Neural response to stress and perceived stress differ in patients with left temporal lobe epilepsy

Abstract

Patients with epilepsy are often able to predict seizure occurrence subsequent to an acute stress experience. However, neuroimaging investigations into the neural basis of this relationship or the potential influence of perceived life stress are limited. The current study assessed the relationship between perceived stress and the neurobehavioral response to stress in patients with left temporal lobe epilepsy (LTLE) and healthy controls (HCs) using heart rate, salivary cortisol level, and functional magnetic resonance imaging and compared these effects between HCs and LTLE. Matched on perceived stress levels, groups of 36 patients with LTLE and 36 HCs completed the Montreal Imaging Stress Task, with control and stress math task conditions. Among LTLEs, 27 reported that prior (acute) stress affected their seizures (LTLES+), while nine did not (LTLES−). The results revealed that increased perceived stress was associated with seizure frequency in LTLE. Further, cortisol secretion was greater in LTLE, but did not vary with perceived stress as observed in HCs. A linear mixed‐effects analysis revealed that as perceived stress increased, activation in the hippocampal complex (parahippocampal gyrus and hippocampus) decreased during stressful math in the LTLES+, increased in HCs, but did not vary in the LTLES−. Task‐based functional connectivity analyses revealed LTLE differences in hippocampal functional connectivity with sensory cortex specific to stressor modalities. We argue that the current study demonstrates an inhibitory hippocampal mechanism underlying differences in resilience to stress between HCs and LTLE, as well as LTLE patients who report stress as a precipitant of seizures.

FMRI response to acute psychological stress differentiates patients with psychogenic non-epileptic seizures from healthy controls – A biochemical and neuroimaging biomarker study

“…The fMRI response to acute psychological stress was assessed using two contrasts: negative versus positive auditory feedback, and hard versus easy math. This is consistent with previous studies utilizing negative versus positive feedback and/or difficult versus easy mental arithmetic in assessing fMRI stress response (Dedovic et al, 2005, Dedovic et al, 2009; Goodman et al, 2016, Goodman et al, 2019). Beta-weight values for the ideal waveform of each event and contrast were determined using linear regression with the 3dREMLfit program.…”

“…Despite the growing fMRI literature in PNES and FNDs, no imaging studies to date have specifically examined the neural underpinnings of psychological stress response in patients with PNES. Thus, we aimed to investigate how patients with PNES respond to acute psychological and emotional stress in a priori defined brain regions of interest (ROIs) involved in emotion processing (insula, hippocampus and amygdala), motor function (precentral gyrus and postcentral gyrus), and emotion/executive control (anterior cingulate and inferior frontal cortex) that have been indicated as vital nodes in the FND/PNES network (Aybek et al, 2014; Ding et al, 2013; Espay et al, 2018a, Espay et al, 2018, Espay et al, 2019; Hassa et al, 2017; Morris et al, 2017; Szaflarski et al, 2018; Szaflarski and LaFrance, 2018; van der Kruijs et al, 2012; Voon et al, 2010) and overlap with regions involved in the fMRI response to psychological stress (Dedovic et al, 2009; Goodman et al, 2019; Pruessner et al, 2008). Based on these previous studies, we hypothesized that compared to HCs, patients with PNES would exhibit similar physiological responses to acute psychological stress, differential fMRI response to acute psychological and emotional stress in these a priori brain regions of interest, and stronger rs-FC between emotion-regulation and motor-control regions.…”

Repeatability of Neural and Autonomic Responses to Acute Psychosocial Stress

“…As in all prior studies, the order of CMT followed by the SMT was identical for all subjects and was not counterbalanced (Allendorfer et al, 2014(Allendorfer et al, , 2019Goodman et al, 2016Goodman et al, , 2019Wheelock et al, 2018;Orem et al, 2019). As demonstrated repeatedly in the stress literature, the acute stress response takes up to 90 min to recover to baseline levels (Kirschbaum et al, 1993;Kudielka et al, 2004;Dedovic et al, 2005;Gaab et al, 2005).…”

“…Participants completed a volume control task during a multiecho reference scan designed to calibrate audio volume for the remainder of the study. Next, during BOLD Echo-Planar imaging (EPI), participants performed control math (CMT) and stress math tasks (SMT) that were adapted to include pre-recorded evaluative auditory feedback, regardless of performance in the tasks (Allendorfer et al, 2014(Allendorfer et al, , 2019Goodman et al, 2019). Participants selected the correct answer to the math problem via pressing either the "1, " "2, " or "3" button on an MR-compatible button box (Current Designs; Philadelphia, PA, United States).…”

“…In particular, the well-established fMRI Montreal Imaging Stress Task [MIST; (Dedovic et al, 2005)] is used for assessing the neural correlates of psychosocial stress reactivity. Prior studies utilizing MIST have demonstrated that a prefrontal cortex (PFC)-hippocampus-amygdala circuit mediates endocrine and autonomic stress responses (i.e., Pruessner et al, 2008;Dedovic et al, 2009a;Khalili-Mahani et al, 2010;Allendorfer et al, 2014;Wheelock et al, 2016Wheelock et al, , 2018Goodman et al, 2019). Despite these contributions to our understanding of the neurobiology of stress, the utility of MIST for assessing longitudinal within-subject changes in reactivity to a common stressor has yet to be validated.…”