Taste Learning in Insular Cortex: Plasticity Is Influenced by Experience Type

The gustatory cortex (GC) has long been studied as the main cortical area encoding taste stimuli and likely integrates sensory, visceral, and emotional information to guide taste-related behaviors. However, our understanding of cortical taste coding on a single-cell level has only become clear in recent years. The anatomical location of GC on the lateral and ventral surface of the brain makes it difficult to target with traditional imaging methods. Thus, much of what we know about cortical taste coding and cortical taste plasticity has been derived either from multiunit electrode recordings or anesthetized imaging experiments, techniques which lack the ability to reliably track neurons over time. To address this limitation, we use miniaturized microendoscope (miniscope) imaging of the calcium indicator GCaMP6s to investigate how cortical taste coding changes with different types of experience. In a basic taste experience paradigm, in which animals consume taste stimuli based on innate taste preferences, we address the question of how novelty and familiarity of taste stimuli effect cortical coding. Using multiday cell tracking, we find two populations of neurons: a stable population encoding taste quality information, and a transient cell population whose activity correlates with the animal's behavioral state. We use the associative learning paradigm conditioned taste aversion (CTA) to show changes in the transient cell population depend upon experience type. With basic experience, the number of transient cells decreases as animals become familiar with taste stimuli and the behavioral task. After increasing situational salience using CTA, the number of transient cells increases to levels seen during novel taste exposure. This research demonstrates a clear role for novelty and familiarity in population responses to taste stimuli in GC, and suggests an overall implication for these effects in cortical coding of sensory stimuli.

Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii

Although most Drosophila species lay eggs in overripe fruit, the agricultural pest Drosophila suzukii lays eggs in ripe fruit. We found that changes in bitter taste perception have accompanied this adaptation. We show that bitter-sensing mutants of Drosophila melanogaster undergo a shift in egg laying preference toward ripe fruit. D. suzukii has lost 20% of the bitter-sensing sensilla from the labellum, the major taste organ of the head. Physiological responses to various bitter compounds are lost. Responses to strawberry purées are lost from two classes of taste sensilla. Egg laying is not deterred by bitter compounds that deter other species. Profiling of labellar transcriptomes reveals reduced expression of several bitter Gr genes (gustatory receptors). These findings support a model in which bitter compounds in early ripening stages deter egg laying in most Drosophila species, but a loss of bitter response contributes to the adaptation of D. suzukii to ripe fruit.

Neural Coding of Food Is a Multisensory, Sensorimotor Function

This review is a curated discussion of the relationship between the gustatory system and the perception of food beginning at the earliest stage of neural processing. A brief description of the idea of taste qualities and mammalian anatomy of the taste system is presented first, followed by an overview of theories of taste coding. The case is made that food is encoded by the several senses that it stimulates beginning in the brainstem and extending throughout the entire gustatory neuraxis. In addition, the feedback from food-related movements is seamlessly melded with sensory input to create the representation of food objects in the brain.

Taste coding strategies in insular cortex

While the cortical representation of sensory stimuli is well described for some sensory systems, a clear understanding of the cortical representation of taste stimuli remains elusive. Recent investigations have focused on both spatial and temporal organization of taste responses in the putative taste region of insular cortex. This review highlights recent literature focused on spatiotemporal coding strategies in insular cortex. These studies are examined in the context of the organization and function of the entire insular cortex, rather than a specific gustatory region of insular cortex. In regard to a taste quality-specific map, imaging studies have reported conflicting results, whereas electrophysiology studies have described a broad distribution of taste-responsive neurons found throughout insular cortex with no spatial organization. The current collection of evidence suggests that insular cortex may be organized into a hedonic or “viscerotopic” map, rather than one ordered according to taste quality. Further, it has been proposed that cortical taste responses can be separated into temporal “epochs” representing stimulus identity and palatability. This coding strategy presents a potential framework, whereby the coordinated activity of a population of neurons allows for the same neurons to respond to multiple taste stimuli or even other sensory modalities, a well-documented phenomenon in insular cortex neurons. However, these representations may not be static, as several studies have demonstrated that both spatial representation and temporal dynamics of taste coding change with experience. Collectively, these studies suggest that cortical taste representation is not organized in a spatially discrete map, but rather is plastic and spatially dispersed, using temporal information to encode multiple types of information about ingested stimuli. Impact statement The organization of taste coding in insular cortex is widely debated. While early work has focused on whether taste quality is encoded via labeled line or ensemble mechanisms, recent work has attempted to delineate the spatial organization and temporal components of taste processing in insular cortex. Recent imaging and electrophysiology studies have reported conflicting results in regard to the spatial organization of cortical taste responses, and many studies ignore potentially important temporal dynamics when investigating taste processing. This review highlights the latest research in these areas and examines them in the context of the anatomy and physiology of the insular cortex in general to provide a more comprehensive description of taste coding in insular cortex.

Taste Coding and Feedforward/Feedback Signaling in Taste Buds

Taste buds are the sensory end organs of the gustatory system. Thousands of these tiny sensory structures are embedded throughout the lingual epithelium and palate. As well-defined anatomical structures, taste buds can provide valuable insight into microcircuit organization. Information transmitted by taste buds to the brain results in conscious perceptions of taste—sweet, sour, salty, bitter, umami, and perhaps fat and others, but they also generate signals that initiate physiological reflexes such as a rapid burst of insulin secretion from the pancreatic islets to prepare the digestive tract for food. These responses are termed cephalic phase reflexes. This chapter presents an overview of how cell-cell communication and synaptic transmission within taste buds might underlie information processing in these sensory end organs, and perhaps also sheds light on the problem of taste coding, at least at its initial stages in the periphery.

Taste coding of complex naturalistic taste stimuli and traditional taste stimuli in the parabrachial pons of the awake, freely licking rat

Several studies have shown that taste-responsive cells in the brainstem taste nuclei of rodents respond to sensory qualities other than gustation. Such data suggest that cells in the classical gustatory brainstem may be better tuned to respond to stimuli that engage multiple sensory modalities than to stimuli that are purely gustatory. Here, we test this idea by recording the electrophysiological responses to complex, naturalistic stimuli in single neurons in the parabrachial pons (PbN, the second neural relay in the central gustatory pathway) in awake, freely licking rats. Following electrode implantation and recovery, we presented both prototypical and naturalistic taste stimuli and recorded the responses in the PbN. Prototypical taste stimuli (NaCl, sucrose, citric acid, and caffeine) and naturalistic stimuli (clam juice, grape juice, lemon juice, and coffee) were matched for taste quality and intensity (concentration). Umami (monosodium glutamate + inosine monophosphate) and fat (diluted heavy cream) were also tested. PbN neurons responded to naturalistic stimuli as much or more than to prototypical taste stimuli. Furthermore, they convey more information about naturalistic stimuli than about prototypical ones. Moreover, multidimensional scaling analyses showed that across unit responses to naturalistic stimuli were more widely separated than responses to prototypical taste stimuli. Interestingly, cream evoked a robust and widespread response in PbN cells. Collectively, these data suggest that natural foods are more potent stimulators of PbN cells than purely gustatory stimuli. Probing PbN cells with pure taste stimuli may underestimate the response repertoire of these cells.

Multimodal stimulus coding by a gustatory sensory neuron in Drosophila larvae

Accurate perception of taste information is crucial for animal survival. In adult Drosophila, gustatory receptor neurons (GRNs) perceive chemical stimuli of one specific gustatory modality associated with a stereotyped behavioural response, such as aversion or attraction. We show that GRNs of Drosophila larvae employ a surprisingly different mode of gustatory information coding. Using a novel method for calcium imaging in the larval gustatory system, we identify a multimodal GRN that responds to chemicals of different taste modalities with opposing valence, such as sweet sucrose and bitter denatonium, reliant on different sensory receptors. This multimodal neuron is essential for bitter compound avoidance, and its artificial activation is sufficient to mediate aversion. However, the neuron is also essential for the integration of taste blends. Our findings support a model for taste coding in larvae, in which distinct receptor proteins mediate different responses within the same, multimodal GRN.