Altered mastication adversely impacts morpho-functional features of the hippocampus: A systematic review on animal studies in three different experimental conditions involving the masticatory function

Piancino, Maria Grazia; Tortarolo, Alessandro; Polimeni, Antonella; Bramanti, Ennio; Bramantı, Placido

doi:10.1371/journal.pone.0237872

Cited by 25 publications

(17 citation statements)

References 47 publications

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“…Furthermore, a meta-analysis of cohort studies found that individuals with <20 teeth were more likely to develop cognitive impairment and dementia, supporting the close correlation between tooth loss and cognitive decline (Cerutti-Kopplin et al 2016). In various animal models of altered mastication, decreases in hippocampal neuron number, synaptic activity, neurogenesis, and spatial memory test performance have been consistently reported (Piancino et al 2020). Thus, disturbed mastication can negatively affect not only the normal function of the hippocampus but also hippocampus-dependent memory and cognition.…”

Section: Introductionmentioning

confidence: 99%

Aβ Accumulation in Vmo Contributes to Masticatory Dysfunction in 5XFAD Mice

Kim

et al. 2021

J Dent Res

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Alzheimer’s disease (AD) shows various symptoms that reflect cognitive impairment and loss of neural circuit integrity. Sensory dysfunctions such as olfactory and ocular pathology are also observed and used as indicators for early detection of AD. Although mastication is suggested to correlate with AD progression, changes in the masticatory system have yet to be established in transgenic animal models of AD. In the present study, we have assessed pathologic hallmarks of AD with the masticatory behavior of 5XFAD mice. We found that masticatory efficiency and maximum biting force were decreased in 5XFAD mice, with no significant change in general motor function. Immunohistochemical analysis revealed significant accumulation of Aβ (amyloid β), increased microglia number, and cell death in Vmo (trigeminal motor nucleus) as compared with other cranial motor nuclei that innervate the orofacial region. Masseter muscle weight and muscle fiber size were also decreased in 5XFAD mice. Taken together, our results demonstrate that Aβ accumulation in Vmo contributes to masticatory dysfunction in 5XFAD mice, suggesting a close association between masticatory dysfunction and dementia.

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Section: Introductionmentioning

confidence: 99%

Aβ Accumulation in Vmo Contributes to Masticatory Dysfunction in 5XFAD Mice

Kim

et al. 2021

J Dent Res

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“…Several experimental models of masticatory dysfunction have been explored to clarify the cellular and molecular mechanisms associated with memory impairment [ 25 , 26 , 27 ]. From these studies, we have learned that chewing maintains hippocampus-dependent cognitive function [ 18 ], and that age-related spatial memory deficits can be aggravated by a sedentary lifestyle and a reduction in masticatory activity [ 26 , 28 , 29 , 30 , 31 ].…”

Section: Introductionmentioning

confidence: 99%

The Sedentary Lifestyle and Masticatory Dysfunction: Time to Review the Contribution to Age-Associated Cognitive Decline and Astrocyte Morphotypes in the Dentate Gyrus

Mendes

Almeida

Falsoni

et al. 2022

IJMS

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As aging and cognitive decline progresses, the impact of a sedentary lifestyle on the appearance of environment-dependent cellular morphologies in the brain becomes more apparent. Sedentary living is also associated with poor oral health, which is known to correlate with the rate of cognitive decline. Here, we will review the evidence for the interplay between mastication and environmental enrichment and assess the impact of each on the structure of the brain. In previous studies, we explored the relationship between behavior and the morphological features of dentate gyrus glial fibrillary acidic protein (GFAP)-positive astrocytes during aging in contrasting environments and in the context of induced masticatory dysfunction. Hierarchical cluster and discriminant analysis of GFAP-positive astrocytes from the dentate gyrus molecular layer revealed that the proportion of AST1 (astrocyte arbors with greater complexity phenotype) and AST2 (lower complexity) are differentially affected by environment, aging and masticatory dysfunction, but the relationship is not straightforward. Here we re-evaluated our previous reconstructions by comparing dorsal and ventral astrocyte morphologies in the dentate gyrus, and we found that morphological complexity was the variable that contributed most to cluster formation across the experimental groups. In general, reducing masticatory activity increases astrocyte morphological complexity, and the effect is most marked in the ventral dentate gyrus, whereas the effect of environment was more marked in the dorsal dentate gyrus. All morphotypes retained their basic structural organization in intact tissue, suggesting that they are subtypes with a non-proliferative astrocyte profile. In summary, the increased complexity of astrocytes in situations where neuronal loss and behavioral deficits are present is counterintuitive, but highlights the need to better understand the role of the astrocyte in these conditions.

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“…Likewise, a reduction in masticatory activity diminishes neurogenesis and the expression of neurotrophic factor brainderived neurotrophic factor (BDNF) receptors in the dentate gyrus, as well as in the CA1 and CA3 regions of the hippocampus (Fukushima-Nakayama et al, 2017). Thus, abnormal masticatory activity impairs morphofunctional features of hippocampus with synaptic dysfunctional activity, suggesting that all life healthy chewing is essential for hippocampal-dependent cognitive function (Piancino et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Sedentary Life and Reduced Mastication Impair Spatial Learning and Memory and Differentially Affect Dentate Gyrus Astrocyte Subtypes in the Aged Mice

et al. 2021

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To explore the impact of reduced mastication and a sedentary lifestyle on spatial learning and memory in the aged mice, as well as on the morphology of astrocytes in the molecular layer of dentate gyrus (MolDG), different masticatory regimens were imposed. Control mice received a pellet-type hard diet, while the reduced masticatory activity group received a pellet diet followed by a powdered diet, and the masticatory rehabilitation group received a pellet diet, followed by powder diet and then a pellet again. To mimic sedentary or active lifestyles, mice were housed in an impoverished environment of standard cages or in an enriched environment. The Morris Water Maze (MWM) test showed that masticatory-deprived group, regardless of environment, was not able to learn and remember the hidden platform location, but masticatory rehabilitation combined with enriched environment recovered such disabilities. Microscopic three-dimensional reconstructions of 1,800 glial fibrillary acidic protein (GFAP)-immunolabeled astrocytes from the external third of the MolDG were generated using a stereological systematic and random sampling approach. Hierarchical cluster analysis allowed the characterization into two main groups of astrocytes with greater and lower morphological complexities, respectively, AST1 and AST2. When compared to compared to the hard diet group subjected to impoverished environment, deprived animals maintained in the same environment for 6 months showed remarkable shrinkage of astrocyte branches. However, the long-term environmental enrichment (18-month-old) applied to the deprived group reversed the shrinkage effect, with significant increase in the morphological complexity of AST1 and AST2, when in an impoverished or enriched environment. During housing under enriched environment, complexity of branches of AST1 and AST2 was reduced by the powder diet (pellet followed by powder regimes) in young but not in old mice, where it was reversed by pellet diet (pellet followed by powder and pellet regime again). The same was not true for mice housed under impoverished environment. Interestingly, we were unable to find any correlation between MWM data and astrocyte morphological changes. Our findings indicate that both young and aged mice subjected to environmental enrichment, and under normal or rehabilitated masticatory activity, preserve spatial learning and memory. Nonetheless, data suggest that an impoverished environment and reduced mastication synergize to aggravate age-related cognitive decline; however, the association with morphological diversity of AST1 and AST2 at the MolDG requires further investigation.

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Altered mastication adversely impacts morpho-functional features of the hippocampus: A systematic review on animal studies in three different experimental conditions involving the masticatory function

Cited by 25 publications

References 47 publications

Aβ Accumulation in Vmo Contributes to Masticatory Dysfunction in 5XFAD Mice

Aβ Accumulation in Vmo Contributes to Masticatory Dysfunction in 5XFAD Mice

The Sedentary Lifestyle and Masticatory Dysfunction: Time to Review the Contribution to Age-Associated Cognitive Decline and Astrocyte Morphotypes in the Dentate Gyrus

Sedentary Life and Reduced Mastication Impair Spatial Learning and Memory and Differentially Affect Dentate Gyrus Astrocyte Subtypes in the Aged Mice

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