The Decline in Intrinsic Connectivity Between the Salience Network and Locus Coeruleus in Older Adults: Implications for Distractibility.

Benjamin Katz,Sun Hyung Kim,Tae-Ho Lee,Mara Mather

doi:10.3389/fnagi.2020.00002

Abstract

We examined functional connectivity between the locus coeruleus (LC) and the salience network in healthy young and older adults to investigate why people become more prone to distraction with age. Recent findings suggest that the LC plays an important role in focusing processing on salient or goal-relevant information from multiple incoming sensory inputs (Mather et al., 2016). We hypothesized that the connection between LC and the salience network declines in older adults, and therefore the salience network fails to appropriately filter out irrelevant sensory signals. To examine this possibility, we used resting-state-like fMRI data, in which all task-related activities were regressed out (Fair et al., 2007; Elliott et al., 2019) and performed a functional connectivity analysis based on the time-course of LC activity. Older adults showed reduced functional connectivity between the LC and salience network compared with younger adults. Additionally, the salience network was relatively more coupled with the frontoparietal network than the default-mode network in older adults compared with younger adults, even though all task-related activities were regressed out. Together, these findings suggest that reduced interactions between LC and the salience network impairs the ability to prioritize the importance of incoming events, and in turn, the salience network fails to initiate network switching (e.g., Menon and Uddin, 2010; Uddin, 2015) that would promote further attentional processing. A chronic lack of functional connection between LC and salience network may limit older adults’ attentional and executive control resources.

Highlights

Studies have suggested that attentional control deficits in older adults are due to age-related changes of the frontal system, the frontoparietal network, composed of the dorsolateral prefrontal cortex (DLPFC), middle frontal gyrus (MFG), inferior frontal gyrus (IFG), and anterior/inferior parietal lobule (Gazzaley et al, 2005; Campbell et al, 2012; Kennedy and Mather, in press), such that older adults typically show reduced activation in the frontoparietal
Neuroimaging research suggests that the default mode network, including the medial PFC (MPFC), posterior cingulate cortex (PCC), and precuneus, the salience network, which includes the anterior cingulate cortex and anterior insula, and the frontoparietal network each are involved in implementing attentional processes in the brain, and that they interact with each other
These regions are considered to be the core of the salience network (Menon and Uddin, 2010; Uddin, 2015). To confirm that these regions showed reduced functional connectivity in older adults (OA) constitute the salience network, additional spatial crosscorrelation analysis with the previously defined salience network template was performed and it showed a high degree of similarity (r > 0.358). This result indicates that the locus coeruleus (LC) is connected to the salience network more strongly in younger adults (YA) than OA, suggesting that the salience network activity is coupled strongly with LC activity in YA but not in OA (Figure 1A; Table 1A)

Summary

Introduction

Studies have suggested that attentional control deficits in older adults are due to age-related changes of the frontal system, the frontoparietal network, composed of the dorsolateral prefrontal cortex (DLPFC), middle frontal gyrus (MFG), inferior frontal gyrus (IFG), and anterior/inferior parietal lobule (Gazzaley et al, 2005; Campbell et al, 2012; Kennedy and Mather, in press), such that older adults typically show reduced activation in the frontoparietalLocus Coeruleus and Salience Network network compared with younger adults (Ferreira and Busatto, 2013; Geerligs et al, 2014; Grady et al, 2016). From a theoretical perspective, when the salience network does not filter out incoming sensory inputs appropriately and continues to activate the frontoparietal network for every sensory signal, it may lead to unnecessary depletion of limited neural resources and impairment of focused, goal-directed attentional processes. Consistent with this possibility, deficits in the salience network (e.g., decreased neural activation and connectivity between local regions within the network) are associated with attention deficits in both younger and aging adults (Lopez-Larson et al, 2012; Song et al, 2014; Cai et al, 2015; Zhao et al, 2017)

Methods

Results

Conclusion