Strength of Structural and Functional Frontostriatal Connectivity Predicts Self-Control in the Healthy Elderly

Abstract

Self-regulation refers to the successful use of executive functions and initiation of top-down processes to control one's thoughts, behavior, and emotions, and it is crucial to perform self-control. Self-control is needed to overcome impulses and can be assessed by delay of gratification (DoG) and delay discounting (DD) paradigms. In children/adolescents, good DoG/DD ability depends on the maturity of frontostriatal connectivity, and its decline in strength with advancing age might adversely affect self-control because prefrontal brain regions are more prone to normal age-related atrophy than other regions. Here, we aimed at highlighting the relationship between frontostriatal connectivity strength and DoG performance in advanced age. We recruited 40 healthy elderly individuals (mean age 74.0 ± 7.7 years) and assessed the DoG ability using the German version of the DoG test for adults in addition to the delay discounting (DD) paradigm. Based on diffusion-weighted and resting-state functional magnetic resonance imaging data, respectively, the structural and functional whole-brain connectome were reconstructed based on 90 different brain regions of interest in addition to a 12-node frontostriatal DoG-specific network and the resulting connectivity matrices were subjected to network-based statistics. The 90-nodes whole-brain connectome analyses revealed subnetworks significantly associated with DoG and DD with a preponderance of frontostriatal nodes involved suggesting a high specificity of the findings. Structural and functional connectivity strengths between the putamen, caudate nucleus, and nucleus accumbens on the one hand and orbitofrontal, dorsal, and ventral lateral prefrontal cortices on the other hand showed strong positive correlations with DoG and negative correlations with DD corrected for age, sex, intracranial volume, and head motion parameters. These associations cannot be explained by differences in impulsivity and executive functioning. This pattern of correlations between structural or functional frontostriatal connectivity strength and self-control suggests that, in addition to the importance of the frontostriatal nodes itself, the structural and functional properties of different connections within the frontostriatal network are crucial for self-controlled behaviors in the healthy elderly. Because high DoG/low DD is a significant predictor of willpower and wellbeing in the elderly population, interventions aiming at strengthening frontostriatal connectivity to strengthen self-controlled behavior are needed in the future.

White matter correlates of temporal discounting in older adults

“…One German-based study investigated functional and structural connectivity associations with a delay of gratification and a delay discounting paradigm in 40 healthy older adults (mean age = 74) using predefined 90-node and 12-node brain region networks (Hanggi et al 2016). Functional and structural connections between nodes located in the frontostriatal regions were implicated after controlling for age, sex, intracranial volume, and head motion.…”

“…We additionally examined whether results remained significant after further adjusting for cognitive function. One prior study investigated temporal discounting associations with DTI measures using a set of predefined regions of interest in 40 healthy older adults (Hanggi et al 2016). We investigated this using a voxelwise whole-brain approach in more than 300 older adults without dementia from the Rush Memory and Aging Project, a longitudinal clinicopathologic study of aging.…”

The role of the dorsal striatum in choice impulsivity

“…Importantly, the caudate activity was linked to reward valuation in the delay‐discounting task, which may correspond to the outcome evaluation function of the caudate . Interestingly, any abnormalities in the caudate with regard to task‐related activation or resting‐state functional connectivity (most commonly between the caudate and the ventral PFC) were coupled to higher choice impulsivity . In sum, the caudate may be crucial for the cognitive control of choice impulsivity, presumably via activity‐dependent reward valuation processing (Fig.…”

“…Interestingly, Hampton and colleagues reported that the structural connectivity from the dorsal striatum to the dlPFC was positively associated with discounting propensity, which seems to oppose the general finding from DTI studies . However, Hampton and colleagues reconciled this conflict, particularly with the study of van den Bos and colleagues, by suggesting that the stronger frontostriatal WM connectivity, comprising the dorsal/ventral part of the dorsal striatum, may be correlated respectively with higher/lower choice impulsivity.…”

“…In contrast, diffusion‐weighted imaging studies using the diffusion tensor imaging (DTI) method have univocally pointed out that the WM integrity of the frontostriatal tract (from the prefrontal cortex (PFC) to the caudate) was negatively correlated with choice impulsivity in the healthy population . In line with this finding, a study with nonhuman primates also demonstrated that lower WM connectivity between the caudate and the dorsal PFC was correlated with higher choice impulsivity .…”