The relationship between neural differentiation and exploratory eye movements in healthy young and older adults

Abstract

Age-related neural dedifferentiation, characterized by lower selectivity of neural responses in the high-level sensory cortex, is thought to be a major contributor to age-related cognitive decline. However, the mechanisms that underlie dedifferentiation are poorly understood. Building on prior evidence that exploratory eye movements differ with age, we investigated the role that eye movement might play in age-related declines in neural selectivity. Healthy young and older adults of both sexes underwent fMRI with simultaneous eye-tracking as they viewed words paired with images of scenes and objects prior to a memory test. Consistent with numerous prior reports, multivoxel pattern similarity analysis (PSA) of the fMRI data revealed age-related neural dedifferentiation in scene-selective, but not object-selective cortex. Eye movements, operationalized as the number of gaze fixations made during stimulus viewing, were elevated in older adults. Analyses examining the relationship between trial-wise estimates of neural selectivity and fixation count revealed an age-invariant positive relationship in the object-selective lateral occipital complex. However, this association was found to be age-dependent in scene-selective cortex, such that there was a robust positive relationship between scene selectivity and fixation count in young, but not older adults. Lastly, scene-related selectivity in the parahippocampal place area predicted subsequent memory performance independently of age group and fixation counts at encoding. These findings suggest that age-related neural dedifferentiation in scene-selective cortex may relate to declines in the functional specialization of exploratory eye movements during scene viewing. Significance statementHealthy aging is associated with lower neural selectivity in brain regions responsive to distinct categories of perceptual stimuli. This phenomenon is most commonly observed in scene-selective cortex, although the underlying reasons remain unknown. Here, we report that trial-wise estimates of neural selectivity positively covary with the number of eye movements made during stimulus viewing. However, we also report an age-related breakdown in this relationship within scene-selective cortex, consistent with the notion that age differences in eye movements and neural selectivity reflect deficits in the extraction and binding of visual information into memory. The present findings highlight the complex interactions that occur between age, neural selectivity and eye movements, and provide novel insights into neural and behavioral mechanisms underlying cognitive aging.