Alcohol Activates a Sucrose-Responsive Gustatory Neural Pathway

Abstract

Lemon, Christian H., Susan M. Brasser, David V. Smith. Alcohol activates a sucrose-responsive gustatory neural pathway. J Neurophysiol 92: 536 -544, 2004. First published February 25, 2004 10.1152/jn.00097.2004. A strong positive association exists between the ingestion of alcohol and sweet-tasting solutions. The neural mechanisms underlying this relationship are unknown, although recent data suggest that gustatory substrates are involved. Here, we examined the role of sweet taste receptors and central neural circuits for sugar taste in the gustatory processing of ethanol. Taste responses to ethanol (3, 5, 10, 15, 25, and 40% vol/vol) and stimuli of different taste qualities (e.g., sucrose, NaCl, HCl, and quinine-HCl) were recorded from neurons of the nucleus of the solitary tract in anesthetized rats prior to and after oral application of the sweet receptor blocker gurmarin. The magnitude of ethanol-evoked activity was compared between sucroseresponsive (n ϭ 21) and sucrose-unresponsive (n ϭ 20) neurons and the central neural representation of ethanol taste was explored using multivariate analysis. Ethanol produced robust concentration-dependent responses in sucrose-responsive neurons that were dramatically larger than those in sucrose-unresponsive cells. Gurmarin selectively and similarly inhibited ethanol and sucrose responses, leaving NaCl, HCl, and quinine responses unaltered. Across-neuron patterns of response to ethanol were most similar to those evoked by sucrose, becoming increasingly more so as the ethanol concentration was raised. Results implicate taste receptors for sucrose as candidate receptors for ethanol and reveal that alcohol and sugar taste are represented similarly by gustatory activity in the CNS. These findings have important implications for the sensory and reward properties of alcohol.

Voluntary ethanol consumption in 22 inbred mouse strains

“…It should be noted that some strains may respond to adulteration of ethanol solutions with other compounds by increasing intake, as D2 mice have been shown to increase their intake of and two-bottle preference for ethanol when it was added to non-alcoholic beer (Grisel et al, 2007). Finally, a recent study has shown that in rats, sucrose-responsive neurons in the nucleus of the solitary tract showed a much larger, concentration-dependent response to an oral ethanol stimulus than sucroseunresponsive cells (Lemon et al, 2004). This suggests a possible physiological basis for differential modulation of ethanol's tase-related cue properties in saccharin preferring versus non-preferring genotypes.…”

Differential neural representation of oral ethanol by central taste-sensitive neurons in ethanol-preferring and genetically heterogeneous rats

“…Rodents also perceive similarities in the oral properties of ethanol and sweet-tasting stimuli, as conditioned aversions to the orosensory features of ethanol generalize to sucrose mixtures in rats (Di Lorenzo et al 1986;Kiefer et al 1990; Kiefer and Lawrence 1988;Kiefer and Mahadevan 1993) and taste aversions to sucrose alone generalize to ethanol in C57BL/6J (B6) mice (Blizard and McClearn 2000). Furthermore, neurophysiological studies across multiple species have demonstrated positive associations between responses to oral alcohol and sweet stimuli in peripheral gustatory fibers (Danilova and Hellekant 2000;Diamant et al 1963;Hellekant et al 1997;Sako and Yamamoto 1999) and central taste-sensitive neurons (Brasser et al 2010;Di Lorenzo et al 1986;Lemon et al 2004;Lemon and Smith 2005). Selective antagonism of sweet taste receptors also directly suppresses oral responses to alcohol by gustatory-sensitive sensory neurons (Lemon et al 2004;Sako and Yamamoto 1999), implicating sweet receptors in the transduction of alcohol taste.…”

Influence of Response Variability on the Coding Performance of Central Gustatory Neurons

“…In phase 1, we analyze taste responses from a large number of NST neurons, some drawn from our files (Lemon et al, , 2004Lemon and Di Lorenzo, 2002) and others newly recorded. All neurons were sampled from naive adult male Sprague Dawley rats under urethane anesthesia.…”

“…All neurons were sampled from naive adult male Sprague Dawley rats under urethane anesthesia. For newly acquired cells, details of the surgical and recording procedures have been reported previously (Lemon et al, , 2004Lemon and Smith, 2005). Briefly, conventional single-unit electrophysiological methods were used to record trains of action potentials from gustatory neurons in the NST.…”

“…Our dataset was composed of 162 rat NST neurons, 122 drawn from our files (76 cells from Lemon et al, 2003Lemon et al, , 2004; 46 cells from Lemon and Di Lorenzo 2002; used here with the consent of P. M. Di Lorenzo, Binghamton University, Binghamton, NY), and 40 cells newly recorded from 28 rats. On the basis of the number of spikes evoked by the four stimuli, 40 neurons responded best to sucrose, 76 responded best to NaCl, 44 responded best to HCl, and two quinine-best neurons were included in our sample.…”