Selective neural coding of object, feature, and geometry spatial cues in humans

Abstract

Orienting in space requires the processing of visual spatial cues. The dominant hypothesis about the brain structures mediating the coding of spatial cues stipulates the existence of a hippocampal-dependent system for the representation of geometry and a striatal-dependent system for the representation of landmarks. However, this dual-system hypothesis is based on paradigms that presented spatial cues conveying either conflicting or ambiguous spatial information and that used the term landmark to refer to both discrete three-dimensional objects and wall features. Here, we test the hypothesis of complex activation patterns in the hippocampus and the striatum during visual coding. We also postulate that object-based and feature-based navigation are not equivalent instances of landmark-based navigation. We examined how the neural networks associated with geometry-, object-, and feature-based spatial navigation compared with a control condition in a two-choice behavioral paradigm using fMRI. We showed that the hippocampus was involved in all three types of cue-based navigation, whereas the striatum was more strongly recruited in the presence of geometric cues than object or feature cues. We also found that unique, specific neural signatures were associated with each spatial cue. Object-based navigation elicited a widespread pattern of activity in temporal and occipital regions relative to feature-based navigation. These findings extend the current view of a dual, juxtaposed hippocampal-striatal system for visual spatial coding in humans.They also provide novel insights into the neural networks mediating object versus feature spatial coding, suggesting a need to distinguish these two types of landmarks in the context of human navigation.

Landmark-based spatial navigation across the human lifespan

“…The differential influence of landmark and geometric cues on human navigation suggests a potential dissociation of the related neural processing pathways. If indeed different subnetworks in the brain mediate the processing of different types of cues ( Ramanoël et al, 2022 ), our results suggest that the subnetwork dedicated to geometric processing matures earlier in development and it is preserved better in aging. Construction of geometry-based spatial representations could thus represent the basic mode of spatial learning, with efficient binding of landmark to the representations of space developing during primary school years and deteriorating early in aging.…”

Common and specific activations supporting optic flow processing and navigation as revealed by a meta-analysis of neuroimaging studies

“…A further systematic literature search was performed using the following string: ‘fMRI AND (“spatial navigation” or “egocentric” or “allocentric”)’. This search produced 127 resulting original articles; based on the inclusion criteria reported above, 11 experiments from 5 of these articles (Ramanoël et al 2020 , 2022 ; Riemer et al 2022 ; Noachtar et al 2022 ; Qi et al 2022 ) were included. In addition to the 91 experiments from 32 papers already included in Teghil et al ( 2021 ), the general meta-analysis on spatial navigation was thus performed on 102 experiments from 37 papers for a total of 1984 participants.…”

Age-related differences in electrophysiological correlates of visuospatial reorientation

“…More recently, Bécu et al (2023) extended these findings by unveiling a specific decline in landmark-based navigation ( i.e., encoding objects) but a preserved performance during geometry-based navigation ( i.e., encoding spatial layouts). These two navigation modalities exhibit specific neural signatures in young adults (Ramanoël et al, 2022) highlighting the importance of considering their neural correlates to gain insight into the specific deficits of older adults in landmark navigation.…”