Altered age-related alpha and gamma prefrontal-occipital connectivity serving distinct cognitive interference variants

Abstract

The presence of conflicting stimuli adversely affects behavioral outcomes, which could either be at the level of stimulus (Flanker), response (Simon), or both (Multisource). Briefly, flanker interference involves conflicting stimuli requiring selective attention, Simon interference is caused by an incongruity between the spatial location of the task-relevant stimulus and prepotent motor mapping, and multisource is combination of both. Irrespective of the variant, interference resolution necessitates cognitive control to filter irrelevant information and allocate neural resources to task-related goals. Though previously studied in healthy young adults, the direct quantification of changes in oscillatory activity serving such cognitive control and associated inter-regional interactions in healthy aging are poorly understood. Herein, we used an adapted version of the multisource interference task and magnetoencephalography to investigate age-related alterations in the neural dynamics governing both divergent and convergent cognitive interference in 78 healthy participants (age range: 20-66 years). We identified weaker alpha connectivity between bilateral visual and right dorsolateral prefrontal cortices (DLPFC) and left dorsomedial prefrontal cortices (dmPFC), as well as weaker gamma connectivity between bilateral occipital regions and the right dmPFC during flanker interference with advancing age. Further, an age-related decrease in gamma power was observed in the left cerebellum and parietal region for Simon and differential interference effects (i.e., flanker-Simon), respectively. Moreover, the superadditivity model showed decreased gamma power in the right temporoparietal junction (TPJ) with increasing age. Overall, our findings suggest age-related declines in the engagement of top-down attentional control secondary to reduced alpha and gamma coupling between prefrontal and occipital cortices.

Keywords: aging; functional connectivity; magnetoencephalography; multisource interference task; superadditivity.

Fig. 1.

Experimental Paradigm and Behavioral performance. Each trial began with a central fixation presented for a randomly varied interstimulus interval of 2000–2400 ms. The fixation was then replaced by a vertically centered horizontal row of three equally spaced integers between 0 and 3. The presentation of the integer stimuli lasted for 1500 ms. Two of these integers were always identical (task irrelevant) and the third was different (task relevant). Prior to beginning the experiment, participants were given a five-finger button pad and instructed that the index, middle, and ring finger locations represented the integers 1, 2, and 3, respectively. Participants were then instructed that on each trial they would be presented with a horizontal row of three integers, and that the objective was to indicate the “odd-number-out” by pressing the button corresponding to its numerical identity (and not its spatial location). Using these stimuli, four interference conditions were possible: (1) control (no interference), (2) Simon (stimulus–response interference), (3) Flanker (stimulus–stimulus interference), and (4) multisource.

Fig. 2.

(A) Results from the behavioral analyses show the main effect of interference condition, with each condition differing in a stair-step pattern. Reaction time is displayed on the y-axis with interference conditions on the x-axis. (B) Reaction time was assessed as a function of age using Pearson correlations. There was a significant correlation between reaction time and age, such that as age increased, reaction time collapsed across all four conditions increased. (C) Behavioral results from the super-additivity analyses, with reaction time on y-axis and inference conditions (i.e., multisource and additive effect) on the x-axis. Plots display the individual data points, along with the median (horizontal line), first and third quartile (box), and local minima and maxima (whiskers). Error bars reflect the SEM. * p < .05, ** p =/ < .001

Fig. 3.. Sensor-level time-frequency analysis.

The MEG sensor spectrograms (left) display the time–frequency representations of neural responses identified by cluster-based permutation analysis (see Methods section), highlighted using the white dotted boundaries. Time (in ms) is denoted on the x-axis and frequency (in Hz) on the y-axis, with the dashed white line at 0 ms indicating the onset of the integer stimuli. The color scale bar for percent change from baseline is displayed above each plot. Each spectrogram represents group- and condition-averaged data from one gradiometer sensor that was representative of the neural response in sensors over either occipito-parietal (top and bottom) or somato-motor (middle) regions. On the far right is the source-imaged representation of each response, with the color scale bar to the right denoting response amplitude in pseudo-t units.

Fig. 4.. Age-related changes in cortico-cortical coherence with bilateral occipital cortices.

In the flanker interference condition (flanker-control), coherence maps revealed decreased connectivity between the bilateral occipital seed and right DLPFC (top) as well as left dmPFC (middle) relative to the baseline with increasing age. In addition, weaker coherence between bilateral occipital seeds and the right dmPFC was also observed for the gamma flanker interference effect (bottom).

Fig. 5.. Age-related superadditivity effects on alpha prefrontal-occipital coherence.

The superadditive effect on coherence was computed by subtracting the additive model (i.e., flanker + simon) from multisource interference. The effect of aging was then examine using whole-brain correlations, which indicated a positive association such that connectivity increased as a function of age.

Fig. 6.. Age-related gamma oscillatory power interference effects.

Whole-brain voxel-wise correlational analysis of interference maps with age revealed a decrease in gamma power in (A) left cerebellum during Simon interference (i.e., simon-control), (B) left SPL/IPS for differential interference (i.e., flanker-simon), and (C) right TPJ during superadditivity interference (i.e., multisource-additive).