Monosodium Glutamate but not Linoleic Acid Differentially Activates Gustatory Neurons in the Rat Geniculate Ganglion

Abstract

To date, only one study has examined responses to monosodium glutamate (MSG) from gustatory neurons in the rat geniculate ganglion and none to free fatty acids. Accordingly, we recorded single-cell responses from geniculate ganglion gustatory neurons in anesthetized male rats to MSG and linoleic acid (LA), as well as to sucrose, NaCl, citric acid, and quinine hydrochloride. None of the 52 neurons responded to any LA concentration. In contrast, both narrowly tuned groups of gustatory neurons (sucrose specialists and NaCl specialists) responded to MSG, as did 2 of the broadly tuned groups (NaCl generalist(I) and acid generalists). NaCl-generalist(II) neurons responded only to the highest MSG concentration and only at low rates. No neuron type responded best to MSG; rather, responses to 0.1 M MSG were significantly less than those to NaCl for Na(+) -sensitive neurons and to sucrose for sucrose specialists. Interestingly, most Na(+) -sensitive neurons responded to 0.3 M MSG at levels comparable with those to 0.1 M NaCl, whereas sucrose specialists responded to 0.1 M MSG despite being unresponsive to NaCl. These results suggest that the stimulatory effect of MSG involves activation of sweet- or salt-sensitive receptors. We propose that glutamate underlies the MSG response of sucrose specialists, whereas Na(+) -sensitive neurons respond to the sodium cation. For the latter neuron groups, the large glutamate anion may reduce the driving force for sodium through epithelial channels on taste cell membranes. The observed concentration-dependent responses are consistent with this idea, as are cross-adaptation studies using 0.1 M concentrations of MSG and NaCl in subsets of these Na(+) -sensitive neurons.

Gustatory neural responses to umami stimuli in the parabrachial nucleus of C57BL/6J mice

“…Conditioned taste aversion studies in rats are consistent with the notion that MSG may be perceived as a salty-sweet amalgamation (Yamamoto et al 1985;1991;Chaudhari et al 1996;Stapleton et al 1999). Physiologically, single chorda tympani (CT) fibers, geniculate ganglion neurons, and central taste neurons responsive to MSG also tend to possess high sensitivity to sucrose and NaCl in the rat (Sato et al 1970;Yamamoto et al 1985;Adachi and Aoyama 1991;Nishijo et al 1991;Breza et al 2007). In contrast to rats, there is evidence that mice can behaviorally discriminate the taste of MSG from stimuli representing the four traditional basic tastes (Ninomiya and Funakoshi 1989a;Nakashima et al 2001;Yamamoto et al 2009; but see Murata et al 2009).…”

Acetic acid modulates spike rate and spike latency to salt in peripheral gustatory neurons of rats

“…Of the eight neurons tested, three responded significantly less (suppression) and two responded significantly more (synergy/enhancement) to the mixtures compared with the sum of the component responses. Thus acid-sensitive generalist neurons are not a homogeneous population as observed previously (Breza et al 2006(Breza et al , 2007Lundy and Contreras 1999).…”

“…We found the insensitivity of NaCl specialists to acid stimuli applied to acetic acid over a broad concentration range that extended 1 log unit higher than the 0.01 M concentration of citric acid (Breza and Contreras 2012;Breza et al 2007;2006;Breza et al 2010;Lawhern et al 2011) and HCl (Lundy and Contreras 1999) used previously. In contrast, acid generalists responded in a concentration-dependent manner to all acetic acid concentrations from 0.003 to 0.1 M. As acetic acid concentration increased, the acid generalist's spike rate response increased and its response latency decreased.…”

“…For single-unit experiments (n ϭ 11), rats were placed in a stereotaxic instrument with blunt ear bars. The geniculate ganglion was exposed with a dorsal approach (Breza and Contreras 2012;Breza et al 2006Breza et al , 2007Breza et al , 2010Lawhern et al 2011;Lundy and Contreras 1999). Each rat's tongue was gently extended and held in place by a suture attached to its ventral surface.…”

“…Although the inhibitory responses to acetic acidNaCl mixtures in NaCl specialists were not as robust as those predicted by whole nerve responses (9% reduction in NaCl specialists vs. 21% reduction in CT), the whole nerve is indeed a summated response and many factors need to be considered. For example, it is possible that there are more NaCl specialists than acid generalists in the rat CT. Over the past 12 years, we have sampled from more NaCl specialists than acid generalists (Breza and Contreras 2012;Breza et al 2006Breza et al , 2007Breza et al , 2010Lawhern et al 2011;Lundy and Contreras 1999). Together, these samples estimate that there are greater than one-third more NaCl specialists than acid generalist in the rat CT nerve, which may contribute to a larger portion of the summated signal.…”