Abstract
Aging affects pain experience and brain functioning. However, how aging leads to changes in pain perception and brain functional connectivity has not yet been completely understood. To investigate resting-state and pain perception changes in old and young participants, this study employed region of interest (ROI) to ROI resting-state functional connectivity (rsFC) analysis of imaging data by using regions implicated in sensory and affective dimensions of pain, descending pain modulation, and the default-mode networks (DMNs). Thirty-seven older (66.86 ± 4.04 years; 16 males) and 38 younger healthy participants (20.74 ± 4.15 years; 19 males) underwent 10 min’ eyes-closed resting-state scanning. We examined the relationship between rsFC parameters with pressure pain thresholds. Older participants showed higher pain thresholds than younger. Regarding rsFC, older adults displayed increased connectivity of pain-related sensory brain regions in comparison to younger participants: increased rsFC between bilateral primary somatosensory area (SI) and anterior cingulate cortex (ACC), and between SI(L) and secondary somatosensory area (SII)-(R) and dorsolateral prefrontal cortex (PFC). Moreover, decreased connectivity in the older compared to the younger group was found among descending pain modulatory regions: between the amygdala(R) and bilateral insula(R), thalamus(R), ACC, and amygdala(L); between the amygdala(L) and insula(R) and bilateral thalamus; between ACC and bilateral insula, and between periaqueductal gray (PAG) and bilateral thalamus. Regarding the DMN, the posterior parietal cortex and lateral parietal (LP; R) were more strongly connected in the older group than in the younger group. Correlational analyses also showed that SI(L)-SII(R) rsFC was positively associated with pressure pain thresholds in older participants. In conclusion, these findings suggest a compensatory mechanism for the sensory changes that typically accompanies aging. Furthermore, older participants showed reduced functional connectivity between key nodes of the descending pain inhibitory pathway.
Highlights
Pain in older adults is poorly understood
It has been shown that brain areas such as the prefrontal cortex (PFC), amygdala (AMY) and insula (INS) undergo a significant reorganization of resting-state functional connectivity with aging (He et al, 2017; Xiao et al, 2018)
These brain regions play a key role in acute pain processing and several studies have shown a strong relationship between resting-state functional connectivity (rsFC) of INS, AMY and anterior cingulate cortex (ACC) with pain perception (Boly et al, 2007; Proverbio et al, 2009; Ploner et al, 2010), empathy for pain (Vaidya and Gordon, 2013) and psychologically induced stress
Summary
Pain in older adults is poorly understood. Aging seems to be associated with increased pain thresholds and poor functioning of endogenous pain inhibition mechanisms (Lautenbacher, 2012; Lautenbacher et al, 2017). Age-related changes in the spontaneous organization of the brain have been linked to the cognitive, perceptual and motor alterations that frequently accompany aging (Ferreira and Busatto, 2013; Madden et al, 2017; King et al, 2018; SolesioJofre et al, 2018) In this sense, previous studies have found that older participants displayed enlarged cortical representations of the body and enhanced cortical excitability of primary somatosensory cortex (SI), leading to reduced tactile perception (Shaffer and Harrison, 2007; Kalisch et al, 2009; Lenz et al, 2012; Catley et al, 2014). It has been shown that brain areas such as the prefrontal cortex (PFC), amygdala (AMY) and insula (INS) undergo a significant reorganization of resting-state functional connectivity (rsFC) with aging (He et al, 2017; Xiao et al, 2018). Most of the literature on rsFC and pain is from younger participants, and no studies have examined rsFC and pain in healthy older adults
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