12 months is a pivotal age for olfactory perceptual learning and its underlying neuronal plasticity in aging mice

• Published in: Neurobiology of aging Vol. 114; pp. 73 - 83
• Main Authors: Greco-Vuilloud, Juliette, Midroit, Maëllie, Terrier, Claire, Forest, Jérémy, Sacquet, Joëlle, Mandairon, Nathalie, Didier, Anne, Richard, Marion
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.06.2022; Elsevier
• Subjects: Adult neurogenesis; Aging; Aging - physiology; Animals; Cognitive Sciences; Granule cell; Life Sciences; Memory; Memory Disorders; Mice; Neurogenesis - physiology; Neuronal Plasticity - physiology; Neurons and Cognition; Odorants; Olfactory Bulb - physiology; Perceptual learning; Smell - physiology; Spine; Structural plasticity; Granule cell; Structural plasticity; Spine; Adult neurogenesis; Memory; Aging; Perceptual learning
• ISSN: 0197-4580; 1558-1497
• DOI: 10.1016/j.neurobiolaging.2022.03.003

Normal brain aging is associated with deficits in cognitive and sensory processes, due to subtle impairment of synaptic contacts and plasticity. Impairment may be discrete in basal conditions but is revealed when cerebral plasticity is involved, such as in learning contexts. We used olfactory perceptual learning, a non-associative form of learning in which discrimination between perceptually similar odorants is improved following exposure to these odorants, to better understand the cellular bases of olfactory aging in mice. We first evaluated learning ability and memory retention in 2-, 6-, 12-, and 18-month-old mice, and identified 12 months as a pivotal age when memory retention subtly declines before learning becomes totally impaired at later ages. We then showed that learning-induced structural plasticity of adult-born granule cells is specific to cells responding to the learned odorants in the olfactory bulb of young adult mice and loses its specificity in 12-month-old mice, in parallel to memory impairment. Taken together, our data refine our understanding of aging-related impairment of plasticity mechanisms in the olfactory bulb and consequent induction of olfactory learning and memory deficits. •Memory after olfactory perceptual learning declines at 12 months.•At 2 months, only neurons responding to learned odorants show structural plasticity.•At 12 months, structural plasticity loses its specificity toward learned odorants.