Neurobiological Underpinnings of Shame and Guilt
Neurobiological Underpinnings of Shame and Guilt
After the fMRI scan, the participants were asked to rate the sentences on a five-point scale (0 = not ashamed/innocent; 5 = very ashamed/guilty) in the category of shame and guilt. We assumed that those items scaled around zero can be considered as neutral. The ratings of the sentences used in our paradigm lead to the following results: The items that had been depicted as shame items received higher values in the category 'shame' (range = 1.90–4.07, mean = 2.87, s.d. = 0.68) than in the category 'guilt' (range = 0.93–3.10, mean = 1.86, s.d. = 0.59; P = 0.001, computed with Wilcoxon Signed Rank Test). The same applies for the guilt items. The guilt sentences received higher values in the category 'guilt' (range = 1.27–4.67, mean = 3.67, s.d. = 0.87) than in the category 'shame' (range = 0.13–4.27, mean = 2.98, s.d. = 1.16; P = 0.002). The neutral sentences received values around zero and differ significantly from the two affective categories (range = 0.00–0.40, mean = 0.04, s.d. = 0.11; for both comparisons neutral vs guilt and neutral–shame; P = 0.000).
First, to calculate the emotion-specific activation, we used the contrasts of 'guilt minus neutral' and 'shame minus neutral' as performed by Takahashi et al. (2004). Second, we added the contrast of 'shame minus guilt' and vice versa. Finally, we report pilot data on gender differences. The neutral condition did not show any significantly increased activation compared with guilt or shame for any of the comparisons.
'Shame Minus Neutral' Condition. First, in the shame condition (relative to the neutral condition), the participants produced an activation in the visual areas [right cuneus (BA 17), right lingual gyrus (BA 18) and left middle occipital gyrus (BA 19)], in the temporal lobe [right fusiform gyrus (BA 19), bilateral parahippocampal gyrus (BA 27, 30), left superior (BA 38) and left middle temporal gyrus (BA 21)] and in a frontal network [left superior (BA 6, 8, 9), bilateral inferior (BA 45, 47), left middle (BA 9) and right medial frontal gyrus (BA 8)] (Figure 2; Table 2).
(Enlarge Image)
Figure 2.
Brain activation in the condition shame minus neutral, red = shame activation: (A) superior temporal gyrus (−42, 17, 14); (B) middle occipital gyrus (x = −27, y = −85, z = 13); (C) superior frontal gyrus (x = −0, y = 63, z = −34); P < 0.0002.
'Guilt Minus Neutral' Condition.Table 2 also shows the results from the comparison of the 'guilt minus neutral' condition. In the guilt condition, outspreading activation was found in the left hemisphere, which approached significance in comparison with the 'shame minus neutral' condition.
The guilt condition is some similarities of brain activation to the shame condition, specifically in the visual cortex [left cuneus (BA 18), bilateral lingual gyrus (BA 17, 18)], in the temporal lobe [bilateral fusiform gyrus (BA 18, 19), left superior (BA 22, 39) and bilateral middle temporal gyrus (BA 21)] and in the frontal area [right superior (BA 8) and left middle frontal gyrus (BA 13, 46)], which were not seen in the neutral condition.
Unlike the shame condition, there was additional activation in the left insula (BA 13), the left orbitofrontal gyrus (BA 11) and the left precentral gyrus (BA 6, 44) (Figure 3).
(Enlarge Image)
Figure 3.
Brain activation in the condition guilt minus neutral, red = guilt activation: (A) insula (x = −54, y = 17, z = 22); (B) superior frontal gyrus (x = 18, y = 47, z = 43); (C) middle temporal gyrus (x = −60, y = −34, z = 1); P < 0.0002.
Table 2 contains the results of the activations in the conditions 'shame minus neutral' and 'guilt minus neutral' with the associated Brodmann areas, hemispheres, coordinates, z-score and the number of voxel.
'Shame Minus Guilt' Condition (And Vice Versa). The shame vs guilt condition were both compared (shame > guilt and vice versa). Because of the subtraction method used for the contrast, only the areas that occur in one of the two conditions are presented (red = shame, blue = guilt). Thus, regions that are activated in both conditions are not indicated.
There was activation of different regions within the temporal lobe in both conditions [shame: cingulate gyrus (BA 32), bilateral parahippocampal gyrus (BA 27, 20, 34, 36); guilt: right fusiform gyrus (BA 37) and left middle temporal gyrus (BA 21)]. Additional frontal activation was found in the shame condition [anterior cingulate cortex (BA 24), right rectal gyrus (BA 11), right medial (BA 10) and right inferior frontal gyrus (BA 47)]. In the guilt condition, an activation of the right amygdala and the insula (BA 13) could be detected, which was not found in the shame condition (Table 3).
Within the female sample there was an activation in the shame and guilt condition (shame > guilt) in the bilateral middle temporal gyrus (BA 19, 21, 39). In addition, the shame condition also activates the parietal lobe [right precuneus (BA 7, 31), right supramarginal gyrus (BA 40)], the temporal lobe [cingulate gyrus (BA 31), parahippocampal gyrus (BA 27)] and the frontal lobe [right precentral gyrus (BA 6), bilateral middle frontal gyrus (BA 10)] (Supplementary Table S2).
The male participants showed activations in shame and guilt (shame > guilt) in the right fusiform gyrus (BA 37). In contrast to the guilt condition, men showed more activation in the left parahippocampal gyrus (BA 35, 36) during the shame condition. The bilateral anterior cingulate cortex (BA 32) and the right orbital frontal gyrus (BA 47) also showed relatively increased activation. The guilt condition was associated with activation in the uncus (BA 34), the right amygdala. Additionally, there was also activation seen in the left inferior occipital and lingual gyrus (BA 18), and bilateral middle frontal gyrus (BA 10) (Supplementary Table S3).
Results
Subjective Ratings of Experimental Stimuli
After the fMRI scan, the participants were asked to rate the sentences on a five-point scale (0 = not ashamed/innocent; 5 = very ashamed/guilty) in the category of shame and guilt. We assumed that those items scaled around zero can be considered as neutral. The ratings of the sentences used in our paradigm lead to the following results: The items that had been depicted as shame items received higher values in the category 'shame' (range = 1.90–4.07, mean = 2.87, s.d. = 0.68) than in the category 'guilt' (range = 0.93–3.10, mean = 1.86, s.d. = 0.59; P = 0.001, computed with Wilcoxon Signed Rank Test). The same applies for the guilt items. The guilt sentences received higher values in the category 'guilt' (range = 1.27–4.67, mean = 3.67, s.d. = 0.87) than in the category 'shame' (range = 0.13–4.27, mean = 2.98, s.d. = 1.16; P = 0.002). The neutral sentences received values around zero and differ significantly from the two affective categories (range = 0.00–0.40, mean = 0.04, s.d. = 0.11; for both comparisons neutral vs guilt and neutral–shame; P = 0.000).
fMRI Results
First, to calculate the emotion-specific activation, we used the contrasts of 'guilt minus neutral' and 'shame minus neutral' as performed by Takahashi et al. (2004). Second, we added the contrast of 'shame minus guilt' and vice versa. Finally, we report pilot data on gender differences. The neutral condition did not show any significantly increased activation compared with guilt or shame for any of the comparisons.
'Shame Minus Neutral' Condition. First, in the shame condition (relative to the neutral condition), the participants produced an activation in the visual areas [right cuneus (BA 17), right lingual gyrus (BA 18) and left middle occipital gyrus (BA 19)], in the temporal lobe [right fusiform gyrus (BA 19), bilateral parahippocampal gyrus (BA 27, 30), left superior (BA 38) and left middle temporal gyrus (BA 21)] and in a frontal network [left superior (BA 6, 8, 9), bilateral inferior (BA 45, 47), left middle (BA 9) and right medial frontal gyrus (BA 8)] (Figure 2; Table 2).
(Enlarge Image)
Figure 2.
Brain activation in the condition shame minus neutral, red = shame activation: (A) superior temporal gyrus (−42, 17, 14); (B) middle occipital gyrus (x = −27, y = −85, z = 13); (C) superior frontal gyrus (x = −0, y = 63, z = −34); P < 0.0002.
'Guilt Minus Neutral' Condition.Table 2 also shows the results from the comparison of the 'guilt minus neutral' condition. In the guilt condition, outspreading activation was found in the left hemisphere, which approached significance in comparison with the 'shame minus neutral' condition.
The guilt condition is some similarities of brain activation to the shame condition, specifically in the visual cortex [left cuneus (BA 18), bilateral lingual gyrus (BA 17, 18)], in the temporal lobe [bilateral fusiform gyrus (BA 18, 19), left superior (BA 22, 39) and bilateral middle temporal gyrus (BA 21)] and in the frontal area [right superior (BA 8) and left middle frontal gyrus (BA 13, 46)], which were not seen in the neutral condition.
Unlike the shame condition, there was additional activation in the left insula (BA 13), the left orbitofrontal gyrus (BA 11) and the left precentral gyrus (BA 6, 44) (Figure 3).
(Enlarge Image)
Figure 3.
Brain activation in the condition guilt minus neutral, red = guilt activation: (A) insula (x = −54, y = 17, z = 22); (B) superior frontal gyrus (x = 18, y = 47, z = 43); (C) middle temporal gyrus (x = −60, y = −34, z = 1); P < 0.0002.
Table 2 contains the results of the activations in the conditions 'shame minus neutral' and 'guilt minus neutral' with the associated Brodmann areas, hemispheres, coordinates, z-score and the number of voxel.
'Shame Minus Guilt' Condition (And Vice Versa). The shame vs guilt condition were both compared (shame > guilt and vice versa). Because of the subtraction method used for the contrast, only the areas that occur in one of the two conditions are presented (red = shame, blue = guilt). Thus, regions that are activated in both conditions are not indicated.
There was activation of different regions within the temporal lobe in both conditions [shame: cingulate gyrus (BA 32), bilateral parahippocampal gyrus (BA 27, 20, 34, 36); guilt: right fusiform gyrus (BA 37) and left middle temporal gyrus (BA 21)]. Additional frontal activation was found in the shame condition [anterior cingulate cortex (BA 24), right rectal gyrus (BA 11), right medial (BA 10) and right inferior frontal gyrus (BA 47)]. In the guilt condition, an activation of the right amygdala and the insula (BA 13) could be detected, which was not found in the shame condition (Table 3).
Gender Effects
Within the female sample there was an activation in the shame and guilt condition (shame > guilt) in the bilateral middle temporal gyrus (BA 19, 21, 39). In addition, the shame condition also activates the parietal lobe [right precuneus (BA 7, 31), right supramarginal gyrus (BA 40)], the temporal lobe [cingulate gyrus (BA 31), parahippocampal gyrus (BA 27)] and the frontal lobe [right precentral gyrus (BA 6), bilateral middle frontal gyrus (BA 10)] (Supplementary Table S2).
The male participants showed activations in shame and guilt (shame > guilt) in the right fusiform gyrus (BA 37). In contrast to the guilt condition, men showed more activation in the left parahippocampal gyrus (BA 35, 36) during the shame condition. The bilateral anterior cingulate cortex (BA 32) and the right orbital frontal gyrus (BA 47) also showed relatively increased activation. The guilt condition was associated with activation in the uncus (BA 34), the right amygdala. Additionally, there was also activation seen in the left inferior occipital and lingual gyrus (BA 18), and bilateral middle frontal gyrus (BA 10) (Supplementary Table S3).
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