Neurons in the human amygdala selective for perceived emotion

Abstract

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.human single unit | medial temporal lobe | limbic system | hippocampus | intracranial

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

“…The neuronal activity in the STN that we observed in the late window (500-2,000 ms) may reflect the formation of conceptual knowledge related to emotional valence and arousal, because this is in line with the late neuronal response (625-1,500 ms) related to different valences of stimuli already described in the amygdala (18). We may speculate that the information represented in ratings of emotional valence and arousal in the late time window depends on processes involving the orbitofrontal and ventromedial prefrontal cortex, which provide significant input to the STN and play a major role in stimulus subjective valuation, representation of hedonic pleasure and value-based decision making (48)(49)(50)(51).…”

“…One such factor is that the study was conducted with PD patients, who are known to have a widespread central nervous system pathology (78) and to experience problems in emotional processing (79), and thus the number of neurons responding to emotional stimuli in the STN might be different from that in healthy subjects. Their number is rather low, but nonetheless is comparable to that reported in previous relevant single-neuron studies on emotion in humans (15,18). Another factor that might have contributed to the relatively low number of neurons is that the study was limited to the routine trajectory of intraoperative microrecording exploration targeting the lateral sensorimotor part of the STN, which has shown less reactivity to emotional stimuli than the ventromedial part (67).…”

“…Participation of the STN in processing emotion has not yet been investigated directly at the single-neuron level in humans. Nonetheless, single-neuron activity related to a priori defined emotional categories (e.g., positive vs. negative) has been detected in a few human brain regions, including the hippocampus, amygdala, and prefrontal and subcallosal cortex (15)(16)(17)(18).…”

“…It has been shown that different features of tasks are linked to neuronal activity in different frequency bands. Whereas beta band oscillations (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) restricted to the dorsolateral (sensorimotor) part of the STN are linked mainly to motor functions and their alteration in PD (23)(24)(25), the gamma band oscillations (30-100 Hz) perhaps have a more general meaning. Along with motor functions, they are modulated by picture perception and early emotional arousal (26,27).…”

The Neuro-Environmental Loop of Plasticity: A Cross-Species Analysis of Parental Effects on Emotion Circuitry Development Following Typical and Adverse Caregiving

“…In a very recent study, 200 single neuron recordings were taken from the amygdala of neurosurgical patients (presurgery) while they looked at degraded pictures of emotion-expressing faces. Amygdala reactivity was found to track patients' subjective judgments of emotions during that task (Wang et al, 2014), suggesting a specific role for the amygdala in emotion perception, rather than correct emotion identification. Amygdala also plays a prominent role in fear learning.…”