Elsevier

Physiology & Behavior

Volume 105, Issue 2, 18 January 2012, Pages 595-606
Physiology & Behavior

Pontine and thalamic influences on fluid rewards: III. Anticipatory contrast for sucrose and corn oil

https://doi.org/10.1016/j.physbeh.2011.06.008Get rights and content

Abstract

An anticipatory contrast effect (ACE) occurs when, across daily trials, an animal comes to respond less than normally to a first stimulus when it is followed shortly by a second, more preferred solution. Classically, ACE is studied using a low (L) concentration of saccharin or sucrose, followed by access to a higher (H) concentration of sucrose. Subjects in the control condition have two bouts of access to the weaker solution presented on the same schedule. The ACE is measured by the difference in intake of the first bout low solution between subjects in the low–low (L–L) vs. the low–high (L–H) conditions. Here we used this paradigm with sham feeding rats and determined that nutritional feedback was unnecessary for the development of ACE with two concentrations of sucrose or with two concentrations of corn oil. Next we showed that ibotenic acid lesions centered in the orosensory thalamus spared ACEs for both sucrose and corn oil. In contrast, lesions of the pontine parabrachial nuclei (PBN), the second central relay for taste in the rat, disrupted ACEs for both sucrose and corn oil. Although the sensory modalities needed for the oral detection of fats remain controversial, it appears that the PBN is involved in processing the comparison of disparate concentrations of sucrose and oil reward.

Highlights

► Sham feeding rats show ACEs for both sucrose and corn oil. ► Lesions of the parabrachial nucleus eliminate ACE for both sucrose and corn oil. ► Lesions of the thalamic orosensory area spare sucrose and corn oil ACE. ► Both control and TOAx rats express an ACE, but the pattern between the two differs.

Introduction

In the previous two articles in this series, the results showed a dissociation in the role of the gustatory system in orosensory processing of corn oil. Rats with lesions of the parabrachial nuclei (PBN) exhibited weaker than normal operant responding for corn oil emulsions [1], [2], [28], [29], [30], [31], [32], [34], but learned a condition aversion to corn oil [3]. Similar PBN damage disrupted responding for sucrose in both tasks. Rats with lesions of the thalamic orosensory area (TOA), on the other hand, showed no deficits in responding for sucrose or corn oil during fixed or progressive ratio tasks and they acquired a conditioned aversion to both stimuli. These results did not fully support our initial hypothesis that the gustatory PBN is important for orosensory processing of sucrose but not corn oil, and, conversely, that the TOA is necessary for processing oil but not for sucrose reward.

In the present study, we focused on reward comparison for orosensory sucrose and corn oil using the anticipatory contrast effect (ACE). The same hypothesis was tested, but with respect to relative, rather than absolute, reward value. Again, ACE previously was demonstrated only with real feeding. In order to focus on the orosensory effects of fluid rewards, Experiment 1 first demonstrated that intact sham feeding rats can exhibit ACE for sucrose and corn oil, the latter of which has never been tested. Experiment 2 tested whether PBN lesions block an ACE for sucrose and TOA damage interferes with the parallel effect for oil. A preliminary report of these results was presented at the annual meeting of the Society for the Study of Ingestive Behavior in 2009.

Section snippets

Experiment 1: anticipatory contrast effects in sham feeding rats

Ingestion of one preferred sapid stimulus is affected by the relative value of another such stimulus presented closely in time. This change in responding as a function of experience is referred to as a contrast effect [4]. An anticipatory contrast effect develops when rats suppress intake of a weak stimulus, e.g., 0.15% saccharin or 0.06 M sucrose, as it comes to predict the future availability of a stronger, more preferred, stimulus, e.g., 1.0 M sucrose. The comparison is with intake by rats

Experiment 2: anticipatory contrast effects in lesioned rats

The original hypothesis is that sensory processing of corn oil requires the intraoral trigeminal somatosensory system that bypasses the PBN and projects directly to the thalamus [20]. This hypothesis has been tested after lesions of the PBN and TOA using operant tasks and conditioned taste aversion (CTA). The results provide some support for the hypothesis in that PBN lesions eliminated learning a conditioned aversion to sucrose but not to 100% corn oil and they eliminated operant responding

Summary of parabrachial and thalamic lesion effects

Operant responding, CTA, and ACE were examined in PBNx and TOAx rats to test whether sucrose and corn oil are processed through the same or different orosensory pathways. A summary of the data appears in Table 1. The results confirm that, when sucrose is the stimulus, rats with PBN lesions fail to respond in operant tasks, to learn a CTA, or to demonstrate an ACE. The same PBNx rats, however, licked corn oil emulsions normally during free access. They learned operant tasks for oil emulsions but

Acknowledgments

The authors thank Dr. Chris Freet for writing the computer programs for the ACE experiments, Han Li for making brain lesions, and Kathy Matayas and Nellie Horvath for histology. This study was supported by grant DK079182, DC00240, and DA012473 from the National Institute of Health, as well as a PA State Tobacco Settlement Award.

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