Enriched environment and masticatory activity rehabilitation recover spatial memory decline in aged mice

Abstract

BackgroundTo measure the impact of masticatory reduction on learning and memory, previous studies have produced experimental masticatory reduction by modified diet or molar removal. Here we induced spatial learning impairment in mice by reducing masticatory activity and then tested the effect of a combination of environmental enrichment and masticatory rehabilitation in recovering spatial learning at adulthood and in later life. For 6 months (6M) or 18 months (18M), we fed three groups of mice from postnatal day 21 respectively with a hard diet (HD) of pellets; pellets followed by a powdered, soft diet (HD/SD, divided into equal periods); or pellets followed by powder, followed by pellets again (HD/SD/HD, divided into equal periods). To mimic sedentary or active lifestyles, half of the animals from each group were raised from weaning in standard cages (impoverished environment; IE) and the other half in enriched cages (enriched environment; EE). To evaluate spatial learning, we used the Morris water maze.ResultsIE6M-HD/SD mice showed lower learning rates compared with control (IE6M-HD) or masticatory rehabilitated (IE6MHD/SD/HD) animals. Similarly, EE-HD/SD mice independent of age showed lower performance than controls (EE-HD) or rehabilitated mice (EE-HD/SD/HD). However, combined rehabilitation and EE in aged mice improved learning rate up to control levels. Learning rates did not correlate with swim speed.ConclusionsReduction in masticatory activity imposed on mice previously fed a hard diet (HD/SD) impaired spatial learning in the Morris water maze. In adults, masticatory rehabilitation recovered spatial abilities in both sedentary and active mice, and rehabilitation of masticatory activity combined with EE recovered these losses in aged mice.

Exposure to Enriched Environment Decreases Neurobehavioral Deficits Induced by Neonatal Glutamate Toxicity

“…Several behavioral parameters are altered in animals raised under enriched conditions, including less stereotypic repetitive movements [35], decreased memory decline in aging [36], less depressive-like symptoms [37], attenuated response to phsychostimulants [38] and effects on risk-taking behavior [39]. Advantageous effects of enriched environment have been described in traumatic, ischemic and toxic neuronal lesions [9,40].…”

Difference of brain-derived neurotrophic factor expression and pyramid cell count during mastication of food with varying hardness

“…Other studies also proved that impaired function of the hippocampus due to long-term soft diet could be improved by providing a hard diet. 27 , 28 Therefore, mastication activity is critical in maintaining hippocampus function for learning and memory. 29 , 30 …”

Trigeminal, Visceral and Vestibular Inputs May Improve Cognitive Functions by Acting through the Locus Coeruleus and the Ascending Reticular Activating System: A New Hypothesis

“…There is evidence that, in addition to these short-term effects on performance and task-induced mydriasis, trigeminal signals may lead to long-term effects on the central nervous system (CNS), that may be helpful in preventing degradation of brain functions (see Ono et al, 2010 for reference). In particular, epidemiological studies have verified that tooth loss before 35 years of age or unilateral masticatory activity represents a significant risk factor for developing dementia or Alzheimer’s disease (AD; Weijenberg et al, 2011 ; Okamoto et al, 2015 ), while masticatory rehabilitation allowed aged animals to recover spatial abilities (Mendes Fde et al, 2013 ). Moreover, it has been documented, in aged animals, that bilateral molar extractions, leading to long-term masticatory dysfunction, decreases the number of pyramidal cells in the hippocampal CA1 and gyrus dentatus (Oue et al, 2013 ), with impairments in spatial learning and memory in water maze tests (Kato et al, 1997 ; Onozuka et al, 1999 ).…”