unavailable attachment figure is hypothesized to maintain grief's core symptoms. Consistent with this hypothesis, we found that bereaved subjects pay more attention to deceased-related than control words and do so in proportion to ratings of intrusive thoughts. This finding extends to bereavement results from the attachment literature in which nonbereaved subjects demonstrate attentional bias toward subliminal threats of interpersonal loss (47
) and follows standard interpretations of the ES task (13
). Of note, because intrinsically emotional words were excluded (e.g., “dog” was permitted but “friend” was not), we interpret attentional bias as reflecting the mourner's current concerns about the deceased (12
) and salience valuations of the concept of the deceased (12
), rather than their evaluation of intrinsic word meaning.
Variation in attentional bias was used to identify brain regions involved in deceased-related processing, including amygdala, insula, and temporoparietal regions (). As hypothesized, these are salience encoding and prefrontal regulatory regions. Amygdala activity is consistent with a role in detecting separation from caregivers and symptoms of separation distress (20
). The insula has direct connections to the amygdala (52
), and in other disorders of salience processing, it correlates with attentional bias toward reminders of the unattainable reward (53
). The temporal and parietal regions activated here contribute to representations of self and others (54
) but a more conservative interpretation emphasizes their role in detecting word salience (57
). This finding may help to explain the clinical experience of grief, in which reminders of the deceased are experienced as particularly meaningful (62
Next, we examined whether variation in two cognitive symptoms of grief, intrusiveness and avoidance, correlated with differential activity in amygdala and prefrontal regulatory regions. These two grief styles are clinically distinct, with avoidant patients rarely presenting for therapy, while those with intrusive experiences often requiring treatment and often going on to develop complicated grief (4
). We expected that the more emotionally distressing style, intrusiveness, would correlate with amygdalar hyperactivity and control region hypoactivity.
Amygdalar results were consistent with the hypothesis. In a single ROI, we found a double dissociation between dorsal and ventral subregions and grief style (). Avoidance correlated with dorsal amygdala dampening while intrusiveness correlated with ventral amygdala activation. Results are consistent with a model in which the amygdala is sensitive to reminders of loss, while intrusiveness and avoidance respectively represent “top down” and “bottom up” processes that modulate this amygdala reactivity. This is consistent with previous work in which ventral amygdala activity correlates with exposure to unconscious (bottom up) stimuli and dorsal amygdala activations correlate to conscious (top down) stimuli (24
Regulatory region and grief style demonstrated a double dissociation (), inverse to the hypothesized pattern. The finding that rACC activation covaries with amygdala activity is consistent with a role for this region in monitoring and contextualizing salience detection activity in amygdala (14
). Future research should seek to explain the finding of DLPFC deactivation covarying with avoidance by examining whether stimulus dampening at an earlier stage of processing, downregulation of salience earlier in bereavement, or decreased baseline attachment cause dampened DLPFC activity.
The third major grief symptom examined was emotional responses to memories of the deceased. Although epidemiological data indicate yearning is the primary emotional symptom in grief, clinical data emphasize sadness as the most common peak emotion (63
). Consistent with this, sadness was the strongest emotion elicited by memories of the deceased, followed by yearning/missing.
Consistent with the hypothesis that amygdala is implicated in sad emotion related to attachment loss (14
), we found that bilateral amygdalar activity, but not rACC or DLPFC activity, predicted peak levels of subsequent sadness ().
We found support for a model in which the rACC and other medial prefrontal structures monitor (29
) and contextualize (2
) information processing in the amygdala, a process that may affect the expression of grief related emotion. depicts a trend from high functional connectivity toward zero FC between rACC and amaygala, as sadness intensity increased. Low connectivity scores between rACC and amygdala may indicate low levels of contextualization, thereby releasing amygdala reactivity, while higher levels of contextualization may indicate improved emotion regulation capacity during mood induction. This hypothesis must be tested in designs in which rACC-amygdala functional connectivity during low-load exposure is correlated with functional connectivity between control regions and the amygdala during explicit efforts to reduce sadness during mood provocation.
We also found evidence supporting a role for the DLPFC in maintaining attentional set on tasks unrelated to grief in the presence of grief-related distractors, a problem seen during clinical grief. DLPFC-amygdala functional connectivity negatively covaried with attentional bias towards deceased words (26
). This is consistent with recent functional connectivity evidence from an fMRI time-series analysis that shows that DLPFC activity is coupled with amygdala activity during cognitive tasks in normal, relative to depressed, subjects (64
The study had several limitations. Its aim was to understand variation in grief responses and therefore employed a between-subjects and not a between-group design, as in several previous studies of grief (10
). The small number of male subjects makes gender comparisons unreliable. Future studies with larger sample sizes may permit exploration of the important question of male and female subject differences. The finding that differences in rACC-amygdala FC predicted subsequent grief-related emotion is not itself evidence of regulatory deficiencies during the emotion but can be used to guide future hypotheses.