Abstract
Relating individual differences in cognitive abilities to neural substrates in older adults is of significant scientific and clinical interest, but remains a major challenge. Previous functional magnetic resonance imaging (fMRI) studies of cognitive aging have mainly focused on the amplitude of fMRI response, which does not measure neuronal selectivity and has led to some conflicting findings. Here, using local regional heterogeneity analysis, or Hcorr, a novel fMRI analysis technique developed to probe the sparseness of neuronal activations as an indirect measure of neuronal selectivity, we found that individual differences in two different cognitive functions, episodic memory and letter verbal fluency, are selectively related to Hcorr-estimated neuronal selectivity at their corresponding brain regions (hippocampus and visual-word form area, respectively). This suggests a direct relationship between cognitive function and neuronal selectivity at the corresponding brain regions in healthy older adults, which in turn suggests that age-related neural dedifferentiation might contribute to rather than compensate for cognitive decline in healthy older adults. Additionally, the capability to estimate neuronal selectivity across brain regions with a single data set and link them to cognitive performance suggests that, compared to fMRI-adaptation—the established fMRI technique to assess neuronal selectivity, Hcorr might be a better alternative in studying normal aging and neurodegenerative diseases, both of which are associated with widespread changes across the brain.
Highlights
Cognitive abilities are highly heterogeneous among individuals, and this variance is typically even higher in older compared to middle-aged adults (Morse, 1993; Spreng et al, 2010)
Given recent findings suggesting that neurons in hippocampus are highly selective with a sparse neural representation (Quiroga et al, 2005; Viskontas et al, 2009), we hypothesized that, in healthy older adults, poor episodic memory is due to reduced neuronal selectivity in the hippocampus and individual differences in episodic memory can be related to variations in neuronal selectivity in the hippocampus
By reanalyzing functional magnetic resonance imaging (fMRI) data from previously published work (Simon et al, 2011) in which subjects were participating in an implicit sequence learning task, we found that the novel heterogeneity of correlations (Hcorr) technique (Jiang et al, 2013) can reliably estimate neuronal selectivity across different brain regions in healthy older adults with a single data set and that individual differences in a specific cognitive function correlated with Hcorr measures at the corresponding–but not other–brain regions
Summary
Cognitive abilities are highly heterogeneous among individuals, and this variance is typically even higher in older compared to middle-aged adults (Morse, 1993; Spreng et al, 2010). Because individuals with lower cognitive performance are at a higher risk of Alzheimer’s disease (AD) and other age-related dementias (Masur et al, 1994; Albert et al, 2001; Riley et al, 2005), identifying the neural bases of these individual cognitive differences in older adults might reveal potential neural targets for interventional therapies These could in turn help to preserve or even improve cognitive function, thereby reducing the risk of AD and other types of dementia. Using a different fMRI technique, multi-voxel pattern analysis (MVPA) (Norman et al, 2006), it has been shown that the distinctiveness of neuronal response to preferred vs non-preferred stimulus classes is reduced in aged brain (Carp et al, 2010) Taken together, these studies reveal a general reduction in the distinctiveness of neural representations with healthy aging, i.e., age-related neural dedifferentiation
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