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Disrupted insula-based neural circuit organization and conflict interference in trauma-exposed youth.

Marusak HA, Etkin A, Thomason ME - Neuroimage Clin (2015)

Bottom Line: We find that trauma-exposed youth are more susceptible to conflict interference and this correlates with higher fronto-insular responses during conflict.Resting-state functional connectivity data collected in the same participants reveal increased connectivity of the insula to SN seed regions that is associated with diminished reward sensitivity, a critical risk/resilience trait following stress.In addition to altered intrinsic connectivity of the SN, we observed altered connectivity between the SN and default mode network (DMN) in trauma-exposed youth.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, USA ; Merrill Palmer Skillman Institute for Child and Family Development, Wayne State University, Detroit, MI, USA.

ABSTRACT
Childhood trauma exposure is a potent risk factor for psychopathology. Emerging research suggests that aberrant saliency processing underlies the link between early trauma exposure and later cognitive and socioemotional deficits that are hallmark of several psychiatric disorders. Here, we examine brain and behavioral responses during a face categorization conflict task, and relate these to intrinsic connectivity of the salience network (SN). The results demonstrate a unique pattern of SN dysfunction in youth exposed to trauma (n = 14) relative to comparison youth (n = 19) matched on age, sex, IQ, and sociodemographic risk. We find that trauma-exposed youth are more susceptible to conflict interference and this correlates with higher fronto-insular responses during conflict. Resting-state functional connectivity data collected in the same participants reveal increased connectivity of the insula to SN seed regions that is associated with diminished reward sensitivity, a critical risk/resilience trait following stress. In addition to altered intrinsic connectivity of the SN, we observed altered connectivity between the SN and default mode network (DMN) in trauma-exposed youth. These data uncover network-level disruptions in brain organization following one of the strongest predictors of illness, early life trauma, and demonstrate the relevance of observed neural effects for behavior and specific symptom dimensions. SN dysfunction may serve as a diathesis that contributes to illness and negative outcomes following childhood trauma.

No MeSH data available.


Related in: MedlinePlus

Schematic representation of (A) salience network (SN) organization and (B) model of SN dysfunction in youth exposed to trauma. (A) The normal function of the SN is to detect relevant internal and external cues among myriad inputs. Ventral sensory pathways, including the amygdala and mid-posterior insular regions, feed forward stimulus information to core SN regions (i.e., right fronto-insular cortex (rFIC) and dorsal anterior cingulate cortex (dACC)). Engaged rFIC may influence dominance in other neurocognitive systems that are relevant for goal-directed cognitive processes (e.g., conflict regulation). This is consistent with suggestions that the FIC is an integrative hub that filters how sensory inputs are further processed (Menon and Uddin, 2010). (B) The present results demonstrate that childhood trauma, a major predisposing factor for psychopathology, is associated with altered function and connectivity of the SN. Fitting with conceptual models of posttraumatic stress disorder (Patel et al., 2012) and major depressive disorder (Hamilton et al., 2012), changes within the SN may lead to a cascade of events that increase risk for cognitive and affective dysfunction hallmark of these disorders. Our results suggest that altered salience processing may underlie the link between early life trauma and development of psychopathology. Specifically, we observed greater performance decrements to conflict trials, which corresponded with increased fronto-insular responses in trauma-exposed youth. We also observed altered connectivity within the SN, and between the SN and the default mode network (DMN). Network-level disruptions may underlie the observed sub-optimal brain and behavioral responses during the conflict task in trauma-exposed youth. Finally, strength of SN connectivity within the insula was associated with reduced reward sensitivity, an affective trait emerging as an important risk/resilience factor in the aftermath of early trauma exposure.
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f0030: Schematic representation of (A) salience network (SN) organization and (B) model of SN dysfunction in youth exposed to trauma. (A) The normal function of the SN is to detect relevant internal and external cues among myriad inputs. Ventral sensory pathways, including the amygdala and mid-posterior insular regions, feed forward stimulus information to core SN regions (i.e., right fronto-insular cortex (rFIC) and dorsal anterior cingulate cortex (dACC)). Engaged rFIC may influence dominance in other neurocognitive systems that are relevant for goal-directed cognitive processes (e.g., conflict regulation). This is consistent with suggestions that the FIC is an integrative hub that filters how sensory inputs are further processed (Menon and Uddin, 2010). (B) The present results demonstrate that childhood trauma, a major predisposing factor for psychopathology, is associated with altered function and connectivity of the SN. Fitting with conceptual models of posttraumatic stress disorder (Patel et al., 2012) and major depressive disorder (Hamilton et al., 2012), changes within the SN may lead to a cascade of events that increase risk for cognitive and affective dysfunction hallmark of these disorders. Our results suggest that altered salience processing may underlie the link between early life trauma and development of psychopathology. Specifically, we observed greater performance decrements to conflict trials, which corresponded with increased fronto-insular responses in trauma-exposed youth. We also observed altered connectivity within the SN, and between the SN and the default mode network (DMN). Network-level disruptions may underlie the observed sub-optimal brain and behavioral responses during the conflict task in trauma-exposed youth. Finally, strength of SN connectivity within the insula was associated with reduced reward sensitivity, an affective trait emerging as an important risk/resilience factor in the aftermath of early trauma exposure.

Mentions: Contemporary neurobiological models suggest that inappropriate assignment of saliency to external stimuli or internal mental events leads to aberrant interactions within and between large-scale neurocognitive networks, and plays a significant role in several psychiatric disorders (Menon, 2011). Recent research in adults supports this conceptualization (e.g., Manoliu et al., 2013; Sripada et al., 2012). However, it is unknown if changes are evident in the brain prior to the emergence of clinically significant symptoms; these may underlie vulnerability. The present study is the first to link early life trauma exposure — a major predisposing factor for the development of psychopathology — to dysfunctional architecture of large-scale neurocognitive networks in a sample of high-risk urban youth. We demonstrate increased SN connectivity within the insula in trauma-exposed youth that has cognitive repercussions: increased SN connectivity corresponds with suboptimal brain and behavioral responses during a conflict task. Further, we demonstrate that altered SN connectivity is associated with individual variation in positive valence systems. That is, higher SN connectivity within the insula was associated with lower RS. These results suggest that enhanced salience detection, diminished sensitivity to reward, and connectome-level brain changes may contribute to later cognitive and affective deficits observed in individuals who have experienced trauma. A schematic representation of the overarching framework is provided in Fig. 6.


Disrupted insula-based neural circuit organization and conflict interference in trauma-exposed youth.

Marusak HA, Etkin A, Thomason ME - Neuroimage Clin (2015)

Schematic representation of (A) salience network (SN) organization and (B) model of SN dysfunction in youth exposed to trauma. (A) The normal function of the SN is to detect relevant internal and external cues among myriad inputs. Ventral sensory pathways, including the amygdala and mid-posterior insular regions, feed forward stimulus information to core SN regions (i.e., right fronto-insular cortex (rFIC) and dorsal anterior cingulate cortex (dACC)). Engaged rFIC may influence dominance in other neurocognitive systems that are relevant for goal-directed cognitive processes (e.g., conflict regulation). This is consistent with suggestions that the FIC is an integrative hub that filters how sensory inputs are further processed (Menon and Uddin, 2010). (B) The present results demonstrate that childhood trauma, a major predisposing factor for psychopathology, is associated with altered function and connectivity of the SN. Fitting with conceptual models of posttraumatic stress disorder (Patel et al., 2012) and major depressive disorder (Hamilton et al., 2012), changes within the SN may lead to a cascade of events that increase risk for cognitive and affective dysfunction hallmark of these disorders. Our results suggest that altered salience processing may underlie the link between early life trauma and development of psychopathology. Specifically, we observed greater performance decrements to conflict trials, which corresponded with increased fronto-insular responses in trauma-exposed youth. We also observed altered connectivity within the SN, and between the SN and the default mode network (DMN). Network-level disruptions may underlie the observed sub-optimal brain and behavioral responses during the conflict task in trauma-exposed youth. Finally, strength of SN connectivity within the insula was associated with reduced reward sensitivity, an affective trait emerging as an important risk/resilience factor in the aftermath of early trauma exposure.
© Copyright Policy - CC BY-NC-ND
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4477108&req=5

f0030: Schematic representation of (A) salience network (SN) organization and (B) model of SN dysfunction in youth exposed to trauma. (A) The normal function of the SN is to detect relevant internal and external cues among myriad inputs. Ventral sensory pathways, including the amygdala and mid-posterior insular regions, feed forward stimulus information to core SN regions (i.e., right fronto-insular cortex (rFIC) and dorsal anterior cingulate cortex (dACC)). Engaged rFIC may influence dominance in other neurocognitive systems that are relevant for goal-directed cognitive processes (e.g., conflict regulation). This is consistent with suggestions that the FIC is an integrative hub that filters how sensory inputs are further processed (Menon and Uddin, 2010). (B) The present results demonstrate that childhood trauma, a major predisposing factor for psychopathology, is associated with altered function and connectivity of the SN. Fitting with conceptual models of posttraumatic stress disorder (Patel et al., 2012) and major depressive disorder (Hamilton et al., 2012), changes within the SN may lead to a cascade of events that increase risk for cognitive and affective dysfunction hallmark of these disorders. Our results suggest that altered salience processing may underlie the link between early life trauma and development of psychopathology. Specifically, we observed greater performance decrements to conflict trials, which corresponded with increased fronto-insular responses in trauma-exposed youth. We also observed altered connectivity within the SN, and between the SN and the default mode network (DMN). Network-level disruptions may underlie the observed sub-optimal brain and behavioral responses during the conflict task in trauma-exposed youth. Finally, strength of SN connectivity within the insula was associated with reduced reward sensitivity, an affective trait emerging as an important risk/resilience factor in the aftermath of early trauma exposure.
Mentions: Contemporary neurobiological models suggest that inappropriate assignment of saliency to external stimuli or internal mental events leads to aberrant interactions within and between large-scale neurocognitive networks, and plays a significant role in several psychiatric disorders (Menon, 2011). Recent research in adults supports this conceptualization (e.g., Manoliu et al., 2013; Sripada et al., 2012). However, it is unknown if changes are evident in the brain prior to the emergence of clinically significant symptoms; these may underlie vulnerability. The present study is the first to link early life trauma exposure — a major predisposing factor for the development of psychopathology — to dysfunctional architecture of large-scale neurocognitive networks in a sample of high-risk urban youth. We demonstrate increased SN connectivity within the insula in trauma-exposed youth that has cognitive repercussions: increased SN connectivity corresponds with suboptimal brain and behavioral responses during a conflict task. Further, we demonstrate that altered SN connectivity is associated with individual variation in positive valence systems. That is, higher SN connectivity within the insula was associated with lower RS. These results suggest that enhanced salience detection, diminished sensitivity to reward, and connectome-level brain changes may contribute to later cognitive and affective deficits observed in individuals who have experienced trauma. A schematic representation of the overarching framework is provided in Fig. 6.

Bottom Line: We find that trauma-exposed youth are more susceptible to conflict interference and this correlates with higher fronto-insular responses during conflict.Resting-state functional connectivity data collected in the same participants reveal increased connectivity of the insula to SN seed regions that is associated with diminished reward sensitivity, a critical risk/resilience trait following stress.In addition to altered intrinsic connectivity of the SN, we observed altered connectivity between the SN and default mode network (DMN) in trauma-exposed youth.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, USA ; Merrill Palmer Skillman Institute for Child and Family Development, Wayne State University, Detroit, MI, USA.

ABSTRACT
Childhood trauma exposure is a potent risk factor for psychopathology. Emerging research suggests that aberrant saliency processing underlies the link between early trauma exposure and later cognitive and socioemotional deficits that are hallmark of several psychiatric disorders. Here, we examine brain and behavioral responses during a face categorization conflict task, and relate these to intrinsic connectivity of the salience network (SN). The results demonstrate a unique pattern of SN dysfunction in youth exposed to trauma (n = 14) relative to comparison youth (n = 19) matched on age, sex, IQ, and sociodemographic risk. We find that trauma-exposed youth are more susceptible to conflict interference and this correlates with higher fronto-insular responses during conflict. Resting-state functional connectivity data collected in the same participants reveal increased connectivity of the insula to SN seed regions that is associated with diminished reward sensitivity, a critical risk/resilience trait following stress. In addition to altered intrinsic connectivity of the SN, we observed altered connectivity between the SN and default mode network (DMN) in trauma-exposed youth. These data uncover network-level disruptions in brain organization following one of the strongest predictors of illness, early life trauma, and demonstrate the relevance of observed neural effects for behavior and specific symptom dimensions. SN dysfunction may serve as a diathesis that contributes to illness and negative outcomes following childhood trauma.

No MeSH data available.


Related in: MedlinePlus