Sweet orosensation induces Arc expression in dorsal hippocampal CA1 neurons in an experience-dependent manner

Hippocampus. 2016 Mar;26(3):405-13. doi: 10.1002/hipo.22532. Epub 2015 Nov 5.

Abstract

There is limited knowledge regarding how the brain controls the timing of meals. Similarly, there is a large gap in our understanding of how top-down cognitive processes, such as memory influence energy intake. We hypothesize that dorsal hippocampal (dHC) neurons, which are critical for episodic memory, form a memory of a meal and inhibit meal onset during the postprandial period. In support, we showed previously that reversible inactivation of these neurons during the period following a sucrose meal accelerates the onset of the next meal. If dHC neurons form a memory of a meal, then consumption should induce synaptic plasticity in dHC neurons. To test this, we determined (1) whether a sucrose meal increases the expression of the synaptic plasticity marker activity-regulated cytoskeleton-associated protein (Arc) in dHC CA1 neurons, (2) whether previous experience with sucrose influences sucrose-induced Arc expression, and (3) whether the orosensory stimulation produced by the noncaloric sweetener saccharin is sufficient to induce Arc expression. Male Sprague-Dawley rats were trained to consume a sweetened solution at a scheduled time daily. On the experimental day, they were given a solution for 7 min, euthanized, and then fluorescence in situ hybridization procedures were used to measure meal-induced Arc mRNA. Compared to caged control rats, Arc expression was significantly higher in rats that consumed sucrose or saccharin. Interestingly, rats given additional experience with sucrose had less Arc expression than rats with less sucrose experience, even though both groups consumed similar amounts on the experimental day. Thus, this study is the first to suggest that orosensory stimulation produced by consuming a sweetened solution and possibly the hedonic value of that sweet stimulation induces synaptic plasticity in dHC CA1 neurons in an experience-dependent manner. Collectively, these findings are consistent with our hypothesis that dHC neurons form a memory of a meal.

Keywords: activity-regulated cytoskeleton-associated protein; immediate early gene; postprandial; saccharin; sucrose.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • AIDS-Related Complex / genetics
  • AIDS-Related Complex / metabolism*
  • Afferent Pathways / drug effects
  • Afferent Pathways / physiology
  • Analysis of Variance
  • Animals
  • CA1 Region, Hippocampal / cytology*
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / physiology
  • Male
  • Neurons / drug effects*
  • Neurons / physiology
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Saccharin / pharmacology
  • Sucrose / pharmacology
  • Sweetening Agents / pharmacology*
  • Taste / drug effects
  • Taste / physiology*
  • Teaching
  • Time Factors

Substances

  • RNA, Messenger
  • Sweetening Agents
  • Sucrose
  • Saccharin