Taste-potentiated Odor Aversion Research Articles

An evaluation of hedonic responses in taste-potentiated odor aversion using the analysis of licking microstructure and orofacial reactivity

Two experiments examined the hedonic responses conditioned to odor cues in the phenomenon of taste-potentiated odor aversion. Experiment 1 analyzed the microstructure of licking behavior during voluntary consumption. A tasteless odor (amyl acetate) was delivered to rats either diluted in water or mixed with saccharin before being injected with LiCl. At test, subjects which had received the odor-taste compound during conditioning showed both lower odor consumption and lick cluster size, a result indicating an increased negative evaluation of the odor. Experiment 2 examined the orofacial reactions elicited by the odor as index of its hedonic impact. During conditioning, the rats were intraorally infused with either the odor alone or the odor-saccharin compound before being injected with LiCl. At test, they were infused with the odor and their orofacial responses video recorded. More aversive orofacial responses were elicited by the odor cue in rats that had compound conditioning, again a result indicating a strengthened negative hedonic reactivity compared to animals experiencing odor aversion conditioning alone. Taken together, these results indicate that taste-mediated potentiation of odor aversion conditioning impacts on the acquisition of conditioned hedonic reactions as well as consumption.

Stability and flexibility of the message carried by semiochemical stimuli, as revealed by devaluation of carbon disulfide followed by social transmission of food preference.

Semiochemicals are volatile compounds that communicate specific meaning between individuals and elicit specific behavioral and/or physiological responses mediated by highly sensitive and highly specific olfactory pathways. Recent work suggests that semiochemicals can activate multiple olfactory pathways at once, but the degree to which parallel pathways activated by the same semiochemical interact and what the behavioral consequences of such interactions are remains a topic of debate. Here, we approached this question behaviorally, investigating whether rats could be trained to avoid carbon disulfide (CS₂; conditional stimulus) via taste-potentiated odor aversion, and asking whether any such learning would have an impact on rats' subsequent use of CS₂ as a semiochemical cue (i.e., in a socially transmitted food preference paradigm). The results show that CS₂-mediated food preference learning is unimpaired by aversions conditioned to CS₂, a result indicating that canonical and semiochemical pathways for the processing of CS₂ function in a largely independent manner.

Olfactory bulbectomy, but not odor conditioned aversion, induces the differentiation of immature neurons in the adult rat piriform cortex

The piriform cortex layer II of young-adult rats presents a population of prenatally generated cells, which express immature neuronal markers, such as the polysialylated form of the neural cell adhesion molecule (PSA-NCAM) or doublecortin (DCX), and display structural characteristics of immature neurons. The number of PSA-NCAM/DCX expressing cells in this region decreases markedly as age progresses, suggesting that these cells differentiate or die. Since the piriform cortex receives a major input from the olfactory bulb and participates in olfactory information processing, it is possible that the immature neurons in layer II are affected by manipulations of the olfactory bulb or olfactory learning. It is not known whether these cells can be induced to differentiate and, if so, what would be their fate. In order to address these questions, we have performed unilateral olfactory bulbectomy (OBX) and an olfactory learning paradigm (taste-potentiated odor aversion, TPOA), in young-adult rats and have studied the expression of different mature and immature neuronal markers, as well as the presence of cell death. We have found that 14 h after OBX there was a dramatic decrease in the number of both PSA-NCAM and DCX expressing cells in piriform cortex layer II, whereas that of cells expressing NeuN, a mature neuronal marker, increased. By contrast, the number of cells expressing glutamate decarboxylase, isoform 67 (GAD67), a marker for interneurons, decreased slightly. Additionally, we have not found evidence of numbers of dying cells high enough to justify the disappearance of immature neurons. Analysis of animals subjected to TPOA revealed that this paradigm does not affect PSA-NCAM expressing cells. Our results strongly suggest that OBX can induce the maturation of immature neurons in the piriform cortex layer II and that these cells do not become interneurons. By contrast, these cells do not seem to play a crucial role in olfactory memory.

Does the olfactory cue activate the same brain network during aging in the rat after taste potentiated odor aversion retrieval?

Depending on the brain networks involved, aging is not accompanied by a general decrease in learning and memory capabilities. We demonstrated previously that learning and retrieval of taste potentiated odor aversion (TPOA) is preserved, and even slightly improved, in senescent rats showing some memory deficiencies in cognitive tasks ( Dardou, Datiche, & Cattarelli, 2008). TPOA is a particular behavior in which the simultaneous presentation of odor and taste cues followed by a delayed visceral illness leads to a robust aversion towards both conditioned stimuli, which permits diet selection and animal survival. The present experiment was performed in order to investigate the stability or the evolution of the brain network underlying TPOA retrieval during aging. By using immunocytochemical detection of Fos and Egr1 proteins we mapped the cerebral activation induced by TPOA retrieval elicited by the odor presentation in the young, the adult and the senescent rats. The pattern of brain activation changed and the number of activated areas decreased with age. Nevertheless, the piriform cortex and the basolateral amygdala nucleus were always activated and seemed essential for TPOA retrieval. The hippocampus and the neocortical areas could have different implications in TPOA memory in relation to age. The patterns of expression of Fos and Egr1 were different, suggesting their differential involvement in TPOA retrieval. Data are discussed according to the possible roles of the brain areas studied and a model of schematic brain network subtending TPOA retrieval induced by the odor cue is proposed.

Taste-potentiated odor aversion learning in rats with lesions of the insular cortex

The current study assessed the influence of excitotoxic lesions of the insular cortex (IC) on taste-potentiated odor aversion (TPOA) learning. Water-deprived rats initially received a single odor-toxicosis or odor/taste-toxicosis pairing and were subsequently tested, in separate trials, with the odor and the taste stimulus. Indicating TPOA, neurologically intact rats conditioned with the odor/taste compound stimulus acquired significantly stronger odor aversions than normal rats conditioned with the odor stimulus. IC lesions disrupted TPOA, conditioned taste aversion and taste neophobia. The finding that taste did not potentiate odor aversion learning in the IC-lesioned rats provides support for the “within-compound association” analysis but is inconsistent with the “sensory-and-gate” account of TPOA learning.

Inactivation of the basolateral amygdala impairs the retrieval of recent and remote taste-potentiated odor aversion memory

Memory reorganization as a time-dependent process can be investigated using various learning tasks such as the taste-potentiated odor aversion (TPOA). In this paradigm rats acquire a strong aversion to an olfactory cue presented simultaneously with a gustatory cue. Together these cues are paired with a delayed visceral illness. The basolateral amygdaloid nucleus (BLA) plays a key role in TPOA acquisition but its involvement in retrieval remains unclear. We investigated the involvement of the BLA in either recent or remote retrieval of TPOA. In each case, the number of licks observed in response to the presentation of either the odor or the taste was used to assess retrieval. Before the retrieval test, rats received a bilateral infusion of lidocaine to inactivate the BLA. We observed that both recent and remote TPOA retrieval tests induced by the odor presentation were disrupted in the lidocaine-injected rats. By contrast, the BLA inactivation had no effect upon the aversion towards the taste cue regardless of the time of retrieval. The present study provides evidence that BLA functioning is necessary for retrieval of aversive odor memory, even with a long post-acquisition delay.

Differences in taste-potentiated odor aversions with O+/OT+ versus OT+/O+ conditioning: Implications for configural associations

The present research demonstrates a conditioning order effect difference: Odor-aversion conditioning is stronger following OT+/O+ conditioning than following O+/OT+ conditioning with specific odor (O) and taste (T) cues. When a weak odor cue was used in Experiments 1A and 1B, OT+/O+ conditioning produced significantly stronger odor aversions than did either O+/OT+ or O+/O+ conditioning, which did not differ. The same design was used in Experiment 2 with a strong odor, but the order effect difference was not replicated, suggesting that the order effect difference is specific to conditions that produce taste-potentiated odor aversions. The interpretation that O+/OT+ conditioning is weaker because of the absence of a taste-odor within-compound association was not supported in Experiments 3 and 4. Notably, using stimuli that supported potentiation in earlier experiments, in Experiment 4, we found evidence of a taste-odor within-compound association in the absence of potentiation. These results confirm that previous theories of potentiation (within-compound association model, sensory-and-gate channeling model) are not sufficient to produce potentiation. Instead, these results are interpreted in terms of taste-odor configural associations.

Memory is differently impaired during aging according to the learning tasks in the rat

The aim of the present study was to determine the impact of aging on learning and retrieval of taste-potentiated odor aversion (TPOA). TPOA, which involves processing of odor, gustatory, and visceral cues, is a particular form of learning important to food selection. The experiment was carried out on young (1.5 month), adult (12 months), and old (20–24 months) rats. To determine whether the possible effects of aging on TPOA were related or not to general memory alterations, mnesic abilities of the rats were previously evaluated by submitting the animals to object recognition, olfactory discrimination, and spatial homing task. It was noted that the young, the adult, and the old rats were able to learn and to retrieve TPOA whatever the stimulus – either odor or taste – used to elicit retrieval. Interestingly, it can be underlined that the rejection of the odor stimulus only was even slightly increasing with the rat age. Thus, TPOA which is important in food selection and in animal survival is spared during aging while mnesic deficits were observed in the other behavioral tasks tested according to the task requirement.

Does taste or odor activate the same brain networks after retrieval of taste potentiated odor aversion?

When simultaneous presentation of odor and taste cues precedes illness, rats acquire robust aversion to both conditioned stimuli. Such a phenomenon referred to as taste-potentiated odor aversion (TPOA) requires information processing from two sensory modalities. Whether similar or different brain networks are activated when TPOA memory is retrieved by either the odor or the taste presentation remains an unsolved question. By means of Fos mapping, we investigated the neuronal substrate underlying TPOA retrieval elicited by either the odor or the taste conditioned stimulus. Whatever the sensory modality used to reactivate TPOA memory, a significant change in Fos expression was observed in the hippocampus, the basolateral nucleus of amygdala and the medial and the orbito-frontal cortices. Moreover, only the odor presentation elicited a significantly higher Fos immunoreactivity in the piriform cortex, the entorhinal cortex and the insular cortex. Lastly, according to the stimulus tested to induce TPOA retrieval, the BLA was differentially activated and a higher Fos expression was induced by the odor than by the taste in this nucleus. The present study indicates that even if they share some brain regions, the cerebral patterns induced by either the odor or the taste are different. Data are discussed in view of the relevance of each conditioned stimulus to reactivate TPOA memory and of the involvement of the different labeled brain areas in information processing and TPOA retrieval.

Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats

Lesions of the basolateral amygdala (BLA) have long been associated with abnormalities of taste-related behaviors and with failure in a variety of taste- and odor-related learning paradigms, including taste-potentiated odor aversion, conditioned taste preference, and conditioned taste aversion. Still, the general role of the amygdala in chemosensory learning remains somewhat controversial. In particular, it has been suggested that the amygdala may not be involved in a form of chemosensory learning that has recently received a substantial amount of study-socially transmitted food preference (STFP). Here, we provide evidence for this involvement by pharmacologically inactivating the basolateral amygdala bilaterally during STFP training. The same inactivation sites that impaired taste aversion learning eliminated the normally conditioned preference for a food smelled on a conspecific's breath. Impairments of learned preference persisted even in testing sessions in which BLA was not inactivated, and learning was normal when the BLA was inactivated only during testing sessions; thus, the impairment was a true acquisition deficit. In conjunction with previous results from other paradigms, therefore, our data suggest that the amygdala is vital for learning procedures involving pairings of potent and arbitrary chemosensory stimuli.

Effects of brain lesions on taste-potentiated odor aversion in rats.

Rats failed to acquire aversions to odor stimulus, which was followed 30 min later by an unconditioned stimulus (US). However, when the odor stimulus was accompanied by a taste stimulus, they acquired odor aversions as well as taste aversions. In this phenomenon, referred to as a taste-potentiated odor aversion, lesions of the amygdala disrupted both taste and odor aversions, whereas lesions of the parvicellular part of ventroposteromedial thalamic nucleus (VPMpc) or insular cortex (IC) disrupted taste aversion but attenuated only odor aversion. These results suggest that both taste and odor stimuli are associated with US in the amygdala and that taste inputs delivered to the amygdala through the IC and/or VPMpc play an important role in potentiation of odor aversion.

Basolateral amygdala NMDA receptors are selectively involved in the acquisition of taste-potentiated odor aversion in the rat.

Basolateral amygdala NMDA receptors are selectively involved in the acquisition of taste-potentiated odor aversion in the rat.

Basolateral amygdala NMDA receptors are selectively involved in the acquisition of taste-potentiated odor aversion in the rat.

In the taste-potentiated odor aversion (TPOA) paradigm, animals acquire a strong aversion to an odor that is followed by delayed intoxication only if a gustatory stimulus is presented with the odor during conditioning. Although previous work has shown that N-methyl-D-aspartate (NMDA) receptors in the basolateral nucleus of the amygdala (BLA) play a role in the acquisition of TPOA, the present study aimed at describing the process in which NMDA receptors in the BLA are involved during acquisition of TPOA. Male Long-Evans rats received intra-BLA infusions of the competitive NMDA receptor antagonist D,L-2-2-amino-5-phosphonovalerate (D-APV; 0.05 and 0.50 microg) immediately before or after the odor-taste conditioned stimulus (CS) presentation, or immediately before the test. Results showed that D-APV impaired acquisition of TPOA when infused before, but not after, the CS presentation, but did not affect retrieval. These results suggest that NMDA receptors of the BLA are involved in the formation of potentiation--by taste--of the olfactory memory trace, but not in the maintenance of this process.

The selective associability of taste aversion learning and its brain mechanisms in the rat

This article reviews the brain mechanisms of taste aversion learning in the rat. First, behavioral experiments on taste aversion learning are reviewed. In this section, the experiment of Garcia and Koelling (1966), and the concepts of belongingness (Garcia et al., 1974) and preparedness (Seligman, 1970) are introduced. Then, studies in the field of behavioral neuroscience are reviewed and summarized. According to the results of several experiments, the parabrachial nucleus and the amygdala are suggested to play important roles in taste aversion learning. Finally, experiments on taste-potentiated odor aversion suggest that the amygdala could be a possible site where the selective associability in taste aversion learning occurs. This article offers implications for the mechanisms of taste aversion learning and information about its brain mechanisms for the fields of learning theory, ethology and for the clinical areas of phobias and anorexia.

An ear for quality: Differential associative characteristics of taste-potentiated auditory and odor avoidance

This research compared the avoidance behavior of rats exposed to either a taste-tone (NaCl-70 dB, 1800 Hz) or a taste-odor (NaCl-almond) compound that had been paired with LiCl-induced illness. When tested in the presence of either the odor or the auditory cue presented alone it was found that taste potentiated both cues, but stronger initial avoidance and resistance to extinction was shown to the odor cue. A second experiment examined the generalization of potentiated odor and auditory aversions to a novel environment. Rats were exposed to either a taste-odor or taste-tone compound, again followed by illness. Half of each group was tested in the conditioning chamber and half in a novel chamber. Odor aversions were not affected by location, whereas auditory aversions were significantly stronger in the conditioning chamber. Experiment 3 showed that taste-potentiated odor and auditory aversions showed different patterns of extinction when the taste aversion on which they were based was gradually extinguished. These experiments provide evidence that while the taste potentiation of auditory cues is a reliable phenomena, the pattern of effects is different from that of taste-potentiated odor aversions

Neuroanatomical and Functional Specificity of the Basolateral Amygdaloid Nucleus in Taste-Potentiated Odor Aversion

The present study aimed at documenting the neurobiological substrate of taste-potentiated odor aversion (TPOA) in the rat. The role of several temporal lobe structures in discriminative TPOA learning was questioned. The effects of excitotoxic lesions (ibotenate) of the basolateral amygdaloid nucleus, the central amygdaloid nucleus, the caudate putamen nucleus, and aspirative lesion of the entorhinal cortex were studied. The results show that only basolateral amygdaloid nucleus (ABL) damage impaired TPOA. This effect was selective of TPOA, since it spared conditioned taste aversion (CTA) and olfactory perception. in order to find out which process in TPOA requires normal functioning of the ABL, the effects of microinjections of a GABA A agonist (muscimol) into the ABL at various stages of the experiment were examined. The results show that application of muscimol during the acquisition, before or after the presentation of the odor-taste stimulus, impaired TPOA without affecting CTA. Contrastingly, application of muscimol before the test impaired neither TPOA nor CTA. These results suggest that ABL is involved in the acquisition but not in the retrieval of TPOA. The efficacy of muscimol microinjected after the presentation of the odor-taste stimulus further suggests that the deficit is not due to a sensory impairment but rather to the disruption of a memory process, critical for TPOA.

Taste-potentiated odor aversion learning based on amphetamine

This study sought to determine whether a taste can potentiate a conditioned odor aversion based on amphetamine as well as those based on lithium. A taste-potentiated odor aversion (TPOA) based on lithium was obtained in Experiment 1 only with a low concentration of an almond odor. This concentration was used in Experiment 2 where the taste, 0.1% saccharin, potentiated an odor aversion based on 1 mg/kg d-amphetamine. This was replicated in Experiment 3 where potentiation was found with doses of both 1 and 3 mg/kg amphetamine, and no effect of dose was detected. It was concluded that TPOA learning is not restricted to drugs such as lithium that produce conditioned unpalatability as well as conditioned aversions to a taste, because amphetamine does not produce conditioned unpalatability at the doses used here. Furthermore, because in Experiment 3 postconditioning extinction of the saccharin aversion removed the potentiation effect, it appears that this form of TPOA may depend on an association between the odor and taste, as proposed by within-compound theory.

Taste-potentiated odor aversion learning: role of the amygdaloid basolateral complex and central nucleus.

The present study examined the relative contributions of the amygdaloid basolateral complex (ABL) and central nucleus (CN) to taste-potentiated odor aversion (TPOA) learning--an associative learning task that is dependent on information processing in two sensory modalities. In Experiment 1, rats with neurotoxic lesions of these systems were trained on the TPOA task by presenting a compound taste-odor conditioned stimulus, which was followed by LiCl administration. Results showed that ABL damage caused an impairment in potentiated odor aversion learning but no deficit in the conditioned taste aversion. In contrast, rats with CN damage learned both tasks. Experiment 2 examined the effects of ABL damage on TPOA and odor discrimination learning. The odor discrimination procedure used a place preference task to demonstrate normal processing of olfactory information. Results indicated that although ABL-lesioned animals were impaired on TPOA, there was no deficit in odor discrimination learning.

Conditioned taste and taste-potentiated odor aversions in the Syracuse high- and low-avoidance (SHA/Bru and SLA/Bru) strains of rats (Rattus norvegicus).

Conditioned taste and taste-potentiated odor aversions in the Syracuse high- and low-avoidance (SHA/Bru and SLA/Bru) strains of rats (Rattus norvegicus).

Taste-potentiated odor aversion learning: Role of the amygdaloid basolateral complex and central nucleus.

The present study examined the relative contributions of the amygdaloid basolateral complex (ABL) and central nucleus (CN) to taste-potentiated odor aversion (TPOA) learning--an associative learning task that is dependent on information processing in two sensory modalities. In Experiment 1, rats with neurotoxic lesions of these systems were trained on the TPOA task by presenting a compound taste-odor conditioned stimulus, which was followed by LiCl administration. Results showed that ABL damage caused an impairment in potentiated odor aversion learning but no deficit in the conditioned taste aversion. In contrast, rats with CN damage learned both tasks. Experiment 2 examined the effects of ABL damage on TPOA and odor discrimination learning. The odor discrimination procedure used a place preference task to demonstrate normal processing of olfactory information. Results indicated that although ABL-lesioned animals were impaired on TPOA, there was no deficit in odor discrimination learning.