Switching between External and Internal Attention in Hippocampal Networks

Abstract

Everyday experience requires processing external signals from the world around us and internal information retrieved from memory. To do both, the brain must fluctuate between states that are optimized for external versus internal attention. Here, we focus on the hippocampus as a region that may serve at the interface between these forms of attention and ask how it switches between prioritizing sensory signals from the external world versus internal signals related to memories and thoughts. Pharmacological, computational, and animal studies have identified input from the cholinergic basal forebrain as important for biasing the hippocampus toward processing external information, whereas complementary research suggests the dorsal attention network (DAN) may aid in allocating attentional resources toward accessing internal information. We therefore tested the hypothesis that the basal forebrain and DAN drive the hippocampus toward external and internal attention, respectively. We used data from 29 human participants (17 female) who completed two attention tasks during fMRI. One task (memory-guided) required proportionally more internal attention, and proportionally less external attention, than the other (explicitly instructed). We discovered that background functional connectivity between the basal forebrain and hippocampus was stronger during the explicitly instructed versus memory-guided task. In contrast, DAN–hippocampus background connectivity was stronger during the memory-guided versus explicitly instructed task. Finally, the strength of DAN–hippocampus background connectivity was correlated with performance on the memory-guided but not explicitly instructed task. Together, these results provide evidence that the basal forebrain and DAN may modulate the hippocampus to switch between external and internal attention. SIGNIFICANCE STATEMENT How does the brain balance the need to pay attention to internal thoughts and external sensations? We focused on the human hippocampus, a region that may serve at the interface between internal and external attention, and asked how its functional connectivity varies based on attentional states. The hippocampus was more strongly coupled with the cholinergic basal forebrain when attentional states were guided by the external world rather than retrieved memories. This pattern flipped for functional connectivity between the hippocampus and dorsal attention network, which was higher for attention tasks that were guided by memory rather than external cues. Together, these findings show that distinct networks in the brain may modulate the hippocampus to switch between external and internal attention.