The environmental sculpting hypothesis of juvenile and adult hippocampal neurogenesis

• Published in: Progress in neurobiology 2021-04, Vol.199, p.101961-101961, Article 101961
• Main Authors: Cushman, Jesse D., Drew, Michael R., Krasne, Franklin B.
• Format: Article
• Language: English
• Subjects: Adult neurogenesis; Aging; Animals; Dentate gyrus; Hippocampus; Learning; Memory; Neurogenesis; Prospective Studies
• ISSN: 0301-0082; 1873-5118
• DOI: 10.1016/j.pneurobio.2020.101961

•We propose that postnatal neurogenesis allows behavioral experience to sculpt dentate connectivity.•Dentate cells become preferentially innervated by environmentally-relevant neocortical input.•Simulations demonstrate that such sculpting can greatly increase storage capacity•Sculpting is needed while animals are becoming familiar with their environment•This explains why neurogenesis declines as animals mature. We propose that a major contribution of juvenile and adult hippocampal neurogenesis is to allow behavioral experience to sculpt dentate gyrus connectivity such that sensory attributes that are relevant to the animal’s environment are more strongly represented. This “specialized” dentate is then able to store a larger number of discriminable memory representations. Our hypothesis builds on accumulating evidence that neurogenesis declines to low levels prior to adulthood in many species. Rather than being necessary for ongoing hippocampal function, as several current theories posit, we argue that neurogenesis has primarily a prospective function, in that it allows experience to shape hippocampal circuits and optimize them for future learning in the particular environment in which the animal lives. Using an anatomically-based simulation of the hippocampus (BACON), we demonstrate that environmental sculpting of this kind would reduce overlap among hippocampal memory representations and provide representation cells with more information about an animal's current situation; consequently, it would allow more memories to be stored and accurately recalled without significant interference. We describe several new, testable predictions generated by the sculpting hypothesis and evaluate the hypothesis with respect to existing evidence. We argue that the sculpting hypothesis provides a strong rationale for why juvenile and adult neurogenesis occurs specifically in the dentate gyrus and why it declines significantly prior to adulthood.