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

Abstract Natural behavior often involves a continuous series of related images, often while the subject is immobile. How is this information processed across the cortico-hippocampal circuit? 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, iso-luminant, black and white movie in head-fixed mice without any task or locomotion demands, or rewards. 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. On average, a 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, partly due to broader movie-fields in hippocampal areas, indicating greater sequence coding. Consistently presentation of the movie images in a scrambled sequence virtually abolished hippocampal but not visual-cortical selectivity. The enhancement of sequential movie tuning compared to the scrambled sequence was eight-fold greater in hippocampal than visual areas, further supporting visual sequence encoding. Thus, a movie was encoded in all mouse-brain areas investigated. Similar results are likely to hold in primates and humans. Hence, movies could provide a unified way to probe neural mechanisms of non-spatial information processing and memory across brain regions and species.