It hurts so good: oral irritation by spices and carbonated drinks and the underlying neural mechanisms

Abstract

This paper reviews neurophysiological and psychological studies of oral irritation elicited by chemicals in spicy foods and carbonated drinks. Oral irritant, thermal and textural sensations are conveyed to the brain by the trigeminal pathway, which is separate from the gustatory and olfactory systems. In humans, repetitive application of capsaicin, citric acid, or concentrated NaCl elicits oral irritation that grows in intensity across trials (“sensitization”). After a rest period, reapplication elicits less irritation (“self-desensitization”), but if given recurrently will eventually evoke a progressive rise in irritation (“stimulus-induced recovery”=SIR). In neurophysiological recordings from neurons in the trigeminal subnucleus caudalis (Vc), the first relay in the pathway for oral somatosensation, these irritants elicit a similar pattern of progressively increasing firing, followed after a rest by self-desensitization and SIR. In contrast, nicotine, menthol or mustard oil elicit irritation that decreases across trials (“desensitization”), a pattern also observed in Vc neuronal responses to these irritants. Carbonated water elicits an oral tingling sensation and excites Vc neurons largely through its conversion to carbonic acid. The good correspondence in temporal profiles for perception and neuronal activity supports a role for Vc neurons in the mediation of oral irritation. Finally, the development of preference for foods containing aversive chemicals is addressed. This may involve mere exposure, social reinforcement, the “thrill” of the strong sensation, or physiological reinforcement associated with satiety or release of endorphins by the painful stimulus.