Age-related disparities in oscillatory dynamics within scene-selective regions during spatial navigation

Abstract

AbstractPosition is a key property that allows certain objects in the environment to attain navigational relevance. Symmetrical processing of object position across the horizontal meridian remains an unchallenged assumption of the spatial navigation literature. Nonetheless, a growing body of research reports vertical inhomogeneities in perceptual tasks, and recent evidence points towards a lower visual field preference in healthy aging. Factoring in the vertical position of objects to better apprehend spatial navigation abilities across the lifespan is essential. The occipital place area (OPA), parahippocampal place area (PPA), and medial place area (MPA) are ideal candidates to support the processing of the vertical location of navigational cues. Indeed, they are implicated in scene processing and spatial cognition, functions that may interact with their underlying retinotopic codes. This study aimed to elucidate whether young and older participants adjusted their gaze patterns and EEG activity within scene-selective regions in response to the vertical arrangement of landmarks. A sample of 21 young and 21 older participants completed a desktop-based task requiring them to navigate using objects at different vertical locations. We equipped them with an eye tracker and a high-density EEG cap. We used a fMRI-informed source-reconstruction algorithm to study the OPA, PPA and MPA with high spatial and temporal precision. Older adults exhibited a higher number of errors compared to young adults during reorientation. This age-related decline in accuracy was accompanied by a tendency among older participants to fixate objects in the lower half of the screen. This gaze bias was absent in young participants, who instead adapted their oculomotor behaviour based on the position of navigationally-relevant information. Another primary finding pertains to the differential pattern of theta and beta band activity in the OPA, PPA and RSC for environments that only contained relevant cues in the upper visual field. It thus appears that scene-selective regions process some aspect of the vertical position of information, irrespectively of their inherent retinotopic biases. Moreover, we revealed striking disparities between age groups in beta/gamma band synchronization in all scene-selective regions, indicating compromised top-down attentional mechanisms during spatial navigation in ageing. These age-related disparities in attentional dynamics might account for performance deficits in older participants. This study sheds light on a systematic downward gaze bias and altered attentional dynamics within scene-selective regions during spatial navigation in older age. It also emphasises the importance of considering vertical positioning as a fundamental property of objects within scenes.