The stability of memories during brain remodeling: A perspective

Abstract

One of the most important features of the nervous system is memory: the ability to represent and store experiences, in a manner that alters behavior and cognition at future times when the original stimulus is no longer present. However, the brain is not always an anatomically stable structure: many animal species regenerate all or part of the brain after severe injury, or remodel their CNS toward a new configuration as part of their life cycle. This raises a fascinating question: what are the dynamics of memories during brain regeneration? Can stable memories remain intact when cellular turnover and spatial rearrangement modify the biological hardware within which experiences are stored? What can we learn from model species that exhibit both, regeneration and memory, with respect to robustness and stability requirements for long-term memories encoded in living tissues? In this Perspective, we discuss relevant data in regenerating planaria, metamorphosing insects, and hibernating ground squirrels. While much remains to be done to understand this remarkable process, molecular-level insight will have important implications for cognitive science, regenerative medicine of the brain, and the development of non-traditional computational media in synthetic bioengineering.

Keywords: brain; learning; memory; metamorphosis; regeneration; remodeling.

Figure 1.

Animal models of memories that survive brain remodeling Holometabolous insects reorganize their brains during pupation in the transition from larva to adult, with many neurons of the central nervous system pruning to the cell body before the generation of adult specific structures. Planarian species are capable of regenerating their entire brain from a tail fragment in the event of fission or amputation, with new tissue arising from a neoblast stem cell population. Arctic ground squirrels demonstrate a drastic reduction in brain volume during hibernation at near freezing temperatures, which is corrected within hours of arousal. In all 3 of these animal groups, learned behaviors have been observed to survive the striking reorganization of the brain. Photos courtesy of Jerry Friedman (Monarch caterpillar), Ianaré Sévi, Linda Mahoney, and Bering Land Bridge National reserve (top, center, and bottom ground squirrel images respectively), used with permission.