Mega-scale movie-fields in the mouse visuo-hippocampal network

Abstract Natural experience often involves a continuous series of related images while the subject is immobile. How does the cortico-hippocampal circuit process this information? The hippocampus is crucial for episodic memory1–3, but most rodent single unit studies require spatial exploration4–6 or active engagement7. Hence, we investigated neural responses to a silent, isoluminant, black and white movie in head-fixed mice without any task or locomotion demands, or rewards, from the Allen Brain Observatory. The activity of most neurons (97%, 6554/6785) in the thalamo-cortical visual areas was significantly modulated by the 30s long movie clip. Surprisingly, a third (33%, 3379/10263) of hippocampal –dentate gyrus, CA1 and subiculum– neurons showed movie-selectivity, with elevated firing in specific movie sub-segments, termed movie-fields. Movie-tuning remained intact when mice were immobile or ran spontaneously. On average, a tuned cell had more than 5 movie-fields in visual areas, but only 2 in hippocampal areas. The movie-field durations in all brain regions spanned an unprecedented 1000-fold range: from 0.02s to 20s, termed mega-scale coding. Yet, the total duration of all the movie-fields of a cell was comparable across neurons and brain regions. We hypothesize that hippocampal responses show greater continuous-sequence encoding than visual areas, as evidenced by fewer and broader movie-fields than in visual areas. Consistent with this hypothesis, repeated presentation of the movie images in a fixed, scrambled sequence virtually abolished hippocampal but not visual-cortical selectivity. The enhancement of continuous movie tuning compared to the scrambled sequence was eight-fold greater in hippocampal than visual areas, further supporting episodic-sequence encoding. Thus, all mouse-brain areas investigated encoded segments of the movie. Similar results are likely to hold in primates and humans. Hence, movies could provide a unified way to probe neural mechanisms of episodic information processing and memory, even in immobile subjects, across brain regions, and species.