Oral sensory alteration affects psycho-emotional behaviors in rats

Abstract

PURPOSE Sensory information plays an important role in determining psycho-emotional behaviors of individuals. This study was conducted to examine the psycho-emotional effects of oral sensory alteration by repeated oral exposure to capsaicin or bilateral transection of the lingual and chorda tympani nerves.

MATERIALS AND METHODS In order to examine the effects of repeated oral capsaicin rats received 1 ml of 0.02% capsaicin into the oral cavity daily, and were subjected to behavioral tests and plasma corticosterone assay following 10 daily administration of capsaicin. And c-Fos immunohistochemistry in the hypothalamic paraventricular nucleus and the brainstem nucleus tractus solitarius was performed one hour after a single exposure to either capsaicin or water. In order to examine the effects of lingual nerve transection, rats were tested for anxiety and depression-related behaviors after either bilateral transection of the lingual and chorda tympani nerves or sham operation. Tissue contents of serotonin and its metabolite in the hippocampus, hypothalamus, and nucleus accumbens were analyzed by high-performance liquid chromatography.

RESULTS The result from the capsaicin-treated rats is as follows. In ambulatory activity test, stereotypy counts and rostral grooming significantly increased, whereas caudal grooming decreased. In elevated plus maze test, not only time spent in open arms but also the rate of entry into open arms were reduced in capsaicin-treated rats. In forced swim test, struggling increased in the experimental group, with the swimming duration decreased. But immobility duration did not differ from the control group. Repeated oral capsaicin did not affect the basal level of plasma corticosterone. However, the stress-induced elevation of plasma corticosterone was prolonged in capsaicin-treated rats. Oral capsaicin exposure significantly increased c-Fos expression not only in the nucleus tractus solitarius but also in the paraventricular nucleus. After bilateral transection of the lingual and chorda tympani nerves, the rats showed the result as follows. Sucrose preference was reduced in comparison with sham rats, suggesting the development of anhedonia, which means decreased pleasure-seeking behavior. Ambulatory activity decreased and anxiety-related behaviors during the activity test increased. Time spent in the open arms during elevated plus maze test decreased, and immobility duration during forced swim test increased. Serotonin level in the hippocampus decreased significantly compared with sham rats.

CONCLUSION Repeated oral exposure to capsaicin increased anxiety-like behaviors in rats, and dysfunction of the hypothalamic-pituitary-adrenal axis may play a role in its pathophysiology. And aberration of oral sensory relay to brain, by bilateral transection of the lingual and chorda tympani nerves, may lead to the development of depression- and anxiety-related disorders, and decreased serotonergic neurotransmission in the hippocampus may play a role in its underlying mechanism. Collectively this study suggests that oral sensory alteration could result in psycho-emotional changes through neural mechanism.