Robust Resilience of the Frontotemporal Syntax System to Aging

Abstract

Brain function is thought to become less specialized with age. However, this view is largely based on findings of increased activation during tasks that fail to separate task-related processes (e.g., attention, decision making) from the cognitive process under examination. Here we take a systems-level approach to separate processes specific to language comprehension from those related to general task demands and to examine age differences in functional connectivity both within and between those systems. A large population-based sample (N = 111; 22-87 years) from the Cambridge Centre for Aging and Neuroscience (Cam-CAN) was scanned using functional MRI during two versions of an experiment: a natural listening version in which participants simply listened to spoken sentences and an explicit task version in which they rated the acceptability of the same sentences. Independent components analysis across the combined data from both versions showed that although task-free language comprehension activates only the auditory and frontotemporal (FTN) syntax networks, performing a simple task with the same sentences recruits several additional networks. Remarkably, functionality of the critical FTN is maintained across age groups, showing no difference in within-network connectivity or responsivity to syntactic processing demands despite gray matter loss and reduced connectivity to task-related networks. We found no evidence for reduced specialization or compensation with age. Overt task performance was maintained across the lifespan and performance in older, but not younger, adults related to crystallized knowledge, suggesting that decreased between-network connectivity may be compensated for by older adults' richer knowledge base.

Significance statement: Understanding spoken language requires the rapid integration of information at many different levels of analysis. Given the complexity and speed of this process, it is remarkably well preserved with age. Although previous work claims that this preserved functionality is due to compensatory activation of regions outside the frontotemporal language network, we use a novel systems-level approach to show that these "compensatory" activations simply reflect age differences in response to experimental task demands. Natural, task-free language comprehension solely recruits auditory and frontotemporal networks, the latter of which is similarly responsive to language-processing demands across the lifespan. These findings challenge the conventional approach to neurocognitive aging by showing that the neural underpinnings of a given cognitive function depend on how you test it.

Keywords: ICA; aging; functional connectivity; language comprehension; syntax; task demands.

Figure 1.

A, Mean RTs for the subordinate, dominant, and unambiguous conditions (dots represent individual datapoints, with a boxplot overlaid). Data are split into three age groups detailed in Table 1. B, Scatterplot showing the relationship between age and syntactic sensitivity (i.e., subordinate–unambiguous RTs).

Figure 2.

Functional networks differentially active during natural listening and task. Left, The group average spatial map for each component rendered on a canonical brain. Right, Individual loading values (with a boxplot overlaid) for each network during Natural Listening and Task for the four conditions (acoustic baseline, subordinate, dominant, and unambiguous).

Figure 3.

Effects of task and within-network connectivity (WNC) on between-network connectivity (BNC). BNC matrices for (A) Task and (B) Natural Listening. Pairwise correlations were computed between-subject-specific time courses for each of the seven networks and then averaged across participants. Color bar indicates the strength of the average correlation (avg corr), with gray squares indicating nonsignificant correlations (p > 0.05, Bonferroni corrected). C, Difference in BNC between task and natural listening. D, E, Asymmetrical matrices showing the correlation between WNC in each network and BNC during Task and Natural Listening, respectively. Network labels listed down the left-hand side signify both the WNC value being correlated, as well as one of the networks in each BNC pair (the other is listed along the bottom).

Figure 4.

Relationship of between-network connectivity (BNC) to age and gray matter during the task (A, B) and natural listening (C, D). Background color indicates average BNC strength. Black dots indicate the correlation between BNC and age or GMC, with diamonds indicating a negative relationship and circles indicating a positive relationship. The size of the dot indicates the strength of the correlation. Some of the effects seen during the task are also replicated during Natural Listening (e.g., age to AUD-FTN, MDN-DMN, and GMC to MDN-DMN), whereas other effects are novel.

Figure 5.

Predictors of overt task performance. A, Background color indicates average BNC strength during the task and black dots indicate a significant correlation (p < 0.05, uncorrected) between connectivity and syntactic sensitivity (i.e., subordinate–unambiguous RTs). B, Scatterplot showing that crystallized intelligence becomes a stronger predictor of task performance with age.