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Front. Neurosci. | doi: 10.3389/fnins.2018.00265

Encoding of sucrose’s palatability in the nucleus accumbens shell and its modulation by exteroceptive auditory cues

  • 1Department of Pharmacology, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Mexico
  • 2Department of Neurobiology, School of Medicine, Duke University, United States

Although the palatability of sucrose is the primary reason for why it is over consumed, it is not well understood how it is encoded in the nucleus accumbens shell (NAcSh), a brain region involved in reward, feeding, and sensory/motor transformations. Similarly, untouched are issues regarding how an external auditory stimulus affects sucrose palatability and, in the NAcSh, the neuronal correlates of this behavior. To address these questions in behaving rats, we investigated how food-related auditory cues modulate sucrose’s palatability. The goals are to determine whether NAcSh neuronal responses would track sucrose’s palatability (as measured by the increase in hedonically positive oromotor responses lick rate), sucrose concentration, and how it processes auditory information. Using brief-access tests, we found that sucrose’s palatability was enhanced by exteroceptive auditory cues that signal the start and the end of a reward epoch. With only the start cue the rejection of water was accelerated, and the sucrose/water ratio was enhanced, indicating greater palatability. However, the start cue also fragmented licking patterns and decreased caloric intake. In the presence of both start and stop cues, the animals fed continuously and increased their caloric intake. Analysis of the licking microstructure confirmed that auditory cues (either signaling the start alone or start/stop) enhanced sucrose’s oromotor-palatability responses. Recordings of extracellular single-unit activity identified several distinct populations of NAcSh responses that tracked either the sucrose palatability responses or the sucrose concentrations by increasing or decreasing their activity. Another neural population fired synchronously with licking and exhibited an enhancement in their coherence with increasing sucrose concentrations. The population of NAcSh’s Palatability-related and Lick-Inactive neurons were the most important for decoding sucrose’s palatability. Only the Lick-Inactive neurons were phasically activated by both auditory cues and may play a sentinel role monitoring relevant auditory cues to increase caloric intake and sucrose’s palatability. In summary, we found that auditory cues that signal the availability of sucrose modulate its palatability and caloric intake in a task dependent-manner and had neural correlates in the NAcSh. These findings show that exteroceptive cues associated with feeding may enhance positive hedonic oromotor-responses elicited by sucrose’s palatability.

Keywords: Sucrose palatability, auditory cues, Taste, feeding, licking, Obesity

Received: 07 Oct 2017; Accepted: 05 Apr 2018.

Edited by:

Benjamin Boutrel, Laboratory on the Neurobiology of Addictive and Eating Disorders - CHUV (Department of Psychiatry), Switzerland

Reviewed by:

Gwenaël Labouèbe, Université de Lausanne, Switzerland
Patricia M. Di Lorenzo, Binghamton University, United States
Susan P. Travers, The Ohio State University, United States
Alexandre Picard, Université de Lausanne, Switzerland  

Copyright: © 2018 Villavicencio, Moreno, Simon and Gutierrez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Ranier Gutierrez, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Department of Pharmacology, Av. IPN No 2508, México City, 07360, Mexico, ranier@cinvestav.mx