Salience network integrity predicts default mode network function after traumatic brain injury

Abstract

Efficient behavior involves the coordinated activity of large-scale brain networks, but the way in which these networks interact is uncertain. One theory is that the salience network (SN)-which includes the anterior cingulate cortex, presupplementary motor area, and anterior insulae-regulates dynamic changes in other networks. If this is the case, then damage to the structural connectivity of the SN should disrupt the regulation of associated networks. To investigate this hypothesis, we studied a group of 57 patients with cognitive impairments following traumatic brain injury (TBI) and 25 control subjects using the stop-signal task. The pattern of brain activity associated with stop-signal task performance was studied by using functional MRI, and the structural integrity of network connections was quantified by using diffusion tensor imaging. Efficient inhibitory control was associated with rapid deactivation within parts of the default mode network (DMN), including the precuneus and posterior cingulate cortex. TBI patients showed a failure of DMN deactivation, which was associated with an impairment of inhibitory control. TBI frequently results in traumatic axonal injury, which can disconnect brain networks by damaging white matter tracts. The abnormality of DMN function was specifically predicted by the amount of white matter damage in the SN tract connecting the right anterior insulae to the presupplementary motor area and dorsal anterior cingulate cortex. The results provide evidence that structural integrity of the SN is necessary for the efficient regulation of activity in the DMN, and that a failure of this regulation leads to inefficient cognitive control. E fficient behavior involves the coordinated activity of largescale brain networks (1, 2). These networks can be identified by studying patterns of brain activity measured by functional MRI (fMRI) (3). A key question is whether-and in what waythe interactions between these networks control behavior. Regions on the medial wall of the frontal lobe, including the anterior cingulate cortex (ACC) and presupplementary motor area (preSMA), often show highly correlated brain activity with the anterior insula (AI) (4-6), and together they have been termed the salience network (SN) (4). In many situations, activity within this network appears to signal the need for behavioral change (7-9), and one proposal is that the SN may operate to dynamically control changes of activity in other networks (6).The role of the SN in mediating the function of other networks is likely to be most evident when a rapid change in behavior is required. We have previously studied this type of behavior in the context of motor control using the stop-signal task (SST) (10). The SST probes the ability to inhibit an action that has already been initiated. Stop trials require a switch from relatively automatic to highly controlled behavior. Parts of the right inferior frontal cortex, including the right AI (rAI), are important for the attentional processes involved in responding to an unexp...

Serum insulin‐like growth factor‐I levels are associated with improved white matter recovery after traumatic brain injury

“…We have previously shown that after TBI, FA measurements in particular WM tracts relate to multiple neuropsychological domains 10, 11, 46. In a separate cross‐sectional cohort of patients after moderate–severe TBI and controls who were scanned once, we confirmed both lower SPCC FA and lower immediate verbal memory recall in patients after TBI compared to controls.…”

Significant Improvements in Cognitive Performance Post-Transcranial, Red/Near-Infrared Light-Emitting Diode Treatments in Chronic, Mild Traumatic Brain Injury: Open-Protocol Study

“…Variability in performance on Stroop inhibition switching was also recently observed among a large number of TBI cases who were studied with resting state functional connectivity MRI (rs-fMRI), task-oriented functional MRI (fMRI) and diffusion tensor imaging (DTI). 53 In that study, 20/46, (43%) performed poorly on the stop signal reaction time (SSRT) task, with slower response inhibition (higher SSRT). These cases with slower reaction times in the NoGo condition were observed to have failure deactivating the DMN, particularly the precuneus/posterior cingulate cortex (precu/PCC) portion.…”

“…The LED placement loci included, in part, a proposed paradigm to target nodes within the default mode network (DMN) and the salience network (SN), areas where functional connectivity MRI studies have reported abnormalities in TBI. 53 The LED placement loci also included dorsolateral prefrontal cortex (DLPFC), part of the central executive network (CEN). 54 Supplementary Figure 1 (see online supplementary material at http://www.liebertonline.com) shows the location of extracranial bone and suture landmarks on the skull, in relationship to approximate surface brain cortex areas.…”

Chronology and Chronicity of Altered Resting-State Functional Connectivity after Traumatic Brain Injury

“…Color image is available online at www.liebertpub.com/neu implicated extensively in a network important for selecting salient stimuli and guiding behavior in coordination with multiple other brain systems, [68][69][70] and the structural integrity of this network has been found to be crucial for DMN functioning in severe TBI. 71 Given that concurrent modulations of the DMN and task-positive regions have been found to support task performance in healthy individuals, [72][73][74][75] an increase in antiphase synchrony during the clinical recovery period may signify a restoration of balanced network function necessary for efficient cognitive processing. In keeping with the view of the DMN and TPN as reciprocal networks, co-occurring internetwork (PCC-TPN) antiphase synchrony and residual intranetwork (PCC-DMN) synchrony may be two parts of a larger effect involving the modulation and optimal balancing of distributed networks.…”