A High-Resolution Study of Positive and Negative Retinotopic Codes in the Hippocampus

Position-dependent activity in response to stimulation of the retina, or retinotopic coding, has long been considered a unique feature of the visual system. However, recent work has shown that higher-order cortical areas, including the default network, show retinotopic sensitivity in the form of decreasing signal during stimulation of their visual receptive field (Szinte and Knapen 2020; Klink et al., 2021). Motivated by this negative coding’s possible relevance to perception-memory interactions (Steel*, Silson* et al. 2023), here we characterize positive and negative retinotopic responses to visual stimuli in the hippocampus. Specifically, building on recent observations of retinotopic sensitivity in the hippocampus (Silson et al., 2021) using population receptive field (pRF) mapping, we explored this region’s positive and negative retinotopic responses using high-resolution (7T, 1.8mm isotropic) pRF mapping data from the Natural Scenes Dataset (Allen et al. 2022). We found that the hippocampus contained a relatively high proportion of negative pRFs, consistent with our prediction. On average across participants, 42% of hippocampal voxels exhibited a significant (R2 ≥ 0.08) retinotopic response, and 43% of these voxels were negative in valence. Negative voxels had similar pRF sizes to their positive counterparts. Consistent with prior work, positive pRFs showed a significant contralateral visual field bias (i.e., left hippocampus tended to represent the right visual field) (p < 0.05), while negative pRFs were more foveal and did not evidence the contralateral bias. Interestingly, resting state functional connectivity analyses suggest positive and negative hippocampal pRFs are differentially coupled to cerebral cortex, co-fluctuating more strongly with congruently signed cerebral pRFs. This work suggests the importance of visual coding in structuring the interaction between the hippocampus and cerebral cortex, and adds support for the view that negative pRFs may play an important role in hippocampally-dependent cognitive processes like episodic memory and scene construction.