The spatiotemporal organization of experience dictates hippocampal involvement in primary visual cortical plasticity

• Published in: Current biology 2021-09, Vol.31 (18), p.3996-4008.e6
• Main Authors: Finnie, Peter S.B., Komorowski, Robert W., Bear, Mark F.
• Format: Article
• Language: English
• Subjects: Animals; hippocampus; Hippocampus - physiology; long-term memory; Long-Term Potentiation; Memory, Long-Term - physiology; Mice; Neocortex; Neuronal Plasticity - physiology; primary visual cortex; synaptic plasticity; systems consolidation; Visual Cortex - physiology
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.06.079

The hippocampus and neocortex are theorized to be crucial partners in the formation of long-term memories. Here, we assess hippocampal involvement in two related forms of experience-dependent plasticity in the primary visual cortex (V1) of mice. Like control animals, those with hippocampal lesions exhibit potentiation of visually evoked potentials after passive daily exposure to a phase-reversing oriented grating stimulus, which is accompanied by long-term habituation of a reflexive behavioral response. Thus, low-level recognition memory is formed independently of the hippocampus. However, response potentiation resulting from daily exposure to a fixed sequence of four oriented gratings is severely impaired in mice with hippocampal damage. A feature of sequence plasticity in V1 of controls, which is absent in lesioned mice, is the generation of predictive responses to an anticipated stimulus element when it is withheld or delayed. Thus, the hippocampus is involved in encoding temporally structured experience, even within the primary sensory cortex. •Hippocampus is required for long-term plasticity in V1 elicited by visual sequences•Hippocampal damage impairs anticipatory activity when sequence elements are withheld•Hippocampus is required for V1 stimulus representations shaped by temporal context Finnie et al. show that hippocampal damage impairs plasticity elicited in primary visual cortex by stimuli presented in temporal sequences, but not by repetitive exposure to a single stimulus. V1 therefore provides a powerful platform to delineate when and how the hippocampus contributes to encoding, storage, and retrieval of sensory experiences.