Aberrant processing of social and affective information is a severe and disabling symptom across many neuropsychiatric disorders, including post-traumatic stress disorder (PTSD) and other anxiety disorders, depression, autism, and schizophrenia. Recent reports demonstrate that direct electrical brain stimulation (EBS) can alter perception, such as changing the identity of a person being viewed or causing memory-related hallucinations. If EBS can distort normal perception, then EBS using different parameters may be able to normalize SAP, for example by modulating affective salience to visual stimuli in PTSD. One key impediment towards developing EBS as a therapy for SAP pathology is that we lack an understanding of how electrical stimulation modulates neurodynamics and cognition. A critical step towards designing rational EBS-based stimulation parameters for SAP pathology is building a causal model of the millisecond-scale temporal dynamics, interregional interactions, and EBS modulation of these dynamics and interactions during SAP. Visual SAP relies on a neural circuit in the temporal lobe that includes the amygdala, fusiform gyrus (FG), and posterior superior temporal sulcus (pSTS). Non-invasive brain imaging techniques either lack the temporal resolution to examine millisecond dynamics (fMRI/PET), or are relatively insensitive to activity in deep brain structures such as the amygdala (MEG/EEG/TMS). Direct neural recordings using intracranial electroencephalography (iEEG) in individuals undergoing neurosurgical evaluation for epilepsy will allow us to overcome these barriers to study the dynamics and interactions in the SAP circuit. Furthermore, delivery of EBS via these implanted electrodes will allow us to examine how electrical modulation of this circuit alters SAP. Using iEEG and advanced analysis methods from machine learning, we recently delineated the set of information processing stages that FG goes through for face perception. In this project, we will test a three- stage dynamic model of the sequence of events and interregional interactions that enable SAP based on these previous results, the work of others, and our preliminary data. We will record iEEG in our regions of interest to test neural dynamics during three critical aspects of social affective processing: perception of facial expression (Aim 1), the inference of actions from motion (Aim 2), and guiding conscious perception to affectively and socially salient stimuli (Aim 3). Then we will employ EBS to modulate perception during these processes. In addition, we will supplement iEEG with magnetoencephalography (MEG), which, while less sensitive to amygdala activity, provides whole-brain cortical coverage and facilitates the comparison of iEEG results to a normative population. The outcome of the proposed research will be a spatially and temporally specific model of the causal dynamics and interactions during SAP. This model will provide testable hypotheses regarding targeted EBS therapies that may normalize pathological SAP.
Abnormalities in social affective perception are a critical part of the etiology of numerous neuropsychiatric diseases, such as autism, schizophrenia, and post-traumatic stress disorder. The proposed research will map the detailed neurodynamics of critical aspects of social affective perception and examine how these neurodynamics, and the associated cognitions, can be modulated by brain stimulation. The results of this research will lead to a deeper understanding of the neurobiology of social affective perception, a circuit relevant to a number of mental disorders, and take a critical step towards determining how brain stimulation may be used to remediate pathological social affective perception.
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