The Relationship between Age, Neural Differentiation, and Memory Performance

Abstract

Healthy aging is associated with decreased neural selectivity (dedifferentiation) in category-selective cortical regions. This finding has prompted the suggestion that dedifferentiation contributes to age-related cognitive decline. Consistent with this possibility, dedifferentiation has been reported to negatively correlate with fluid intelligence in older adults. Here, we examined whether dedifferentiation is associated with performance in another cognitive domain-episodic memory-that is also highly vulnerable to aging. Given the proposed role of dedifferentiation in age-related cognitive decline, we predicted there would be a stronger link between dedifferentiation and episodic memory performance in older than in younger adults. Young (18-30 years) and older (64-75 years) male and female humans underwent fMRI scanning while viewing images of objects and scenes before a subsequent recognition memory test. We computed a differentiation index in two regions of interest (ROIs): parahippocampal place area (PPA) and lateral occipital complex (LOC). This index quantified the selectivity of the BOLD response to preferred versus nonpreferred category of an ROI (scenes for PPA, objects for LOC). The differentiation index in the PPA, but not the LOC, was lower in older than in younger adults. Additionally, the PPA differentiation index predicted recognition memory performance for the studied items. This relationship was independent of and not moderated by age. The PPA differentiation index also predicted performance on a latent "fluency" factor derived from a neuropsychological test battery; this relationship was also age invariant. These findings suggest that two independent factors, one associated with age, and the other with cognitive performance, influence neural differentiation.SIGNIFICANCE STATEMENT Aging is associated with neural dedifferentiation-reduced neural selectivity in "category-selective" cortical brain regions-which has been proposed to contribute to cognitive aging. Here, we examined whether neural differentiation is predictive of episodic memory performance, and whether the relationship is moderated by age. A neural differentiation index was estimated for scene-selective (PPA) and object-selective (LOC) cortical regions while participants studied images for a subsequent memory test. Age-related reductions were observed for the PPA, but not for the LOC, differentiation index. Importantly, the PPA differentiation index demonstrated age-invariant correlations with subsequent memory performance and a fluency factor derived from a neuropsychological battery. Together, these findings suggest that neural differentiation is associated with two independent factors: age and cognitive performance.

Keywords: dedifferentiation; lateral occipital complex; neural selectivity; older adults; parahippocampal place area; recognition memory.

Figure 1.

Schematic overview of the memory task. Participants studied an intermixed list of object and scene images under intentional encoding instructions while undergoing fMRI scanning. Each image was preceded by a task cue that instructed participants to rate the image for pleasantness (P?) or to determine which movie genre the image was best associated with (M?). There was a total of five scanned study phases. After the final study phase, an out-of-scanner recognition memory test was administered. The test phase comprised the studied objects and scenes intermixed with new images. Participants were instructed to select one of four memory judgments for each image. The four judgments comprised options for whether participants had high confidence both that they studied the image and could recollect the study task (Old Pleasant and Old Movie responses), had high confidence that they studied the image but were had low confidence in their memory for or could not remember the study task (Old-Don't Know response), or whether they did not have high confidence that the image was studied (New response). Two measures of memory performance were obtained from the test phase: item recognition and recall of the encoding task (i.e., source recall).

Figure 2.

A, Voxels comprising the regions-of-interest (ROIs) in the PPA (yellow voxels) and LOC (red voxels) derived from an unpublished dataset. Note that the ROIs were anatomically masked using the Neuroinformatics atlas included in SPM12. The anatomical labels for this mask included bilateral parahippocampal, fusiform, middle occipital, and inferior occipital gyri. B, Statistical parameteric maps (SPMs) from the unpublished experiment showing the one-tailed contrasts of Scene > Objects and Objects > Scenes. C, SPMs for the Scene > Objects and Objects > Scene contrast in the 24 young and 24 older adults in the present data (collapsed across age group). The SPMs are thresholded at FWE of p < 0.05.

Figure 3.

A, Plot of the differentiation index computed from the LOC and PPA for young and older adults. B, Plot of the across-trial mean β-values for each image type and region of interest. Each green and orange circle represents an individual participant's data, and the black circle represents the group mean, with error bars denoting ±1 SEM.

Figure 4.

A–D, Scatter plots showing the partial correlation between the PPA differentiation index and item recognition (A, B) and source memory (C, D). The partial plots control for age group (A, C), age group and source memory (B), and age group and item recognition (D).

Figure 5.

Scatter plots showing the partial correlation between the PPA differentiation index and the factor score for fluency (RC4) controlling for age.

Figure 6.

A, Plot of the similarity index (within-between similarity for the preferred image type) computed from the LOC and PPA for young and older adults. B, Scatter plot showing the partial correlation between the similarity index in the PPA and item recognition controlling for age group.