Alan C. Spector

Analytical issues in the evaluation of food deprivation and sucrose concentration effects on the microstructure of licking behavior in the rat.

A microstructural analysis of licking behavior in nondeprived and 23-hr food-deprived rats (n = 15) presented with various sucrose solutions (0.03-1.0 M) in daily single-bottle, 1-hr sessions was conducted. Food deprivation and concentration interacted to increase total licks. The effects of food deprivation and concentration on burst size (BS), burst number (BN), and other parameters varied as a function of the pause criterion (PC; 0.3-100 s) used to define licking bursts. A rationale for selecting a 1-s PC for further analysis is presented. Despite the lack of correlations between temporally contiguous burst and pause combinations, mean BS decreased and pause duration increased as meals progressed. At the 1-s PC, BS increased linearly with concentration, implying that this microstructural parameter is influenced in part by taste. Food deprivation did not affect BS but rather increased BN and proportionally extended the meal duration.

Gastric bypass reduces fat intake and preference

Roux-en-Y gastric bypass is the most effective therapy for morbid obesity. This study investigated how gastric bypass affects intake of and preference for high-fat food in an experimental (rat) study and within a trial setting (human). Proportion of dietary fat in gastric bypass patients was significantly lower 6 yr after surgery compared with patients after vertical-banded gastroplasty (P = 0.046). Gastric bypass reduced total fat and caloric intake (P < 0.001) and increased standard low-fat chow consumption compared with sham controls (P < 0.001) in rats. Compared with sham-operated rats, gastric bypass rats displayed much lower preferences for Intralipid concentrations > 0.5% in an ascending concentration series (0.005%, 0.01%, 0.05%, 0.1%, 0.5%, 1%, 5%) of two-bottle preference tests (P = 0.005). This effect was demonstrated 10 and 200 days after surgery. However, there was no difference in appetitive or consummatory behavior in the brief access test between the two groups (P = 0.71) using similar Intralipid concentrations (0.005% through 5%). Levels of glucagon-like peptide-1 (GLP-1) were increased after gastric bypass as expected. An oral gavage of 1 ml corn oil after saccharin ingestion in gastric bypass rats induced a conditioned taste aversion. These findings suggest that changes in fat preference may contribute to long-term maintained weight loss after gastric bypass. Postingestive effects of high-fat nutrients resulting in conditioned taste aversion may partially explain this observation; the role of GLP-1 in mediating postprandial responses after gastric bypass requires further investigation.

Parabrachial gustatory lesions impair taste aversion learning in rats.

Lesions in the gustatory zone of the parabrachial nuclei (PBN) severely impair acquisition of a conditioned taste aversion (CTA) in rats. To test whether this deficit has a memorial basis, intact rats (n = 15) and rats with PBN lesions (PBNX; n = 10) received seven intraoral taste stimulus infusions (30 s, 0.5 ml) distributed over a 30.5-min period after either LiCl or NaCl injection. This task measures the rapid formation of a CTA and has minimum demands on memory. LiCl-injected intact rats progressively changed their oromotor response profile from one of ingestion to one of aversion. NaCl-injected intact rats did not change their ingestive pattern of responding. In contrast, there was no difference between LiCl- and NaCl-injected PBNX rats. These same PBNX rats failed to avoid licking the taste stimulus when tested in a different paradigm. A simple impairment in a memorial process is not likely the basis for the CTA deficit.

Taste reactivity as a dependent measure of the rapid formation of conditioned taste aversion: a tool for the neural analysis of taste-visceral associations.

Several explanations may account for deficits in the ability of animals to form taste aversions following neural manipulations. These encompass impairments in conditioned stimulus (CS) and unconditioned stimulus (US) processing, conditioned response (CR) measurement, and expression, memory, and taste-visceral integration. A behavioral procedure that aids in the distinction between some of these possibilities is presented. In Experiment 1, 10 rats received seven intraoral (IO) infusions of sucrose (30 s, 0.55 ml) spaced every 5 min starting immediately after the injection of 3.0 mEq/kg of lithium chloride (LiCl). Control rats (n = 12) were treated identically except that they were injected with sodium chloride (NaCl). Oromotor and somatic taste reactivity behaviors were videotaped and analyzed. Lithium-injected rats systematically decreased their ingestive taste reactivity behavior over time, whereas aversive behavior increased. Control rats maintained high and stable levels of ingestive responding and demonstrated virtually no aversive behavior over the 30-min period following sodium injection. Rats were tested several days later for the presence of a conditioned taste aversion (CTA). Rats previously injected with lithium during sucrose infusions demonstrated significantly more aversive behavior than the control group, which demonstrated none. There were no differences in the level of ingestive behavior displayed by the two groups on the CTA test. Experiment 3 revealed that when similarly treated rats were tested for a CTA while in a lithium-induced state, a difference in the ingestive behavior between the two groups was observed. In Experiment 2, naive rats were injected with either NaCl or LiCl but did not receive their first sucrose infusion until 20 min later. These rats also received sucrose infusions at 25 and 30 min postinjection. There were no differences in the taste reactivity behavior displayed by lithium- or sodium-injected rats during any of the sucrose infusions. Collectively, these findings indicate that rats dramatically change their oromotor responses to sucrose during the period following LiCl administration, provided that the infusions start immediately after injection. Furthermore, this time-related behavioral change is predominantly attributable to associative processes. This paradigm can be useful in distinguishing between neural manipulations that affect the establishment of taste-visceral associations from others that affect the animals ability to retain such associations over the commonly employed 24-hr conditioning-test interval.

The Representation of Taste Quality in the Mammalian Nervous System

The process by which the mammalian nervous system represents the features of a sapid stimulus that lead to a perception of taste quality has long been controversial. The labeled-line (sparse coding) view differs from the across-neuron pattern (ensemble) counterpoint in proposing that activity in a given class of neurons is necessary and sufficient to generate a specific taste perception. This article critically reviews molecular, electro-physiological, and behavioral findings that bear on the issue. In the peripheral gustatory system, the authors conclude that most qualities appear to be signaled by labeled lines; however, elements of both types of coding characterize signaling of sodium salts. Given the heterogeneity of neuronal tuning functions in the brain, the central coding mechanism is less clear. Both sparse coding and neuronal ensemble models remain viable possibilities. Furthermore, temporal patterns of discharge could contribute additional information. Ultimately, until specific classes of neurons can be selectively manipulated and perceptual consequences assessed, it will be difficult to go beyond mere correlation and conclusively discern the validity of these coding models.

Linking gustatory neurobiology to behavior in vertebrates.

Technological advances in neuroscience in general, and molecular biology in particular, offer tremendous experimental opportunities for researchers studying the vertebrate gustatory system. Ultimately, however, the neurobiological events must be linked to the taste-related behavior of the animal. Although there has been some promising work in this regard, progress has been hampered by an absence of a unified theoretical framework regarding function, unconfirmed assumptions inherent in many experimental designs, and a misguided predilection for researchers to interpret results from a variety of vertebrate models in the context of human psychophysics. This review article offers a heuristic for the organization of taste function and encourages greater coordination between behavioral and neurobiological approaches to the problem of understanding gustatory processes in the nervous system. The potential power of such coordinated efforts is discussed as well as the possible interpretive pitfalls associated with the neural analysis of gustation.

A Quantitative Comparison of Taste Reactivity Behaviors to Sucrose Before and After Lithium Chloride Pairings: A Unidimensional Account of Palatability

Alterations in the motivation to ingest sucrose can be quantified by measuring the number and type of oral motor and somatic responses (i.e., taste reactivity [TR]) that are elicited by sucrose. In 2 experiments, rats had intraorally infused sucrose paired with LiCl injections for several trials, or they were injected with LiCl and had sucrose infused every 5 min during the 30-min postinjection period (data from Spector, Breslin, & Grill, 1988). In both experiments, ingestive TR responses decreased, whereas aversive TR responses increased over trials. Individual response components that comprise the ingestive and aversive categories followed the same trends of increase or decrease but changed at different rates as a function of number of trials or exposures. Overall, the array of response components could be projected onto a single unidimensional scale of palatability to capture the motivational states that ranged from acceptance to rejection.

Gastric bypass surgery for obesity decreases the reward value of a sweet-fat stimulus as assessed in a progressive ratio task

BACKGROUND Obesity is among the leading causes of disease and death. Bariatric surgery is the most effective treatment of obesity. There is increasing evidence that after gastric bypass surgery, patients and animal models show a decreased preference for sweet and fatty foods. The underlying mechanism may include alterations in taste function. OBJECTIVE We hypothesize that a gastric bypass reduces the reward value of sweet and fat tastes. DESIGN In this prospective case-control study, 11 obese patients who were scheduled to undergo a gastric bypass and 11 normal-weight control subjects in the fed state clicked a computer mouse to receive a sweet and fatty candy on a progressive ratio schedule 10 wk apart (in patients, testing took place 2 wk before and 8 wk after gastric bypass surgery). Subjects worked progressively harder to obtain a food reward (reinforcer) until they stopped clicking (ie, the breakpoint), which was a measure of the reinforcer value. Breakpoints were assessed by the number of mouse clicks in the last completed ratio. The experiment was repeated in a different cohort by using vegetable pieces as the reinforcer. RESULTS Breakpoints in the test sessions of control subjects correlated highly for both reinforcers. The median breakpoint for candies, but not vegetables, was reduced by 50% in the obese group after gastric bypass. Patients with the largest reduction in the breakpoint had the largest decrease in BMI. CONCLUSIONS Gastric bypass surgery resulted in the selective reduction of the reward value of a sweet and fat tastant. This application of the progressive ratio task provided an objective and reliable evaluation of taste-driven motivated behavior for food stimuli after obesity surgery.

Behavioral Discrimination between Quinine and KCl Is Dependent on Input from the Seventh Cranial Nerve: Implications for the Functional Roles of the Gustatory Nerves in Rats

The rat glossopharyngeal nerve (GL), which innervates posterior tongue taste buds, contains several physiologically defined taste fiber types; at least one type is primarily responsive to certain alkaloids (such as quinine), and another is primarily responsive to acids and salts. In contrast, the chorda tympani (CT), which innervates anterior tongue taste buds, does not appear to contain fibers that differentially respond to quinine relative to salts and acids. It was therefore predicted that GL transection should disrupt behavioral discriminations between quinine and either acids or salts. Water-restricted rats were trained to press one of two levers if a sampled taste stimulus was quinine (0.1–1.0 mm) and the second lever if the sampled stimulus was KCl (0.1–1.0 m). Sham surgery, GL transection, and sublingual and submaxillary salivary gland extirpation were found to have no effect relative to presurgical performance. Both CT transection and combined GL and CT transection caused a substantial and approximately equal decrement in discrimination performance. Removal of the gustatory branches of the seventh cranial nerve [CT and greater superficial petrosal (GSP)] nearly eliminated the discrimination of the taste stimuli, and combined transection of the CT, GL, and GSP unequivocally reduced performance to chance levels. Although these findings were not presaged by the known electrophysiology, they nonetheless compare favorably with other studies reporting little effect of GL transection on behavioral responses to quinine. These results, in the context of other discrimination studies reported in the literature, suggest that, in rats, the neural coding of taste quality depends primarily on the input of the facial nerve.

Excitotoxic lesions of the parabrachial nuclei prevent conditioned taste aversions and sodium appetite in rats.

Electrolytic lesions of the parabrachial nuclei (PBN) disrupt conditioned taste aversion (CTA) in the rat, but it is not known whether this effect is due to damaging axons of passage or to destruction of intrinsic neurons. We tested 10 rats with electrophysiologically guided, ibotenic acid lesions of the PBN (PBNx) to determine whether they could acquire a LiCl-induced CTA to l-alanine (0.3 M) or demonstrate a sodium appetite following furosemide treatment and overnight access to sodium deficient chow. Vehicle-treated and nonsurgical controls were included in the design. PBNx rats failed to develop a CTA, even after 3 conditioning trials. Moreover, more than 8 months later, a subset of the PBNx rats were again unable to learn a CTA using NaCl as the conditional stimulus (CS). After the furosemide treatment, the control rats drank an average of 20.3 ml of strong salt in 24 hr. The PBNx rats drank virtually no NaCl during the first 2 hr and averaged only 4.0 ml in 24 hr. In the PBN, damage to neuronal somata is more critical than interrupting fibers of passage for producing deficits in taste-guided behaviors.