An official website of the United States government
Abstract Processing facial expressions of emotion draws on a distributed brain network. In particular, judging ambiguous facial emotions involves coordination between multiple brain areas. Here, we applied multimodal functional connectivity analysis to achieve network-level understanding of the neural mechanisms underlying perceptual ambiguity in facial expressions. We found directional effective connectivity between the amygdala, dorsomedial prefrontal cortex (dmPFC), and ventromedial PFC, supporting both bottom-up affective processes for ambiguity representation/perception and top-down cognitive processes for ambiguity resolution/decision. Direct recordings from the human neurosurgical patients showed that the responses of amygdala and dmPFC neurons were modulated by the level of emotion ambiguity, and amygdala neurons responded earlier than dmPFC neurons, reflecting the bottom-up process for ambiguity processing. We further found parietal-frontal coherence and delta-alpha cross-frequency coupling involved in encoding emotion ambiguity. We replicated the EEG coherence result using independent experiments and further showed modulation of the coherence. EEG source connectivity revealed that the dmPFC top-down regulated the activities in other brain regions. Lastly, we showed altered behavioral responses in neuropsychiatric patients who may have dysfunctions in amygdala-PFC functional connectivity. Together, using multimodal experimental and analytical approaches, we have delineated a neural network that underlies processing of emotion ambiguity.
more »
« less
A Neurocomputational Model of Posttraumatic Stress Disorder
Despite the well-defined behavioral criteria for posttraumatic stress disorder (PTSD), clinical care is com- plicated by the heterogeneity of biological factors underly- ing impairment. Eye movement tasks provide an opportunity to assess the relationships between aberrant neurobiological function and non-volitional performance metrics that are not dependent on self-report. A recent study using an emotional variant of the antisaccade task demonstrated attentional control biases that interfered with task performance in Veterans with PTSD. Here we present a neuroanatomically-inspired com- putational model based on gated attractor networks that is designed to replicate oculomotor behavior on an affective anti- saccade task. The model includes the putative neural circuitry underlying fear response (amygdala) and top-down inhibitory control (prefrontal cortex), and is capable of generating testable predictions about the causal implications of changes in this circuitry on task performance and neural activation associated with PTSD. Calibrating the model with the results of behavioral and neuroimaging studies on patient populations yields a pattern of connectivity changes characterized by increased amygdala sensitivity and reduced top-down prefrontal control that is consistent with the fear conditioning model of PTSD. In addition, the model makes experimentally verifiable predictions about the consequences of increased prefrontal connectivity associated with cognitive reappraisal training. Keywords: posttraumatic stress disorder, antisaccade task, inhibitory control deficits, attentional bias, cognitive control.
more »
« less
- Award ID(s):
- 1632976
- PAR ID:
- 10287578
- Date Published:
- Journal Name:
- International IEEE/EMBS Conference on Neural Engineering 2021
- Page Range / eLocation ID:
- 107 to 110
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract The neurophysiological mechanisms in the human amygdala that underlie post-traumatic stress disorder (PTSD) remain poorly understood. In a first-of-its-kind pilot study, we recorded intracranial electroencephalographic data longitudinally (over one year) in two male individuals with amygdala electrodes implanted for the management of treatment-resistant PTSD (TR-PTSD) under clinical trial NCT04152993. To determine electrophysiological signatures related to emotionally aversive and clinically relevant states (trial primary endpoint), we characterized neural activity during unpleasant portions of three separate paradigms (negative emotional image viewing, listening to recordings of participant-specific trauma-related memories, and at-home-periods of symptom exacerbation). We found selective increases in amygdala theta (5–9 Hz) bandpower across all three negative experiences. Subsequent use of elevations in low-frequency amygdala bandpower as a trigger for closed-loop neuromodulation led to significant reductions in TR-PTSD symptoms (trial secondary endpoint) following one year of treatment as well as reductions in aversive-related amygdala theta activity. Altogether, our findings provide early evidence that elevated amygdala theta activity across a range of negative-related behavioral states may be a promising target for future closed-loop neuromodulation therapies in PTSD.more » « less
-
REM sleep is important for the processing of emotional memories, including fear memories. Rhythmic interactions, especially in the theta band, between the medial prefrontal cortex (mPFC) and limbic structures are thought to play an important role, but the ways in which memory processing occurs at a mechanistic and circuits level are largely unknown. To investigate how rhythmic interactions lead to fear extinction during REM sleep, we used a biophysically based model that included the infralimbic cortex (IL), a part of the mPFC with a critical role in suppressing fear memories. Theta frequency (4–12 Hz) inputs to a given cell assembly in IL, representing an emotional memory, resulted in the strengthening of connections from the IL to the amygdala and the weakening of connections from the amygdala to the IL, resulting in the suppression of the activity of fear expression cells for the associated memory. Lower frequency (4 Hz) theta inputs effected these changes over a wider range of input strengths. In contrast, inputs at other frequencies were ineffective at causing these synaptic changes and did not suppress fear memories. Under post-traumatic stress disorder (PTSD) REM sleep conditions, rhythmic activity dissipated, and 4 Hz theta inputs to IL were ineffective, but higher-frequency (10 Hz) theta inputs to IL induced changes similar to those seen with 4 Hz inputs under normal REM sleep conditions, resulting in the suppression of fear expression cells. These results suggest why PTSD patients may repeatedly experience the same emotionally charged dreams and suggest potential neuromodulatory therapies for the amelioration of PTSD symptoms. SIGNIFICANCE STATEMENT Rhythmic interactions in the theta band between the mPFC and limbic structures are thought to play an important role in processing emotional memories, including fear memories, during REM sleep. The infralimbic cortex (IL) in the mPFC is thought to play a critical role in suppressing fear memories. We show that theta inputs to the IL, unlike other frequency inputs, are effective in producing synaptic changes that suppress the activity of fear expression cells associated with a given memory. Under PTSD REM sleep conditions, lower-frequency (4 Hz) theta inputs to the IL do not suppress the activity of fear expression cells associated with the given memory but, surprisingly, 10 Hz inputs do. These results suggest potential neuromodulatory therapies for PTSD.more » « less
-
Self-control failures are often attributed to a lack of top-down behavioral regulation. Self-report measures of selfcontrol reflect higher-level cognitive appraisals of behavioral control and lower-level innate temperamental traits associated with reactive processes. However, few studies have examined the extent to which different aspects of self-control relate to reactive processes. Using a large sample (n = 246), we investigated whether individual differences in six self-control trait measures were predictive of low-level processing indexed by the mismatch negativity (MMN) elicited from a passive auditory oddball task. Larger MMNs are associated with greater prediction error when the input stimulus conflicts with expectation. Self-control traits were measured by effortful control, perfectionism, impulsiveness, procrastination, perceived stress, and anxiety scales. We assumed personality traits develop around innate differences in reaction to environmental changes, resulting in differential adult expressions of self-control reflected in the six traits. All but perfectionism and perceived stress correlated with MMN amplitudes: reater self-control associated with smaller MMNs; stronger negative traits associated with larger MMNs. When the correlated measures were entered into a backwards multiple regression on MMN amplitudes, procrastination and anxiety remained in the model as significant, relatively independent contributors. Procrastination may reflect a top-down modulation of underlying reactivity. Trait anxiety may reflect a basic temperament of greater reactivity to environmental change. Individuals with strong innate reactivity and weaker top-down processes may be hypervigilant to deviations from expectation, producing larger prediction errors and MMNs. Self-control failures may reflect reduced top-down control, when the balance in cortical activity favors reactive systems over the prefrontal cortex.more » « less
-
Sustained attention (SA) is essential for maintaining focus over time, with disruptions linked to various neuro- logical and psychiatric disorders. The oscillatory dynamics and functional connectivity in the dorsal fronto- parietal network (dFPN) are crucial in SA. However, the neuronal mechanisms that control the level of SA, especially in response to heightened attentional demands, remain poorly understood. To examine the role of rhythmic synchronization in the dFPN in SA, we recorded local 昀椀eld potential and single unit activity in ferrets that performed the 5-Choice Serial Reaction Time Task (5-CSRTT) under both low and high attentional load. Under high attentional load, dFPN exhibited a pronounced state shift that corresponded with behavioral changes in the animal. Prior to the onset of the target stimulus, animals transitioned from a stationary state, characterized by frontal theta oscillations and dFPN theta connectivity, to an active exploration state associated with sensory processing. This shift was indexed by a suppression of inhibitory alpha oscillations and an increase in excitatory theta and gamma oscillations in parietal cortex. We further show that dFPN theta connectivity predicts per- formance 昀氀uctuations under high attentional load. Together, these results suggest that behavioral strategies for maintaining SA are tightly linked to neuronal state dynamics in the dFPN. Importantly, these 昀椀ndings identify rhythmic synchronization within the FPN as a potential neural target for novel therapeutic strategies for dis- rupted attention.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Conference Paper:
- https://doi.org/10.1109/NER49283.2021.9441345
