Rapid coordination of effective learning by the human hippocampus
The hippocampus is essential for long-term memory (1) and memory-guided behaviors such as spatial navigation (2–4). For example, long-term memory guides visuospatial attention (5, 6) such that past experiences can influence the rapid (∼2 to 5/s) saccadic eye movements needed to sample complex stimuli such as visual scenes (7–9). Yet, the role of the hippocampus in guiding visual sampling might be far more immediate, supporting online representations that emerge across sequential visual fixations and rapidly guide choices of where to look next (10, 11). During the first exposure to complex stimuli, hippocampal lesions disrupt viewing patterns that reflect building a memory for the relations among distinct stimulus features (12, 13), and these viewing patterns correlate with hippocampal activity as measured via functional magnetic resonance imaging (fMRI) in healthy individuals (12, 14). Failure to effectively sample relations among distinct features via eye movements could also underlie impaired perception and short-term retention of complex stimuli identified following hippocampal lesions (15–21). These short-term behavioral deficits are surprising given the standard model of hippocampal involvement in long-term memory and suggest that long-term memory impairments could result from disrupted visual sampling during initial encoding. However, previous studies have been inconclusive in demonstrating that the hippocampus has a short-term role in the rapid formation and online use of memory to guide viewing because those studies lacked the requisite spatial and temporal resolution.
We therefore used intracranial electroencephalography (iEEG) to provide temporally precise measurement of human hippocampal activity aligned to saccadic eye movements during scene memory formation (Fig. 1A). The goal was to test whether hippocampal activity recorded while participants (N = 6) viewed novel scenes reflected the influence of the rapidly forming scene memory on an effective eye-movement pattern that enhanced learning. To achieve this, we identified an eye movement pattern termed “revisitation” while subjects studied novel scenes that reflected the influence of short-term/within-episode memory on viewing. Revisitation signaled effective viewing for memory formation in that it predicted scene-specific spatiotemporal memory as expressed via eye movements during delayed testing. Thus, we hypothesized that revisitation eye movements would temporally dissociate hippocampal iEEG correlates of short-term retrieval, occurring immediately before and therefore initiating the viewing pattern, versus encoding, occurring immediately after the viewing pattern and reflecting its impact on enhanced memory formation.