Influence of age and cognitive performance on resting-state brain networks of older adults in a population-based cohort

Jockwitz, Christiane; Caspers, Svenja; Lux, Silke; Eickhoff, Simon B.; Jütten, Kerstin; Lenzen, S.; Moebus, Susanne; Pundt, Noreen; Reid, Andrew; Hoffstaedter, Felix; Jöckel, Karl‐Heinz; Erbel, Raimund; Cichon, Sven; Nöthen, Markus M.; Shah, N. Jon; Zilles, Karl; Amunts, Katrin

doi:10.1016/j.cortex.2017.01.008

Cited by 56 publications

(47 citation statements)

References 104 publications

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“…Taken together, the results of the present study complement a previous resting-state fMRI study reporting age-related increases in iFC in the right fronto-parietal network 49 .…”

Section: Discussionsupporting

confidence: 89%

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Right-lateralized fronto-parietal network and phasic alertness in healthy aging

Haupt

Ruiz‐Rizzo

Sorg

et al. 2019

Preprint

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Phasic alerting cues temporarily increase the brain's arousal state. In younger and older participants, visual processing speed in a whole report task, estimated based on the theory of visual attention (TVA), is increased in cue compared to no-cue conditions. The present study assessed whether older participants' ability to profit from warning cues is related to iFC in the cingulo-opercular and/or right fronto-parietal network. We obtained resting-state functional magnetic resonance imaging (rs-fMRI) data from 31 older participants. By combining an independent component analysis and dual regression, we investigated iFC in both networks. A voxel-wise multiple regression in older participants revealed that higher phasic alerting effects on visual processing speed were significantly associated with lower right fronto-parietal network iFC. We then compared healthy older participants to a previously reported sample of healthy younger participants to assess whether behaviour-iFC relationships are age group specific. The comparison revealed that the association between phasic alerting and cingulo-opercular network iFC is significantly lower in older than in younger adults. Additionally, it yielded a stronger association between phasic alerting and right fronto-parietal network iFC in older versus younger participants. The results support a particular role of the right fronto-parietal network in maintaining phasic alerting capabilities in aging.3 IntroductionWarning cues induce short-lived changes in the brain's "state of readiness" defined as phasic alertness 1 . In verbal whole report paradigms of briefly presented letter arrays combined with modelling based on the computational Theory of Visual Attention (TVA), previous studies demonstrated that visual 2 and auditory warning cues 3 increase visual processing speed. Furthermore, we demonstrated that auditory alerting was effective in both healthy younger and older participants 4 .Concerning neural correlates, in younger adults, we found that the individual phasic alerting effect on visual processing speed was related to intrinsic functional connectivity (iFC) in the cingulo-opercular network 5 . IFC was measured in a separate resting-state fMRI session, which allowed to measure ongoing fluctuations of the blood oxygen level dependent (BOLD) signal with a frequency around 0.01-0.1Hz 6 . Spatial patterns of coherent, i.e. correlated, BOLD fluctuations over time (iFC) constitute intrinsic brain networks which are stable on an intra-7 and inter-subject 8,9 level. The cingulo-opercular network (CON) is also referred to as "salience network" 10 or "ventral attention network" 11 . It comprises the anterior prefrontal cortex, anterior insula, frontal operculum, dorsal anterior cingulate cortex, medial superior frontal cortex, and thalamus 12 .With respect to older adults, it is unclear whether their preserved enhancement of visual processing speed following alertness cues relies on the same or a different intrinsic brain network. In a comprehensive review on the role of the...

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“…Taken together, the results of the present study complement a previous resting-state fMRI study reporting age-related increases in iFC in the right fronto-parietal network 49 .…”

Section: Discussionsupporting

confidence: 89%

Section: Discussionmentioning

confidence: 92%

Right-lateralized fronto-parietal network and phasic alertness in healthy aging

Haupt

Ruiz‐Rizzo

Sorg

et al. 2019

Preprint

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“…Importantly, greater connectivity does not automatically imply better behavioural performance. Previous studies have demonstrated that lower behavioural scores were associated with higher iFC in the brain networks of interest 16,17 . Based on such evidence, Ferreira and Busatto 18 summarised that the assumption "the more, the better" is overly simplistic and might be misleading in the interpretation of findings.…”

Section: Discussionmentioning

confidence: 92%

Right-lateralized fronto-parietal network and phasic alertness in healthy aging

Haupt

Ruiz‐Rizzo

Sorg

et al. 2020

Sci Rep

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Phasic alerting cues temporarily increase the brain's arousal state. In younger and older participants, visual processing speed in a whole report task, estimated based on the theory of visual attention, is higher in cue than no-cue conditions. The present study assessed whether older participants' ability to profit from warning cues is related to intrinsic functional connectivity (iFC) in the cingulo-opercular and/ or right fronto-parietal network. We acquired resting-state functional magnetic resonance imaging data from 31 older participants. By combining an independent component analysis and dual regression, we investigated iFC in both networks. A voxel-wise multiple regression in older participants yielded that higher phasic alerting effects on visual processing speed were significantly related to lower right fronto-parietal network iFC. This result supports a particular role of the right fronto-parietal network in maintaining phasic alerting capabilities in aging. We then compared healthy older participants to a previously reported sample of healthy younger participants to assess whether behaviour-ifc relationships are age group specific. The comparison revealed that the association between phasic alerting and cingulo-opercular network iFC is significantly lower in older than in younger adults.Phasic alertness refers to momentary enhancements of the brain's "state of readiness" due to warning cues 1 . Previous studies, using a whole report task with briefly presented letter arrays and parametric modelling of report performance based on the theory of visual attention (TVA) 2 , demonstrated that perceptual speed of visual processing is enhanced by visual 3 and auditory warning cues 4 . Furthermore, auditory alerting was shown to be effective in both healthy younger and older participants 5 . Concerning neural correlates underlying phasic alerting effects in younger adults, we found that the individual cueing benefits were significantly related to intrinsic functional connectivity (iFC) in the cingulo-opercular network (CON) 6 . IFC refers to spatial patterns of correlated blood oxygen level dependent (BOLD) signal with a frequency of 0.01-0.1 Hz over time 7 . These BOLD fluctuations can be measured using resting-state functional magnetic resonance imaging (rs-fMRI).With respect to older adults, it is unclear whether their preserved phasic alertness response relies on the same intrinsic brain network as in younger adults or a different one. Reviewing the importance of right-hemispheric structures for cognitive reserve 8 , Robertson suggested that the integrity and functional connectivity of the right fronto-parietal network (rFPN) is decisive for the late-life maintenance of attentional abilities and, especially, alertness functions 9,10 . He summarized evidence for a close, bidirectional relationship of the availability of noradrenaline provided by the locus coeruleus, which is decisive for the ability to increase arousal 11,12 , and the integrity of the right fronto-parietal network in aging individuals. The m...

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“…For example, patients with T2D exhibit reduced activity in the default mode network (Musen et al, 2012), which has been associated with a wide range of neurological conditions and cognitive impairments (Browndyke et al, 2017; Contreras et al, 2017; Jockwitz et al, 2017; von Rhein et al, 2017) but BMI, which was higher in T2D, was not accounted for. Similarly, the putative confound of glucose intolerance is often not considered when examining the relationship between obesity and cognition.…”

Section: It Is Unknown If Neurocognitive Deficits Are Associated Withmentioning

confidence: 99%

Dopamine Adaptations as a Common Pathway for Neurocognitive Impairment in Diabetes and Obesity: A Neuropsychological Perspective

Small

2017

Front. Neurosci.

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Evidence accumulates linking obesity and diabetes with cognitive dysfunction. At present the mechanism(s) underlying these associations and the relative contribution of diet, adiposity, and metabolic dysfunction are unknown. In this perspective key gaps in knowledge are outlined and an initial sketch of a neuropsychological profile is developed that points toward a critical role for dopamine (DA) adaptations in neurocognitive impairment secondary to diabetes and obesity. The precise mechanisms by which diet, metabolic dysfunction, and adiposity influence the DA system to impact cognition remains unclear and is an important direction for future research.

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Influence of age and cognitive performance on resting-state brain networks of older adults in a population-based cohort

Cited by 56 publications

References 104 publications

Right-lateralized fronto-parietal network and phasic alertness in healthy aging

Right-lateralized fronto-parietal network and phasic alertness in healthy aging

Right-lateralized fronto-parietal network and phasic alertness in healthy aging

Dopamine Adaptations as a Common Pathway for Neurocognitive Impairment in Diabetes and Obesity: A Neuropsychological Perspective

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