Neutrophil responses to injury or inflammation impair peripheral gustatory function

Abstract The adult peripheral taste system is capable of extensive functional plasticity after injury. Sectioning the chorda tympani (CT), a primary sensory afferent nerve, elicits transient changes in the uninjured, contralateral population of taste receptor cells. Remarkably, the deficits are spec...

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Bibliographic Details
Published in:Neuroscience 2010-05, Vol.167 (3), p.894-908
Main Authors: Steen, P.W, Shi, L, He, L, McCluskey, L.P
Format: Article
Language:English
Subjects:
Action Potentials - physiology
Animals
Biological and medical sciences
Chemotaxis, Leukocyte - physiology
Chorda Tympani Nerve - injuries
Chorda Tympani Nerve - physiopathology
Denervation
Facial Nerve Injuries - complications
Facial Nerve Injuries - physiopathology
Female
Food, Formulated
Fundamental and applied biological sciences. Psychology
Inflammation - complications
Inflammation - physiopathology
Mouth - cytology
Mouth - innervation
Mouth - physiopathology
Neurology
Neutrophils - physiology
Olfactory system and olfaction. Gustatory system and gustation
Rats
Rats, Sprague-Dawley
Sodium - deficiency
Sodium Channels - metabolism
Taste - physiology
Taste Buds - physiopathology
Taste Disorders - etiology
Taste Disorders - physiopathology
Tongue - cytology
Tongue - innervation
Tongue - physiopathology
Vertebrates: nervous system and sense organs
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Summary:Abstract The adult peripheral taste system is capable of extensive functional plasticity after injury. Sectioning the chorda tympani (CT), a primary sensory afferent nerve, elicits transient changes in the uninjured, contralateral population of taste receptor cells. Remarkably, the deficits are specific to the sodium transduction pathway. Normal function is quickly restored in the intact nerve, in parallel with an influx of macrophages to both the denervated and uninjured sides of the tongue. However, changing the dietary environment by restricting sodium blocks the macrophage response and prolongs functional alterations. Since the functional deficits occur before macrophages are present in the peripheral taste system, we hypothesized that neutrophils play a role in modulating neural responses in the intact CT. First, the dynamics of the neutrophil response to nerve injury were analyzed in control-fed and sodium-deficient rats. Nerve sectioning briefly increased the number of neutrophils on both the denervated and uninjured sides of the tongue. The low-sodium diet amplified and extended the bilateral neutrophil response to injury, in parallel with the persistent changes in sodium taste function. To test the impact of neutrophils on taste function, we depleted these cells prior to nerve sectioning and recorded neural responses from the intact CT. This treatment restored normal sodium responses in the uninjured nerve. Moreover, recruiting neutrophils to the tongue induced deficits in sodium taste function in both CT nerves. Neutrophils play a critical role in ongoing inflammatory responses in the oral cavity, and may induce changes in taste perception. We also suggest that balanced neutrophil and macrophage responses enable normal neural responses after neural injury.
ISSN:0306-4522
1873-7544
DOI:10.1016/j.neuroscience.2010.02.056