Learning affective values for faces is expressed in amygdala and fusiform gyrus (original) (raw)
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Affective learning increases sensitivity to graded emotional faces
Emotion, 2008
How does the affective significance of emotional faces affect perceptual decisions? We manipulated affective significance by pairing 100% fearful faces with aversive electrical stimulation and hypothesized that increasing the significance of a stimulus via its prior history would lead to enhanced processing. After fear conditioning, participants viewed graded emotional faces that ranged from neutral to fearful. Faces were shown either in a color that was previously paired with shock or a color not paired with shock during conditioning. Increases in the frequency of "fearful" responses for faces shown in the shock-paired color were most robust for faces at intermediate intensity levels (40 -60% fearful). Psychometric fits to the data revealed significant increased sensitivity for shock-paired relative to unpaired faces. Thus, despite identical physical features for shock-paired and unpaired stimuli (aside from the color, which was counterbalanced), more frequent (and faster) "fearful" responses were made when participants viewed affectively significant stimuli.
Preferential Amygdala Reactivity to the Negative Assessment of Neutral Faces
Biological Psychiatry, 2009
Background: Prior studies suggest that the amygdala shapes complex behavioral responses to socially ambiguous cues. We explored human amygdala function during explicit behavioral decision making about discrete emotional facial expressions that can represent socially unambiguous and ambiguous cues.
2013
Learning does not only depend on rationality, because real-life learning cannot be isolated from emotion or social factors. Therefore, it is intriguing to determine how emotion changes learning, and to identify which neural substrates underlie this interaction. Here, we show that the task-independent presentation of an emotional face before a reward-predicting cue increases the speed of cue-reward association learning in human subjects compared with trials in which a neutral face is presented. This phenomenon was attributable to an increase in the learning rate, which regulates reward prediction errors. Parallel to these behavioral findings, functional magnetic resonance imaging demonstrated that presentation of an emotional face enhanced reward prediction error (RPE) signal in the ventral striatum. In addition, we also found a functional link between this enhanced RPE signal and increased activity in the amygdala following presentation of an emotional face. Thus, this study revealed an acceleration of cue-reward association learning by emotion, and underscored a role of striatum-amygdala interactions in the modulation of the reward prediction errors by emotion.
Role of the monkey amygdala in social cognition
International Congress Series, 2003
Recent studies demonstrated the role of the primate amygdala (AM) in social cognition. In the present study, neuronal responses in the monkey amygdala were analyzed during discrimination of facial expressions and discrimination of various rewarding and aversive stimuli, such as food and objects associated with electric shock. The results indicated that activity of some amygdalar neurons preferentially increased in response to human facial expressions. Patterns of correlation coefficients between the different facial expressions indicated that facial expressions of a familiar person to the monkey were more discriminately represented than those of unfamiliar persons. Furthermore, responses of these neurons to facial expressions seemed to be independent of reward contingency. Other neurons responded to various objects that were biologically important, including food as reward and real humans. These amygdalar neurons displayed modulation of responses to the objects in various situations, including satiation and reversal, and modulation of responses to real humans who approached and withdrew from the monkey. These results suggest that there are at least two classes of amygdalar neurons: one type of neuron is involved in processes independent of one's own emotional state such as recognition of facial expression and inferring the emotional states of other persons, and the other type is involved in the ongoing evaluation of all sensory stimuli based on one's own emotional state.
Neural mechanisms of affective matching across faces and scenes
The emotional matching paradigm, introduced by Hariri and colleagues in 2000, is a widely used neuroimaging experiment that reliably activates the amygdala. In the classic version of the experiment faces with negative emotional expression and scenes depicting distressing events are compared with geometric shapes instead of neutral stimuli of the same category (i.e. faces or scenes). This makes it difficult to clearly attribute amygdala activation to the emotional valence and not to the social content. To improve this paradigm, we conducted a functional magnetic resonance imaging study in which emotionally neutral and, additionally, positive stimuli within each stimulus category (i.e. faces, social and non-social scenes) were included. These categories enabled us to differentiate the exact nature of observed effects in the amygdala. First, the main findings of the original paradigm were replicated. Second, we observed amygdala activation when comparing negative to neutral stimuli of the same category. However, for negative faces, the amygdala response habituated rapidly. Third, positive stimuli were associated with widespread activation including the insula and the caudate. This validated adaption study enables more precise statements on the neural activation underlying emotional processing. These advances may benefit future studies on identifying selective impairments in emotional and social stimulus processing. Amygdala functioning is of high interest for clinical psychology, psychiatry and neuroscience, as heightened amygdala activation has been reported in various patient groups 1-5. The emotional matching paradigm by Hariri et al. 6 and its extended version 7 are widely used as emotional reactivity measures, which reliably activate the amygdala 8-10. Despite its current use in psychiatry, this paradigm has a potential drawback since faces with negative emotional expressions and negative social scenes are compared with simple geometric shapes. Thus, it compares pictures that differ in more than one domain: social content and emotional valence. It is therefore difficult to draw conclusions about which of the two different domains causes the increase in amygdala activation. This differentiation may arguably not be relevant for all purposes, but to study specific populations, such as patients with deficits in one or the other domain (e.g. those with autism spectrum disorder (ASD)) 11,12 , it is crucial to distinguish the two. A second issue is that negative emotions have been studied more widely than positive emotions, as exemplified by the original emotional matching paradigm, putatively due to their high functional value for action. For example previous research suggests that threatening scenes, whether they contained faces or no human features, elicited activation in the extrastriate body area, suggesting that this activity to threatening scenes, represents the capacity of the brain to associate certain situations with threat, in order to prepare for fast reactions 13. Positive emotions are, however, the other side of the coin, as they allow psychological growth and well-being 14. Positive stimuli are most commonly used in the context of reward experiments, for example in performance-based feedback tasks 15,16. A brain region that has been related to the processing of various reward types, ranging from primary reinforcers to more abstract social rewards 17,18 , is the ventral striatum 19. Also, meta-analytically, the ventral striatum elicits the strongest activation across the different reward types such as monetary, food and erotic rewards 20. The amygdala was also found to be activated in response to positive stimuli. For direct comparisons of positive and negative faces, not all studies found amygdala activation differences 21 , but a meta-analysis of 1
Transient Neural Activation in Human Amygdala Involved in Aversive Conditioning of Face and Voice
Journal of Cognitive Neuroscience, 2010
■ Elucidating the neural mechanisms involved in aversive conditioning helps find effective treatments for psychiatric disorders such as anxiety disorder and phobia. Previous studies using fMRI and human subjects have reported that the amygdala plays a role in this phenomenon. However, the noxious stimuli that were used as unconditioned stimuli in previous studies (e.g., electric shock) might have been ecologically invalid because we seldom encounter such stimuli in daily life. Therefore, we investigated whether a face stimulus could be conditioned by using a voice that had negative emotional valence and was collected from a real-life environment. A skin conductance response showed that healthy subjects were con-ditioned by using these stimuli. In an fMRI study, there was greater amygdala activation in response to the faces that had been paired with the voice than to those that had not. The right amygdala showed transient activity in the early stage of acquisition. A psychophysiological interaction analysis indicated that the subcortical pathway from the medial geniculate body to the amygdala played a role in conditioning. Modulation of the subcortical pathway by voice stimuli preceded the transient activity in the amygdala. The finding that an ecologically valid stimulus elicited the conditioning and amygdala response suggests that our brain is automatically processing unpleasant stimuli in daily life. ■
Neurons in the human amygdala selective for perceived emotion
2014
The human amygdala plays a key role in recognizing facial emotions and neurons in the monkey and human amygdala respond to the emotional expression of faces. However, it remains unknown whether these responses are driven primarily by properties of the stimulus or by the perceptual judgments of the perceiver. We investigated these questions by recording from over 200 single neurons in the amygdalae of 7 neurosurgical patients with implanted depth electrodes. We presented degraded fear and happy faces and asked subjects to discriminate their emotion by button press. During trials where subjects responded correctly, we found neurons that distinguished fear vs. happy emotions as expressed by the displayed faces. During incorrect trials, these neurons indicated the patients' subjective judgment. Additional analysis revealed that, on average, all neuronal responses were modulated most by increases or decreases in response to happy faces, and driven predominantly by judgments about the eye region of the face stimuli. Following the same analyses, we showed that hippocampal neurons, unlike amygdala neurons, only encoded emotions but not subjective judgment. Our results suggest that the amygdala specifically encodes the subjective judgment of emotional faces, but that it plays less of a role in simply encoding aspects of the image array. The conscious percept of the emotion shown in a face may thus arise from interactions between the amygdala and its connections within a distributed cortical network, a scheme also consistent with the long response latencies observed in human amygdala recordings.
Brain Responses to the Acquired Moral Status of Faces
Neuron, 2004
seen during perception of biological motion as well as Institute of Neurology during more abstract tasks involving inferences about University College of London intentions, beliefs, and feelings of other persons (for London WC1N 3BG reviews, see Allison et al., 2000; Frith and Frith, 2003; United Kingdom Puce and Perrett, 2003). Further evidence for this circuitry derives from imaging studies focusing on the processing of socially salient features in the human face Summary such as emotional expressions (Morris et al., 1996; Phillips et al., 1997; Winston et al., 2003), facial attractiveness We examined whether neural responses associated (Aharon et al., 2001; O'Doherty et al., 2003), trustworthiwith judgments of socially relevant aspects of the huness (Winston et al., 2002), or racial identity (Hart et al., man face extend to stimuli that acquire their signifi-2000; Phelps et al., 2000; Phelps, 2001). These studies cance through learning in a meaningful interactive conhighlight engagement of the amygdala, dorsal and ventral text, specifically reciprocal cooperation. During fMRI, striatum, orbitofrontal cortex (OFC), insula, and highersubjects made gender judgments on faces of people order visual areas such as fusiform face areas and supewho had been introduced as fair (cooperators) or unrior temporal sulcus (STS) in deliberative and implicit fair (defector) players through repeated play of a sesocial judgments. quential Prisoner's Dilemma game. To manipulate moral