Trauma-associated anterior cingulate connectivity during reward learning predicts affective and anxiety states in young adults

Eckstrand, Kristen; Hanford, Lindsay; Bertocci, Michele; Chase, Henry W.; Greenberg, Tsafrir; Lockovich, Jeanette; Stiffler, Richelle; Aslam, Haris; Graur, Simona; Bebko, Genna; Forbes, Erika E.; Phillips, Mary L.

doi:10.1017/s0033291718002520

Cited by 18 publications

(13 citation statements)

References 70 publications

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“…The thalamus and insula are two key components of the reward neurocircuitry which links motivation with complex behaviors [76]. Auditory participats in the reward process with acoustic stimuli [77], and anxiety disorders often exert negative effect on the reward network [78]. More work is needed to determine how SNHL contributes to reward process and its correlation with SNHL-induced anxiety.…”

Section: Discussionmentioning

confidence: 99%

Dissociation between Cerebellar and Cerebral Neural Activities in Humans with Long-Term Bilateral Sensorineural Hearing Loss

Yun

Tang

et al. 2019

Neural Plasticity

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Abnormal neural activity in the cerebellum has been implicated in hearing impairments, but the effects of long-term hearing loss on cerebellar function are poorly understood. To further explore the role of long-term bilateral sensorineural hearing loss on cerebellar function, we investigated hearing loss-induced changes among neural networks within cerebellar subregions and the changes in cerebellar-cerebral connectivity patterns using resting-state functional MRI. Twenty-one subjects with long-term bilateral moderate-to-severe sensorineural hearing loss and 21 matched controls with clinically normal hearing underwent MRI scanning and a series of neuropsychological tests targeting cognition and emotion. Voxel-wise functional connectivity (FC) analysis demonstrated decreased couplings between the cerebellum and other cerebral areas, including the temporal pole (TP), insula, supramarginal gyrus, inferior frontal gyrus (IFG), medial frontal gyrus, and thalamus, in long-term bilateral sensorineural hearing loss patients. An ROI-wise FC analysis found weakened interregional connections within cerebellar subdivisions. Moreover, there was a negative correlation between anxiety and FC between the left cerebellar lobe VI and left insula. Hearing ability and anxiety scores were also correlated with FC between the left cerebellar lobe VI and left TP, as well as the right cerebellar lobule VI and left IFG. Our results suggest that sensorineural hearing loss disrupts cerebellar-cerebral circuits, some potentially linked to anxiety, and interregional cerebellar connectivity. The findings contribute to a growing body showing that auditory deprivation caused by cochlear hearing loss disrupts not only activity with the classical auditory pathway but also portions of the cerebellum that communicates with other cortical networks.

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Section: Discussionmentioning

confidence: 99%

Dissociation between Cerebellar and Cerebral Neural Activities in Humans with Long-Term Bilateral Sensorineural Hearing Loss

Yun

Tang

et al. 2019

Neural Plasticity

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“…In addition to changes in regional brain activity, emotional perception may also alter the interregional functional connectivity (FC) as well as the brain network topology. At the connectivity level, studies have employed FC analysis and investigated reorganized FC induced by emotional processing (Anticevic et al, 2011; Kim et al, 2011; Klapwijk et al, 2013; Eckstrand et al, 2018; Ewbank et al, 2018). At the network level, the recent advancement in computational approaches, especially graph-theoretical analysis, has provided the means to characterize the brain network topology (Rubinov and Sporns, 2010).…”

Section: Introductionmentioning

confidence: 99%

Investigation of functional brain network reconfiguration during vocal emotional processing using graph-theoretical analysis

Lin

Lee

Chen

et al. 2019

Social Cognitive and Affective Neuroscience

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Vocal expression is essential for conveying the emotion during social interaction. Although vocal emotion has been explored in previous studies, little is known about how perception of different vocal emotional expressions modulates the functional brain network topology. In this study, we aimed to investigate the functional brain networks under different attributes of vocal emotion by graph-theoretical network analysis. Functional magnetic resonance imaging (fMRI) experiments were performed on 36 healthy participants. We utilized the Power-264 functional brain atlas to calculate the interregional functional connectivity (FC) from fMRI data under resting state and vocal stimuli at different arousal and valence levels. The orthogonal minimal spanning trees method was used for topological filtering. The paired-sample t -test with Bonferroni correction across all regions and arousal–valence levels were used for statistical comparisons. Our results show that brain network exhibits significantly altered network attributes at FC, nodal and global levels, especially under high-arousal or negative-valence vocal emotional stimuli. The alterations within/between well-known large-scale functional networks were also investigated. Through the present study, we have gained more insights into how comprehending emotional speech modulates brain networks. These findings may shed light on how the human brain processes emotional speech and how it distinguishes different emotional conditions.

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“…The FC between IPL and frontal regions is implicated in attention control and decision‐making processes (Chen et al, 2013), the FC between IPL and visual regions subserves visual attentional processing (Numssen, Bzdok, & Hartwigsen, 2021), and the FC between insula and STG is involved in internal‐focused attention (Jang et al, 2018). Previous studies have found reduced FCs of the IPL with visual regions (Philip, Kuras, et al, 2013) and ACC (Eckstrand et al, 2019) were related to early life trauma exposure. Of note, CM‐related reduced FC between the IPL and dorsolateral PFC during sustained attention was moderated by SNP rs3800373 (Hart et al, 2017).…”

Section: Discussionmentioning

confidence: 89%

“…Previous studies have found reduced FCs of the IPL with visual regions (Philip, Kuras, et al, 2013) and ACC (Eckstrand et al, 2019) were related to early life trauma exposure. Of note, CM-related reduced FC between the IPL and dorsolateral PFC during sustained attention was moderated by SNP rs3800373 (Hart et al, 2017).…”

Section: Altered Tom Connectome Related With CMmentioning

confidence: 81%

“…CM, childhood maltreatment; L, left; MVPA, multivoxel pattern analysis; IPL, inferior parietal lobule; PI, posterior insula; R, right CM was related to altered cortical thickness and gray matter volume in the PFC, ACC, STG, insula, IPL, and occipital regions (Lim et al, 2014;Tozzi et al, 2020). Maltreatment participants showed increased activation in the IPL and occipital cortex during inhibitory control (Bruce et al, 2013), increased STG and insula activation during emotional stimuli (Blair et al, 2019;McCrory et al, 2011), and increased ACC activation during reward prediction error (Eckstrand et al, 2019). In addition, CM was also linked to decreased regional homogeneity and fractional amplitude of low frequency fluctuation in the IPL and STG Lu, Pan, et al, 2017;Philip, Kuras, et al, 2013).…”

Section: Altered Tom Connectome Related With CMmentioning

confidence: 99%

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Enduring effect of abuse: Childhood maltreatment links to altered theory of mind network among adults

Pang

Zhao

et al. 2022

Human Brain Mapping

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Childhood maltreatment (CM) confers a great risk of maladaptive development outcomes later in life, however, the neurobiological mechanism underlying this vulnerability is still unclear. The present study aimed to investigate the long-term consequences of CM on neural connectivity while controlling for psychiatric conditions, medication, and, substance abuse. A sample including adults with (n = 40) and without CM (n = 50) completed Childhood Trauma Questionnaire (CTQ), personality questionnaires, and resting-state functional magnetic resonance imaging scan were recruited for the current study. The whole-brain functional connectivity (FC) was evaluated using an unbiased, data-driven, multivariate pattern analysis method. Relative to controls, adults with CM suffered a higher level of temperament and impulsivity and showed decreased FC between the insula and superior temporal gyrus (STG) and between inferior parietal lobule (IPL) and middle frontal gyrus, STG, and dorsal anterior cingulate cortex (dACC), while increased FC between IPL and cuneus and superior frontal gyrus (SFG) regions. The FCs of IPL with dACC and SFG were correlated with the anxious and cyclothymic temperament and attentional impulsivity.Moreover, these FCs partially mediated the relationship between CM and attentional impulsivity. Our results suggest that CM has a significant effect on the modulation of FC within theory of mind (ToM) network even decades later in adulthood, and inform

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Trauma-associated anterior cingulate connectivity during reward learning predicts affective and anxiety states in young adults

Cited by 18 publications

References 70 publications

Dissociation between Cerebellar and Cerebral Neural Activities in Humans with Long-Term Bilateral Sensorineural Hearing Loss

Dissociation between Cerebellar and Cerebral Neural Activities in Humans with Long-Term Bilateral Sensorineural Hearing Loss

Investigation of functional brain network reconfiguration during vocal emotional processing using graph-theoretical analysis

Enduring effect of abuse: Childhood maltreatment links to altered theory of mind network among adults

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