On the role of the mouth and gut in the control of saccharin and sugar intake: A reexamination of the sham-feeding preparation

doi:10.1016/0361-9230(85)90106-6

Brain Research Bulletin

Volume 14, Issue 6, June 1985, Pages 569-576

https://doi.org/10.1016/0361-9230(85)90106-6 Get rights and content

Abstract

Adult female rats, each fitted with a gastric fistula, were tested for their “normal-feeding” (fistula closed) and “sham-feeding” (fistula open) response to saccharin and sugar solutions under a variety of conditions. When hungry, rats consumed no more of a 0.2% saccharin solution with their fistula open than they did with their fistula closed. Increasing or decreasing the saccharin concentration did not increase the amount of solution sham fed, but adding a small amount of glucose (3%) to the saccharin solution did increase the amount sham fed. Thirsty rats, unlike hungry rats, significantly increased their 0.2% saccharin solution intake when tested with an open fistula. When tested with a 32% glucose solution, hungry rats consumed up to six times more solution with their fistula open than with their fistula closed. The hungry rats also sham fed significantly more of the 32% glucose solution than of the 0.2% saccharin solution or 0.2% saccharin + 3% glucose solution. Sham-feeding of a 32% sucrose solution significantly elevated blood glucose levels, but blocking this effect by adding acarbose, a drug that inhibits sucrose digestion, did not reduce the amount of solution sham fed. Several possible explanations for the differential sham-feeding response to saccharin and sugar solutions are discussed.

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Episodic meal-related memories provide the brain with a powerful mechanism for tracking and controlling eating behavior because they contain a detailed record of recent energy intake that likely outlasts the physiological signals generated by feeding bouts. This review briefly summarizes evidence from human participants showing that episodic meal-related memory limits later eating behavior and then describes our research aimed at investigating whether hippocampal neurons mediate the inhibitory effects of meal-related memory on subsequent feeding. Our approach has been inspired by pioneering work conducted by Ivan Izquierdo and others who used posttraining manipulations to investigate memory consolidation. This review describes the rationale and value of posttraining manipulations, how Izquierdo used them to demonstrate that dorsal hippocampal (dHC) neurons are critical for memory consolidation, and how we have adapted this strategy to investigate whether dHC neurons are necessary for mnemonic control of energy intake. I describe our evidence showing that ingestion activates the molecular processes necessary for synaptic plasticity and memory during the early postprandial period, when the memory of the meal would be undergoing consolidation, and then summarize our findings showing that neural activity in dHC neurons is critical during the early postprandial period for limiting future intake. Collectively, our evidence supports the hypothesis that dHC neurons mediate the inhibitory effects of ingestion-related memory on future intake and demonstrates that post-experience memory modulation is not confined to artificial laboratory memory tasks.
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Citation Excerpt :
In these experiments, animals are given limited exposure to saccharin to reduce the likelihood of any conditioned responses to the taste. Under such conditions, saccharin has minimal postingestive consequences (Foletto et al., 2016; Mook et al., 1980; Renwick, 1985, 1986; Sclafani and Nissenbaum, 1985) and unlike sucrose, saccharin meal size and meal frequency are controlled primarily by oropharyngeal satiety (Kushner and Mook, 1984; Mook et al., 1980, 1981; Renwick, 1985, 1986; Sclafani and Nissenbaum, 1985). Nonetheless, the possibility remains that dHC inhibition disrupts saccharin intake by interfering with the processing of any mechanical stimulation produced by the saccharin solution in the gut (Waise et al., 2018).
This paper reviews evidence demonstrating a bidirectional relationship between memory and eating in humans and rodents. In humans, amnesia is associated with impaired processing of hunger and satiety cues, disrupted memory of recent meals, and overconsumption. In healthy participants, meal-related memory limits subsequent ingestive behavior and obesity is associated with impaired memory and disturbances in the hippocampus. Evidence from rodents suggests that dorsal hippocampal neural activity contributes to the ability of meal-related memory to control future intake, that endocrine and neuropeptide systems act in the ventral hippocampus to provide cues regarding energy status and regulate learned aspects of eating, and that consumption of hypercaloric diets and obesity disrupt these processes. Collectively, this evidence indicates that diet-induced obesity may be caused and/or maintained, at least in part, by a vicious cycle wherein excess intake disrupts hippocampal functioning, which further increases intake. This perspective may advance our understanding of how the brain controls eating, the neural mechanisms that contribute to eating-related disorders, and identify how to treat diet-induced obesity.
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Research involving human participants indicates that memories of recently eaten meals limit how much is eaten during subsequent eating episodes; yet, the brain regions that mediate the inhibitory effects of ingestion-related memory on future intake are largely unknown. We hypothesize that dorsal hippocampal (dHC) neurons, which are critical for episodic memories of personal experiences, mediate the inhibitory effects of ingestion-related memory on future intake. Our research program aimed at testing this hypothesis has been influenced in large part by our mentor James McGaugh and his research on posttraining manipulations. In the present study, we used an activity-guided optogenetic approach to test the prediction that if dHC glutamatergic neurons limit future intake through a process that requires memory consolidation, then inhibition should increase subsequent intake when given soon after the end of a meal but delayed inhibition should have no effect. Viral vectors containing CaMKIIα-eArchT3.0-eYFP and fiber optic probes were placed in the dHC of male Sprague-Dawley rats. Compared to intake on a day when no inhibition was given, postmeal inhibition of dHC glutamatergic neurons given for 10 min after the end of a saccharin meal increased the likelihood that rats would consume a second meal 90 min later and significantly increased the amount of saccharin solution consumed during that next meal when the neurons were no longer inhibited. Importantly, delayed inhibition given 80 min after the end of the saccharin meal did not affect subsequent intake of saccharin. Given that saccharin has minimal postingestive gastric consequences, these effects are not likely due to the timing of interoceptive visceral cues generated by the meal. These data show that dHC glutamatergic neural activity is necessary during the early postprandial period for limiting future intake and suggest that these neurons inhibit future intake by consolidating the memory of the preceding meal.
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One explanation for the discrepancy between initial first hour and daily sugar consumption is that intake reached a caloric limit [23], beyond which the intermittent group could not elevate their daily consumption, nor maintain elevated consumption beyond the first hour of solution access. A limit on caloric intake [23] would also explain why sham-fed rats consume large amounts of highly concentrated sucrose solutions that would otherwise not be possible [24–26]. Thus, a caloric limit on consumption may prevent daily access-induced consumption differences from emerging with highly concentrated sucrose solutions.
Rats given intermittent access to 4% (w/v) sucrose solution elevate their consumption of solution relative to rats with continuous access, a difference that does not appear at higher concentrations. Here, we examined the hypothesis that a limit on the intake of sucrose calories prevents rats from demonstrating access-induced differences in consumption of a more concentrated sucrose solution. Energy-replete rats were given every day (ED) or every third day (E3D) access to sucrose solutions adulterated with bitter quinine which reduced solution palatability and consumption levels while intake was measured. In experiment 1, previously collected data were compiled to examine the trajectory of consumption of continuously available 4% sucrose solution which was shown to stabilize by day 3 and then informed group assignment. In experiment 2, daily consumption levels were higher for rats with E3D access to 4% sucrose solution than rats with ED access to the same solution, whereas rats consumed similar amounts of 8% sucrose solution across access schedules. In the first hour of solution availability rats with E3D access showed elevated sucrose solution consumption, relative to rats with ED access, for both 4% and 8% sucrose solution. Upon the addition of quinine (0.005%) sucrose solution consumption decreased and the E3D access group consumed more daily sucrose solution than the ED access group for both 4% and 8% sucrose solution. In experiment 3, four groups of rats were given ED or E3D access to 8% sucrose solution adulterated with 0.0025%, 0.005%, 0.01%, or 0.02% quinine. Quinine adulteration reduced 8% sucrose solution consumption and allowed rats with E3D access to elevate their consumption levels relative to rats with ED access; this effect persisted when all groups were switched to 8% sucrose + 0.02% quinine solution. Thus, daily access-induced consumption differences develop but do not emerge because of a caloric limit on sucrose solution intake. This work underscores the interaction of availability and caloric intake as determinants of sugar consumption and highlights an important distinction between animal models of food addiction and binge eating.
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There is a large gap in our understanding of how top-down cognitive processes, such as memory, influence energy intake. Similarly, there is limited knowledge regarding how the brain controls the timing of meals and meal frequency. Understanding how cognition influences ingestive behavior and how the brain controls meal frequency will provide a more complete explanation of the neural mechanisms that regulate energy intake and may also increase our knowledge of the factors that contribute to diet-induced obesity. We hypothesize that dorsal hippocampal neurons, which are critical for memory of personal experiences (i.e., episodic memory), form a memory of a meal, inhibit meal onset during the period following a meal, and limit the amount ingested at the next meal. In support, we describe evidence from human research suggesting that episodic memory of a meal inhibits intake and review data from human and non-human animals showing that impaired hippocampal function is associated with increased intake. We then describe evidence from our laboratory showing that inactivation of dorsal hippocampal neurons decreases the interval between sucrose meals and increases intake at the next meal. We also describe our evidence suggesting that sweet orosensation is sufficient to induce synaptic plasticity in dorsal hippocampal neurons and raise the possibility that impaired dorsal hippocampal function and episodic memory deficits contribute to the development and/or maintenance of diet-induced obesity. Finally, we raise some critical questions that need to be addressed in future research.

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^☆: Portions of this report were presented at the Society for Neuroscience Meeting, Anaheim, CA, October 1984 and the Satellite Symposium on Neurol and Metabolic Bases of Feeding, Napa, CA, October, 1984. Data from Experiment 5 and additional data have also been published by Sclafani and Nissenbaum [24]. This research was supported by NIH Grant AM 31135 and a grant from the Faculty Research Award Program of the City University of New York. We thank Dr. Kathleen V. Axen for her critical comments on this manuscript.

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On the role of the mouth and gut in the control of saccharin and sugar intake: A reexamination of the sham-feeding preparation☆

Abstract

Prog Neurobiol

Physiol Behav

Physiol Behav

Appetite

Appetite

Physiol Behav

Physiol Behav

Physiol Behav

Conditioned satiety in the rat

J Comp Physiol Psychol

Disappearance of preference and aversions for sapid solutions in rats ingesting untasted fluids

J Comp Physiol Psychol

Saccharin as a sugar surrogate

J Comp Physiol Psychol

Taste as a dipsogenic stimulus

J Comp Physiol Psychol

Sugar infusion can enhance feeding

Science

Blood glucose selectively affects taste-evoked activity in rat nucleus tractus solitarius

Physiol Behav

Gastric modulation of gustatory afferent activity

Physiol Behav

Oral glucose is the prime elicitor of preabsorptive insulin secretion

Am J Physiol

Stimulation of the gerbil's gustatory receptors by saccharin

J Neurosci