Reinnervation of cross-regenerated gustatory nerve fibers into amiloride-sensitive and amiloride-insensitive taste receptor cells

Abstract

Single nerve fiber responses to NaCl and their inhibition by amiloride were compared among the chorda tympani (CT) and glossopharyngeal (IXth), and their cross-regenerated nerves in the C57BL͞KsJ mice. The CT nerve innervating the anterior part of the tongue contained approximately equal numbers of two types of NaCl-responsive neurons; one type showed strong suppression of NaCl responses by amiloride [amiloride-sensitive (AS) type], and the other type showed only weak or no suppression of NaCl responses by amiloride [amiloride-insensitive (AI) type]. In contrast, the IXth nerve innervating the posterior part of the tongue has almost exclusively the AI type. This relative abundance of the AS and AI types of fibers was not altered by cross-regeneration of the two gustatory nerves into the reverse tongue regions. This suggests that regenerated taste axons selectively recouple with the appropriate type of receptor cell whether they innervate the front or the back of the tongue. Such selective synapse reformation may help explain the stability of response profiles of taste neurons during continual receptor cell turnover.Taste receptor cells turn over with an average life span of about 10 days in mammals (1-3). The replacement of receptor cells is accompanied by continuing synaptic reconnection between newly formed taste cells and first-order gustatory fibers. Little is known about how a stable sensory code for taste quality is maintained under such continual synaptic reconnection. More than 20 years ago it was observed (4) that branches of a single taste fiber have very similar relative responsiveness to taste stimuli, implying that a given class of taste axons maintains a persistent association with its corresponding class of receptor cells. However, since then little additional evidence for this possibility has been reported. This may largely be because of the lack of a selective taste modifier to identify particular taste receptor types that taste axons innervate.Recently, it was found in many mammals that a sodium transport blocker, amiloride, specifically inhibits taste responses to NaCl, but does not suppress responses to sweet, sour, and bitter substances (5-7). Using this specific NaCl response inhibitor, subsequent neural response analyses in rodents suggested the existence of two subtypes of receptor mechanisms for NaCl: amiloride-sensitive and amilorideinsensitive. These two subtypes were localized in taste buds in fungiform papillae located on the anterior two-thirds of the tongue, which are innervated by the chorda tympani (CT) nerve (8-10). In marked contrast, it was also reported that in C57BL͞KsJ mice (11) and SHR and WKY rats (12) the taste buds in vallate and foliate papillae located on the posterior one-third of the tongue, innervated by the glossopharyngeal (IXth) nerve, may lack the amiloride-sensitive subtype.It has been shown that transection of the gustatory nerves (the CT and IXth nerves) results in degeneration of taste buds within 7 days, and the taste buds reappear after regenerati...

Taste Preference for Fatty Acids Is Mediated by GPR40 and GPR120

“…Whole nerve responses were integrated with a time constant of 1.0 s and recorded on a computer for later analysis using PowerLab system (PowerLab/sp4; ADInstruments). (For more details, see Ninomiya, 1998;Kawai et al, 2000. ) The solutions used to stimulate the tongue are oleic acid, linolenic acid, docosahexaenoic acid (DHA) 1 mM, 3 mM, 10 mM each, lauric acid and linoleic acid 1 mM, 3 mM, 10 mM, 30 mM, 100 mM each, 0.1%, 0.3% and 1% Ultralec, a mix of phosphatidyl choline, phosphatidyl ethanolamine and phosphatidyl inositol, 0.1%, 0.3%, 1% mineral oil, 0.1 mM, 1 mM, 10 mM, 20 mM, 50 mM denatonium benzoate with or without 55 M linoleic acid and 33 M oleic acid, 10 mM, 30 mM, 100 mM, 300 mM, 1 M NaCl, 1 mM, 3 mM, 10 mM HCl, 10 mM, 30 mM, 100 mM, 300 mM, 1 M monopotassium glutamate, 10 mM, 30 mM, 100 mM, 300 mM, 500 mM,1 M sucrose and 3%, 5% and 8% ethanol.…”

“…To determine whether GPR40 and GPR120 are involved in the detection of fat by the gustatory system, we recorded whole nerve responses of the mouse taste nerves (Ninomiya, 1998;Kawai et al, 2000) to fatty acids ( Fig. 4; supplemental Tables S4, S5, supplemental Fig.…”

Multiple Umami Receptors and Their Variants in Human and Mice

“…In previous studies, MSG-responsive single fibers in the two taste nerves were classified into 4 groups based on a cluster analysis, S-type, 6,22) M-type, 23,24) N-type and E-type (or H-type). [25][26][27][28][29] S-type fibers are characterized by their best response to sucrose and large synergism between MSG and IMP. 6,22) M-type fibers exhibited best responses to umami stimuli and showed small synergism.…”

Modulation of Taste Responsiveness by Angiotensin II

“…Subsequent studies using amiloride in rodents suggested that two distinct components underlie cellular sensitivity to NaCl: one that is amiloride-sensitive and another that is amilorideinsensitive. Both amiloride-sensitive and -insensitive components are observed in taste buds in fungiform papillae located on the anterior two-thirds of the tongue; these papillae are innervated by the chorda tympani (CT) nerve (Ninomiya and Funakoshi, 1988, Ninomiya, 1998, Yasumatsu, 2003. On the other hand, the taste buds in circumvallate and foliate papillae located on the posterior one-third of the tongue are innervated by the glossopharyngeal (IXth) nerve and have amiloride-insensitive components (almost no amiloride-sensitive response) (Ninomiya et al, 1991, Formaker andHill, 1991).…”

“…Salty taste transduction occurs through amiloride-sensitive and -insensitive sodium transport pathways (Ninomiya and Funakoshi, 1988, Ninomiya, 1998, Yasumatsu, 2003 tastants. The effects of Ang II on nerve responses were inhibited by pretreatment with a specific antagonist of AT1, CV11974 (Kinugawa et al, 1993).…”