Impulsive traits and unplanned suicide attempts predict exaggerated prefrontal response to angry faces in the elderly

Abstract

Objective: Abnormal responses to social stimuli are seen in people vulnerable to suicidal behavior, indicating possible disruptions in the neural circuitry mediating the interpretation of socioemotional cues. These disruptions have not been empirically related to psychological and cognitive pathways to suicide. In the present study of older suicide attempters, we examined neural responses to emotional faces and their relationship to impulsivity, one of the components of the suicidal diathesis.

Methods: Using functional magnetic resonance imaging, we recorded neurohemodynamic responses to angry faces in a carefully characterized sample of 18 depressed elderly with history of suicide attempts, 13 depressed nonsuicidal patients, and 18 healthy individuals, all aged 60+. Impulsivity was assessed with the Social Problem Solving Inventory Impulsivity/Carelessness Style subscale and Barratt Impulsiveness Scale. The Suicide Intent Scale planning subscale was used to describe the degree of planning associated with the most lethal attempt.

Results: Depression and history of attempted suicide were not associated with neural responses to angry faces, failing to replicate earlier studies. Higher impulsivity, however, predicted exaggerated responses to angry faces in fronto-opercular and dorsomedial prefrontal cortex (pcorr <0.05). Poorly planned suicide attempts also predicted increased fronto-opercular responses. Results were robust to effects of medication exposure, comorbid anxiety and addiction, severity of depression, burden of physical illness, and possible brain injury from suicide attempts.

Conclusion: Impulsive traits and history of unplanned suicide attempts partly explain the heterogeneity in neural responses to angry faces in depressed elderly. Displays of social emotion command excessive cortical processing in impulsive suicide attempters.

Keywords: Aging; impulsivity; neuroimaging; prefrontal cortex; social threat; suicide.

Figure 1

Faces and shapes task.

Figure 2

Task contrast (faces > shapes) positively modulated the blood oxygenation level-dependent signal in the prefrontal cortex ([1–3] right and left inferior frontal gyri; Brodmann areas [BAs] 44 and 45), occipital cortex ([5] BAs 17 and 18) and limbic regions ([6] right amygdala), shown in warm colors. The 20-voxel cluster in the right amygdala (p_svc = .001) and the 15-voxel cluster in the left amygdala (p_svc = .002, not shown) did not pass the whole-brain cluster threshold. Signal was negatively modulated in somatosensory areas, shown in cold colors ([4] - postcentral cortex; BA 2). Activity detected at P_corr < .05, voxelwise threshold P_.001 is shown in contrasting color over the activity detected at voxelwise P_.005.

Figure 3

Brain activation map shows areas with greater BOLD response for high impulsivity compared with low in medial prefrontal cortex ([1] left superior medial gyrus) and the frontal operculum ([2] left middle/inferior frontal gyrus [BA 45]) for SPSI-ICS subscale, shown on Panel A, and the frontal operculum ([3] left precentral gyrus [BA 44]) for BIS, shown on Panel B.

Figure 4

SIS-planning and activity in frontal operculum independently defined by task contrast (A: right BA 44; B: right BA 45; and C: left BA 44/45).