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 exploration4–6or 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.

A place with a view: A first‐person perspective in the hippocampal memory space

“…That visual stimuli, thus views, play an important role in controlling hippocampal activity in rodents or primates is undeniable. Indeed, the hippocampus responds to various visual stimuli in rodents (Lee et al, 2022; Purandare et al, 2022; Purandare & Mehta, 2023) and monkeys (Jutras et al, 2013; Sliwa et al, 2016; Wirth et al, 2003) and humans (Donoghue et al, 2023, in this issue; Quian Quirago, 2012). Rather the most intriguing question is whether and how an allocentric position code is derived from visual processing, across species.…”