Regional response differences across the human amygdaloid complex during social conditioning

Department of Psychological & Brain Sciences, Dartmouth College, 6207 Moore Hall, Hanover, NH 03755, USA.
Cerebral Cortex (Impact Factor: 8.67). 07/2009; 20(3):612-21. DOI: 10.1093/cercor/bhp126
Source: PubMed

ABSTRACT The amygdala is consistently implicated in biologically relevant learning tasks such as Pavlovian conditioning. In humans, the ability to identify individual faces based on the social outcomes they have predicted in the past constitutes a critical form of associative learning that can be likened to "social conditioning." To capture such learning in a laboratory setting, participants learned about faces that predicted negative, positive, or neutral social outcomes. Participants reported liking or disliking the faces in accordance with their learned social value. During acquisition, we observed differential functional magnetic resonance imaging activation across the human amygdaloid complex consistent with previous lesion, electrophysiological, and functional neuroimaging data. A region of the medial ventral amygdala and a region of the dorsal amygdala/substantia innominata showed signal increases to both Negative and Positive faces, whereas a lateral ventral region displayed a linear representation of the valence of faces such that Negative > Positive > Neutral. This lateral ventral locus also differed from the dorsal and medial loci in that the magnitude of these responses was more resistant to habituation. These findings document a role for the human amygdala in social learning and reveal coarse regional dissociations in amygdala activity that are consistent with previous human and nonhuman animal data.

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Available from: Tom Johnstone, Aug 18, 2015
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    • "As a consequence, it remains unclear whether socially anxious individuals react more sensitive to socially relevant stimuli. So far, there is only little research investigating the neural correlates of social conditioning, which is the associative process whereby humans learn to identify individuals that have predicted threats or rewards in the past (Davis et al., 2010). Davis examined social learning with neutral faces and written verbal feedback and reported increased amygdala activation in response to faces paired with negative and positive comments . "
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    ABSTRACT: In search of causative factors of social anxiety disorder (SAD), classical conditioning has been discussed as a potential trigger mechanism for many years. Recent findings suggest that the social relevance of the unconditioned stimulus (US) might play a major role in learning theories of SAD. Thus, this study applied a social conditioning paradigm with disorder-relevant US to examine the electrocortical correlates of affective learning. Twenty-four high socially anxious (HSA) and 23 age- and gender-matched low socially anxious (LSA) subjects were conditioned to 3 different faces flickering at a frequency of 15 Hz which were paired with auditory insults, compliments or neutral comments (US). The face-evoked electrocortical response was measured via steady-state visually evoked potentials and subjective measures of valence and arousal were obtained. Results revealed a significant interaction of social anxiety and conditioning, with LSA showing highest cortical activity to faces paired with insults and lowest activity to faces paired with compliments, while HSA did not differentiate between faces. No group differences were discovered in the affective ratings. The findings indicate a potentially impaired ability of HSA to discriminate between relevant and irrelevant social stimuli, which may constitute a perpetuating factor of SAD.
    Social Cognitive and Affective Neuroscience 10/2014; 10(7). DOI:10.1093/scan/nsu140 · 5.88 Impact Factor
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    • "According to anatomical data obtained in animal studies, the former is considered the major input system of the amygdala, receiving inputs from various sensory systems (Amaral et al., 1992; LeDoux, 1996), whereas the latter is considered a major output system of the amygdala, communicating with cortical systems through its connections with various neuromodulatory systems, such as the basal forebrain (Kapp et al., 1994; Jolkkonen et al., 2002). Despite the limited spatial resolution of fMRI, a similar anatomical distinction within the amygdala has been observed in a number of recent human fMRI studies, including those with resolution levels (i.e. 3 Â 3 Â 3 mm 3 voxel size) that are routinely employed by numerous neuroimaging laboratories (Morris et al., 2001; Whalen et al., 2001; Kim et al., 2003; Davis et al., 2010; Gamer et al., 2010; Bach et al., 2011). Furthermore, the regional differences within the amygdala that were observed in this study nicely corresponded to the known anatomy of the human amygdala, as well as to a recent theoretical framework about the functional dissociation between the amygdala subregions, which argues that the amygdala, particularly its dorsal subregion, is a key structure in detecting and resolving predictive uncertainty in an emotional context (Whalen et al., 2001; Kim et al., 2003). "
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    ABSTRACT: Despite the well-known role of the amygdala in mediating emotional interference during tasks requiring cognitive resources, no definite conclusion has yet been reached regarding the differential roles of functionally and anatomically distinctive subcomponents of the amygdala in such processes. In the present study, we examined female participants and attempted to separate the neural processes for the detection of emotional information from those for the regulation of cognitive interference from emotional distractors by adding a temporal gap between emotional stimuli and a subsequent cognitive Stroop task. Reaction time data showed a significantly increased Stroop interference effect following emotionally negative stimuli compared to neutral stimuli, and functional magnetic resonance imaging data revealed that the anterior ventral amygdala (avAMYG) showed greater responses to negative stimuli compared to neutral stimuli. In addition, individuals who scored high in neuroticism showed greater posterior dorsal amygdala (pdAMYG) responses to incongruent compared to congruent Stroop trials following negative stimuli, but not following neutral stimuli. Taken together, the findings of this study demonstrated functionally distinctive contributions of the avAMYG and pdAMYG to the emotion-modulated Stroop interference effect and suggested that the avAMYG encodes associative values of emotional stimuli while the pdAMYG resolves cognitive interference from emotional distractors.
    Social Cognitive and Affective Neuroscience 03/2013; DOI:10.1093/scan/nst021 · 5.88 Impact Factor
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    • "Given our previous demonstrations of amygdala responses to ambiguous facial expressions during passive viewing (Davis et al., 2010; Whalen et al., 2009; Kim et al., 2003 "
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    ABSTRACT: Extant research has examined the process of decision making under uncertainty, specifically in situations of ambiguity. However, much of this work has been conducted in the context of semantic and low-level visual processing. An open question is whether ambiguity in social signals (e.g., emotional facial expressions) is processed similarly or whether a unique set of processors come on-line to resolve ambiguity in a social context. Our work has examined ambiguity using surprised facial expressions, as they have predicted both positive and negative outcomes in the past. Specifically, whereas some people tended to interpret surprise as negatively valenced, others tended toward a more positive interpretation. Here, we examined neural responses to social ambiguity using faces (surprise) and nonface emotional scenes (International Affective Picture System). Moreover, we examined whether these effects are specific to ambiguity resolution (i.e., judgments about the ambiguity) or whether similar effects would be demonstrated for incidental judgments (e.g., nonvalence judgments about ambiguously valenced stimuli). We found that a distinct task control (i.e., cingulo-opercular) network was more active when resolving ambiguity. We also found that activity in the ventral amygdala was greater to faces and scenes that were rated explicitly along the dimension of valence, consistent with findings that the ventral amygdala tracks valence. Taken together, there is a complex neural architecture that supports decision making in the presence of ambiguity: (a) a core set of cortical structures engaged for explicit ambiguity processing across stimulus boundaries and (b) other dedicated circuits for biologically relevant learning situations involving faces.
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