Neurons in the human amygdala selective for perceived emotion

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.The human amygdala plays a crucial role in processing socially and emotionally salient stimuli (1, 2). A large literature, primarily from studies in animals, shows that the amygdala is critical for conditioned fear responses (3). However, a number of other studies show that it is involved also in broader aspects of social perception, notably aspects of face processing (4). These two themes converge in several human studies: there is an impairment in recognizing fear faces in subjects that lack a functional amygdala (5) in addition to the impairment of fear conditioning (6, 7). Neuroimaging studies have also reported significant activation of the amygdala to fear faces (8).In humans, it has been reported that amygdala neurons are selective for a variety of visual stimuli (9, 10). One category of stimuli that the amygdala plays a key role in analyzing is faces and facial emotions. Subjects with amygdala damage fail to recognize fear faces (5), although there is now a consensus that the amygdala is involved in processing many emotions from faces, not just fear (11). Electrophysiological recordings in monkeys have found single neurons that respond not only to faces as such (12, 13), but also to face identities, facial expressions, and gaze directions (14, 15). Single neurons in the human amygdala discriminate faces from inanimate objects (10). Furthermore, single neurons in the human amygdala were found to encode whole faces selectively (16) and show abnormal facial feature selectivity in autism (17). Thus, there is substantial evidence from neurophysiological, lesion, and functional MRI studies for the involvement of the primate amygdala in face processing.More detailed investigations suggest that impaired fear recognition after amygdala damage can be attributed to a failure to fixate on the eyes (18), suggesting that the amygdala might act as a detector of perceptual saliency and biological relevance (19, 20). This was complemented by a neuroimaging study showing that amygdala activity was specifically enhanced for fear faces when saccading from the mouth to the eye region (21). Patients with schizophrenia (22), social phobia (23), and autism (24) also show abnormal facial scanning patterns, which have been hypothesized to result from amygdala dysfunction (25). The functional role of the amygdala is supported by its connection with visual cortices specialized for face processing (26–28) as well as reciprocal connections with multiple visually responsive areas in the temporal (29–31) and frontal lobes (32). All of these findings, while supporting a clear role for the amygdala in face processing, also suggest that this role may be relatively specific for certain properties or features of faces, raising the question of what function distinguishes the amygdala’s role in face processing from the better-known role of temporal cortex in face processing (Discussion). We focused on one particular question in the present study.Neurons in the monkey and human amygdala respond to the emotional expression of faces, but it remains unknown whether these responses are driven primarily by image properties of the stimuli, by the perceptual judgments of the perceiver, or by behavioral categorization in terms of motor output. To investigate this question, we recorded 210 neurons from 7 neurosurgical patients with implanted depth electrodes on an established “bubbles” task (18, 33), in which patients discriminated emotions from sparsely sampled fear or happy faces. We first characterize neurons that distinguished fear vs. happy emotions expressed by the displayed faces, on those trials where subjects responded correctly. Next we show that these neurons tracked the patients’ subjective judgment regardless of whether it was correct or incorrect. Population permutation analysis confirmed the robustness of this result, on average, across the entire population of neurons. Our data suggest that neuronal responses within the human amygdala are selective for perceived emotion shown in faces and track subjective judgment expressed by behavior rather than visual properties of the stimuli.