Abstract

The hypoglossal nerve controls tongue movements, and damages of it result in difficulty in mastication and food intake. Mastication has been reported to maintain hippocampus‐dependent cognitive function. This study was conducted to examine the effect of tongue motor loss on the hippocampus‐dependent cognitive function and its underlying mechanism. Male Sprague Dawley rats were subjected to the initial training of Morris water maze task before or after the bilateral transection of hypoglossal nerves (Hx). When the initial training was given before the surgery, the target quadrant dwelling time during the probe test performed at a week after the surgery was significantly reduced in Hx rats relative to sham‐operated controls. When the initial training was given after the surgery, Hx affected the initial and reversal trainings and probe tests. Brain‐derived neurotrophic factor (BDNF) expression, cell numbers and long‐term potentiation (LTP) were examined in the hippocampus on the 10th day, and BrdU and doublecortin staining on the 14th day, after the surgery. Hx decreased the hippocampal BDNF and cells in the CA1/CA3 regions and impaired LTP. BrdU and doublecortin staining was decreased in the dentate gyrus of Hx rats. Results suggest that tongue motor loss impairs hippocampus‐dependent cognitive function, and decreased BDNF expression in the hippocampus may be implicated in its underlying molecular mechanism in relation with decreased neurogenesis/proliferation and impaired LTP.

Highlights

  • Neuronal circuits in taste sensory system are closely connected with other nerve systems for efficient handling of taste information; that is, taste sensory information that reached the nucleus tractus of solitarius is principally relayed to the gustatory cortex via the parabrachial nucleus, and targets other areas of the brain, such as the cerebral cortex, hippocampus, amygdala, hypothalamus and nucleus accumbens for better storage or recall of taste memory or the innate and instinctive response such as preference and aversion [1,2,3]

  • Tissue sections at 40 lm thickness were collected in 0.1 M phosphate buffer with 240-lm intervals between each section and incubated in blocking solution [phosphate-buffered saline (PBS) containing 2% normal horse serum and 0.3% TX-100] for 1 hr, and with rabbit anti-DCX antibody (1:500; ab18723, Abcam) for overnight

  • In the boundary of our knowledge, this is the first report demonstrating that tongue motor loss may affect hippocampus-dependent cognitive function

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Summary

Introduction

Neuronal circuits in taste sensory system are closely connected with other nerve systems for efficient handling of taste information; that is, taste sensory information that reached the nucleus tractus of solitarius is principally relayed to the gustatory cortex via the parabrachial nucleus, and targets other areas of the brain, such as the cerebral cortex, hippocampus, amygdala, hypothalamus and nucleus accumbens for better storage or recall of taste memory or the innate and instinctive response such as preference and aversion [1,2,3]. It is expected that the deprivation or disruption of taste sensory relays may affect the function of those brain regions. Some patients in dental clinics appeal altered taste perception and negative emotion after lingual nerve damages. Oral sensory deficits in rodents with lingual nerve damages increased anxiety- and depression-like behaviours [6] and affected food intake [7]. It has been demonstrated that mastication is of great importance for oral sensory input to the hippocampus for preserving and promoting the cognitive function. Accumulating evidence indicates that mastication maintains hippocampus-dependent cognitive function, and impaired masticatory function, that is, impaired oral motor stimulation, causes morphological and functional alterations of the hippocampus inducing a 2017 The Authors

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