The Role of the Subgenual Anterior Cingulate Cortex and Amygdala in Environmental Sensitivity to Infant Crying.

Newborns and infants communicate their needs and physiological states through crying and emotional facial expressions. Little is known about individual differences in responding to infant crying. Several theories suggest that people vary in their environmental sensitivity with some responding generally more and some generally less to environmental stimuli. Such differences in environmental sensitivity have been associated with personality traits, including neuroticism. This study investigated whether neuroticism impacts neuronal, physiological, and emotional responses to infant crying by investigating blood-oxygenation-level dependent (BOLD) responses using functional magnetic resonance imaging (fMRI) in a large sample of healthy women (N = 102) with simultaneous skin conductance recordings. Participants were repeatedly exposed to a video clip that showed crying infants and emotional responses (valence, arousal, and irritation) were assessed after every video clip presentation. Increased BOLD signal during the perception of crying infants was found in brain regions that are associated with emotional responding, the amygdala and anterior insula. Significant BOLD signal decrements (i.e., habituation) were found in the fusiform gyrus, middle temporal gyrus, superior temporal gyrus, Broca's homologue on the right hemisphere, (laterobasal) amygdala, and hippocampus. Individuals with high neuroticism showed stronger activation in the amygdala and subgenual anterior cingulate cortex (sgACC) when exposed to infant crying compared to individuals with low neuroticism. In contrast to our prediction we found no evidence that neuroticism impacts fMRI-based measures of habituation. Individuals with high neuroticism showed elevated skin conductance responses, experienced more irritation, and perceived infant crying as more unpleasant. The results support the hypothesis that individuals high in neuroticism are more emotionally responsive, experience more negative emotions, and may show enhanced cognitive control during the exposure to infant distress, which may impact infant-directed behavior.

Who gets afraid in the MRI-scanner? Neurogenetics of state-anxiety changes during an fMRI experiment.

Experiments using functional magnetic resonance imaging (fMRI) play a fundamental role in affective neuroscience. When placed in an MR scanner, some volunteers feel safe and relaxed in this situation, while others experience uneasiness and fear. Little is known about the basis and consequences of such inter-individually different responses to the general experimental fMRI setting. In this study emotional stimuli were presented during fMRI and subjects' state-anxiety was assessed at the onset and end of the experiment while they were within the scanner. We show that Val/Val but neither Met/Met nor Val/Met carriers of the catechol-O-methyltransferase (COMT) Val(158)Met polymorphism-a prime candidate for anxiety vulnerability-became significantly more anxious during the fMRI experiment (N=97 females: 24 Val/Val, 51 Val/Met, and 22 Met/Met). Met carriers demonstrated brain responses with increased stability over time in the right parietal cortex and significantly better cognitive performances likely mediated by lower levels of anxiety. Val/Val, Val/Met and Met/Met did not significantly differ in state-anxiety at the beginning of the experiment. The exposure of a control group (N=56 females) to the same experiment outside the scanner did not cause a significant increase in state-anxiety, suggesting that the increase we observe in the fMRI experiment may be specific to the fMRI setting. Our findings reveal that genetics may play an important role in shaping inter-individual different emotional, cognitive and neuronal responses during fMRI experiments.

Time scales of auditory habituation in the amygdala and cerebral cortex.

Habituation is a fundamental form of learning manifested by a decrement of neuronal responses to repeated sensory stimulation. In addition, habituation is also known to occur on the behavioral level, manifested by reduced emotional reactions to repeatedly presented affective stimuli. It is, however, not clear which brain areas show a decline in activity during repeated sensory stimulation on the same time scale as reduced valence and arousal experience and whether these areas can be delineated from other brain areas with habituation effects on faster or slower time scales. These questions were addressed using functional magnetic resonance imaging acquired during repeated stimulation with piano melodies. The magnitude of functional responses in the laterobasal amygdala and in related cortical areas and that of valence and arousal ratings, given after each music presentation, declined in parallel over the experiment. In contrast to this long-term habituation (43 min), short-term decreases occurring within seconds were found in the primary auditory cortex. Sustained responses that remained throughout the whole investigated time period were detected in the ventrolateral prefrontal cortex extending to the dorsal part of the anterior insular cortex. These findings identify an amygdalocortical network that forms the potential basis of affective habituation in humans.

Anatomical specificity of functional amygdala imaging of responses to stimuli with positive and negative emotional valence.

Non-invasive neuroimaging is increasingly used for investigating the human amygdala. Accurate functional localization in the amygdala region is, however, challenging and quantitative data on the anatomical specificity of functional amygdala imaging is lacking. We have therefore retrospectively investigated 114 recently published human functional imaging studies concerned with the amygdala. We determined the anatomical assignment probabilities of a total of 339 reported activation sites to the amygdala defined using a cytoarchitectonically verified probabilistic atlas system. We find that approximately 50% of reported responses were located in the region with high probability (> or =80%) of belonging to the amygdala. This group included responses related both to stimuli of positive and negative emotional valence. Approximately 10% of reported response sites were assigned to the hippocampus, with up to 100% assignment probability. The remaining peaks were either located in the border regions of the amygdala and/or hippocampus or outside of both of these structures. Within the amygdala, the majority of peaks (96.3%) were found in the laterobasal (LB) and superficial (SF) subregions. Only 3.7% of peaks were found in the centromedial group (CM), possibly because anatomically delineating the CM region of the amygdala is particularly difficult and hence its extent might have been underestimated. Moreover, these results show that a core region of the amygdala is responsive to stimuli both of positive and negative emotional valence. The current findings highlight the usefulness of probabilistic amygdala maps and also point to a need for the development of accurate in vivo delineation and parcellation of the amygdala.

Functional organization of the human anterior insular cortex.

The human insular cortex is involved in a wide range of functions including motor control, language, and homeostatic regulation. Little is known, however, how these functions are topographically organized in the insular cortex and how they are functionally related to the amygdala, which is anatomically connected to the insular cortex. We have investigated these questions by conducting an activation likelihood estimate (ALE) meta-analysis of previously published neuroimaging studies reporting insula effects. We find auditory and language tasks to preferentially activate an area in the dorsal part of the anterior insular cortex (AIC). Motor tasks involving both the upper and lower extremity reproducibly activated a posterior AIC region, adjacent to the sulcus centralis insulae (SCI). Significant co-activation with the probabilistically defined amygdala was located in the ventral AIC where also responses related to peripheral physiological changes were repeatedly reported. These findings show that the human AIC is a functionally differentiated brain region. The dorsal region of the AIC may be involved in auditory-motor integration, while the ventral part of the AIC may interface the amygdala with insular regions involved in the regulation of physiological changes related to emotional states. Thus, the present findings provide insights into the organization of human AIC and a methodological approach that may be further used to refine the emerging functional map of the insular cortex.