Central taste pathways: an overview (2023)

4.24.1.1 Taste Route Entrances to Reward System and Food Center

The neural pathway of the brain's reward system has also been studied and documented (Berridge, KC and Robinson, TE, 1998; Wise, R.A., 2002for reviews). as it is shown inFigure 1and described in more detail in later sections of this chapter, the essential components are the ventral tegmental area (VTA) in the midbrain, the origin of the mesolimbic dopaminergic system, the nucleus accumbens (Acc), an essential interface between motivation (p. palatability) and action (e.g. feeding), and the ventral pallidum (VP) located between the Acc and the LH, known as the feeding center.

When we consider the roles of taste in eating and reward, we need to be clear about how the taste system interacts with the reward and eating systems. However, this has not yet been clarified. The amygdala (AMY), prefrontal cortex (PFC), including the ventrolateral (or anterior sulcal) and dorsomedial cortices, and the IC are candidates for interfaces between the two systems. The insular taste cortex sends axons to the PFC (Saper, CB, 1982; Shi, C.-J. y Cassell, MD, 1998), and dorsomedial PFC neurons actually respond to taste stimuli (lucas, b.and another, 2002; Karadi, Z.and another, 2005). Among other structures, the PFC is interconnected with subcortical areas related to feeding, such as the basal forebrain.Divac, E.and another, 1978), tonsil (Pérez-Jaranay, J.M. and Vives, F., 1991), HE (Kita, H. and Oomura, Y., 1981), VTA (Divac, E.and another, 1978; Kosobud, A.E.and another, 1994) and tell (Brog, JSand another, 1993). Behavioral studies have shown that the PFC is associated with several mechanisms in the central control of feeding, for example, lesions of the dorsomedial PFC result in pampering.Kolb, B. and Nonneman, A. J., 1975) and impairment of conditioned taste aversion (CTA) (Hernadi, I.and another, 2000; Karadi, Z.and another, 2005), whereas injury and electrical stimulation of the ventrolateral PFC induce eating disorders (Kolb, B. y Nonneman, A.J., 1975; Brandes, J. S. e Johnson, A. K., 1978) and feeding (Bielajew, C. and Trzcinska, M., 1994), respectively.

3.14.2 Introduction

This review will predominantly focus on studies conducted with rodent species (especially rats, hamsters, and mice), as these models were amenable to experimental neuroanatomical and neurophysiological techniques that proved crucial in establishing central taste connectivity. Additionally, they share much of the same characteristic core flavor architecture (although there may be minor differences). Therefore, studies will generally be cited and discussed in this review without explicitly distinguishing between rodent species. However, we have included (whenever possible) among the most recent studies cited, studies with mice, a species that has gained prominence in neuroscience research in the last decade, thanks to advances in circuit research using transgenic models. and molecular tools (Harris and others, 2014;Lerner and others, 2016;Oh and, 2014;December 2016). We also highlight the mouse-flavored CNS in the figures accompanying this review; Previous reviews with a focus on taste pathways and areas in the rat can be consulted (Lundy and Norgren, 2015) and the hamster (Smith y Davis, 2000). Finally, additional reviews are suggested for further analysis of taste pathways in primates and humans (scrolls, 1995;Scott and Silver-Salaman;small, 2006,2012).

3.25.3.2 Electrophysiology

In rodents and monkeys, taste cells along the central taste pathway were sampled using electrophysiological techniques and this may reveal some species-specific characteristics. For example, in rats, the NST cell taste response appears to be modulated by physiological needs and satiety signals (eg, gastric distension;Glenn y Erickson, 1976). However, NST taste cells in primates are not affected by satiety, as demonstrated, for example, by reversing the incentive value of glucose in a specific type of sensory satiety experiment.Yaxleyand another., 1985). This apparent distinction between rodent and primate cases can be partially explained by the fact that, in primates, NST projection fibers bypass the PBN, where visceral and physiological information may be preferentially processed.

Up-down regulation is an important feature of taste processing, since stimulation of the hypothalamus or the central nucleus of the amygdala can modulate taste responses in the TSN and parabrachial nuclei.Butand another,2002;liand another., 2005). This is important, as both the amygdala and the hypothalamus receive information from the cortical areas of taste and can therefore function as intermediaries for cortical modulation of taste processing at the brainstem level. Note that these descending pathways also exist in primates (Price and Amaral, 1981).

In primates, despite the name, only a small proportion of cells in the primary taste cortex actually respond exclusively and consistently to taste stimuli.Scott and Silver-Salaman; ~6.5%), while a higher proportion (~23%) responded during tongue or jaw movements, for example. This suggests that the primate primary taste cortex may be simultaneously encoding taste and the oral somatosensory properties of (intraoral) stimuli. These recording studies constitute an early indication that multisensory encoding may occur in the primary taste cortex.

In the primary taste cortex (in primates, including the frontal opercular and dysgranular insula), the responses of taste-related neurons are multisensory and more tuned than in the NST and pcVPM.Sewards y Sewards, 2001). Curiously, I did not case two rodents,Katzand another(2001, 2002)showed that when time is taken into account as a source of variability, the taste specificity of the responses increased from approximately 10%, when only the average activity is considered, to 41% of the recorded taste cells, suggesting that the Temporal information encoding is a characteristic core of flavor processing. In this regard,Katzand another(2002)also showed that neurons that exhibit synchronous activity can also contribute to the identification of tasters.

Single-cell recording studies of the secondary taste cortex (orbitofrontal cortex) were able to more clearly demonstrate the distributed and multimodal features of taste processing in primates. The role of the primate orbitofrontal cortex in reward processing has been consistently established by several different lines of evidence. In non-human primates, there is strong evidence at the single-neuron level that the orbitofrontal cortex responds based on the reward value of taste.rollsand another., 1989), olfactory (Critchley y Rolls, 1996) and visual stimuli (Critchley y Rolls, 1996). This shows that vision, a sensory modality specially developed in primates, can also provide information to associate with gustatory perceptual information (seeEvolution of the primate brain in the phylogenetic context).

In the specific case of neurons that respond to the reward value of taste stimuli, neurons in the macaque monkey orbitofrontal cortex have been shown to respond in a sensory-specific manner to satiety.rollsand another., 1989). Furthermore, reward-related learning and expectation appear to be represented at the level of a single neuron in the primate orbitofrontal cortex.Schultzand another., 2000), probably involving the midbrain dopaminergic system. Thus, the findings detailed above provide evidence that a part of the primate taste cortex may support simultaneous encoding of multiple sensory features of taste stimuli, including stimulus identity, multisensory (olfactory, somatosensory) combinations, and the value of the reward (seeThe loss of olfactory receptor genes in human evolution,Evolution of the somatosensory system: clues from specialized species).

4.13.3 Neuroanatomy of taste and learning of conditioned taste aversion

Yamamoto and others (1995)studied the effects of lesions on various structures of the forebrain, including the PBN, hippocampus, pcVPM, gustatory and entorhinal cortices, amygdala, and the lateral and ventromedial hypothalamic nuclei, and reported that lesions in the PBN affected acquisition and CTA retention. Other studies have suggested that the basic integration between flavor and visceral inputs actually occurred at the PBN level.

The PBN projects to the VPMpc (Hamilton and Norgren, 1984), and from the relay station in the thalamus, taste information is transmitted to the taste cortex (GC), which resides in the anterior portion of the insular cortex. Small lesions in the pcVPMV did not affect CTA learning or recovery (Reilly y Pritchard, 1996), but a combination of lesions in VPMpc and GC abolished CTA learning (Yamamoto, 1995).

Humans and monkeys have an additional secondary taste area, and it has been suggested that subdivisions within the insular cortex may serve as a secondary taste area in the rat brain. In the same way that the subcortical areas convert taste information, as described, the insular cortex also processes taste information (in its anterior part) and visceral information (caudodorsally to the GC).

The first indication of the role of the GC in the processing of flavor information was provided byBrown and others. (1972). Later, many experimental techniques, based on lesions, electrophysiology, imaging, correlative biochemistry, pharmacology and, recently, direct imaging studies, proved useful to analyze the role of SLNs in taste learning. It is clear that GC plays a key role in CTA acquisition and retention. The reversible inactivation of the amygdala and insular cortex by microinjection of tetrodotoxin (TTX) into these two brain structures at different intervals prior to taste learning suggests that the insular cortex is critical for taste learning, while the amygdala is crucial for taste learning. taste formation.Gallo and others, 1992). The insular cortex and its taste portion can be divided anatomically into granular (normal neocortex), dysgranular, and agranular (ie, fading fourth layer) cortices. In rodents, most of the neurons that respond to taste stimuli reside in the dysgranular insular cortex. However, the input of PCVPM terminates in the granular and dysgranular insular cortices. A topographic spatial organization of the SLN in relation to the various taste stimuli was recently suggested through direct images of the SLN.live(Accolla et al., 2007).

The taste experience has other dimensions beyond the chemical input itself, such as temperature and structure. It is assumed that these dimensions are processed by the adjacent cortex, but also by the granular insular cortex itself (Simon and others, 2006).

The hippocampus, a forebrain structure known to be involved in many forms of learning, has also been investigated for its role in taste learning. The role of the hippocampus in ATC is controversial; however, its involvement in neophobic taste responses has been reported in several experiments. A temporally correlated response was found in the hippocampus and GC. However, different molecular pathways were activated in the hippocampus and insular cortex.Yefet et al., 2006).

Introduction

The function of the taste system is to detect, identify and establish the palatability of specific chemical substances present in foods and beverages, here called "tasters". Sugars, salts, acids, alkaloids, and amino acids can dissolve in saliva, bind to specific receptors, and activate taste receptor cells located in the taste buds. Activation of different receptors initiates the chain of events that leads to the perception of different taste qualities: sweet, salty, sour, bitter, and umami (salty). Information processed in the taste buds is transmitted to afferent fibers of three cranial nerves, facial (CN VII), glossopharyngeal (CN IX), and vagus (CN X). The cell bodies of these afferent fibers are located in the ganglia of the cranial nerves, the central branches of which enter the central nervous system in the brainstem. Signals regarding the chemical identity of taste stimuli are processed by the brainstem nuclei before ascending to the gustatory thalamus and finally reaching the gustatory cortex. This pathway has been widely studied for its role in the analysis of chemical information present in the mouth.Spector y Travers, 2005;Spector y Glendinning, 2009;Carleton and others, 2010). Regarding this function, two main theories have been formulated, each postulating a different strategy for encoding chemosensory signals (Lemon and Katz, 2007). The first theory, the labeled line theory, proposes that information about different taste qualities is encoded by distinct groups of neurons that must be tightly tuned to uniquely encode a single taste quality.Hellekant et al., 1998;Chandrashekar and others, 2006). From this point of view, each structure, region, or nucleus along the central taste pathway contains distinct neurons to signal sweet, salty, sour, bitter, and umami sensations. According to the most extreme view of the marked line theory, the same coding strategy is applied from the tongue to the cortex (Chen et al., 2011). A second theory, historically rooted in the theory of patterns between neurons (Ericson, 1963), postulates that taste qualities are encoded by the combined and dynamic activity of large assemblies of neurons (Katz et al., 2002). Each taste quality may involve the same group of neurons, but evoke different patterns of activity. Thus, individual taste neurons do not need to be closely tuned, but can encode information about multiple taste qualities. For several decades, the opposition between these two theories dominated the debate on the function of the taste system. Although the exact coding scheme has been controversial, no theory has challenged the view of the taste system as solely dedicated to representing flavor qualities.

However, recent data have opened the door to a more integrative perspective of the taste system (Jones et al., 2006;Simon and others, 2006;Fontanini Winners, 2016b). According to this view, neurons in the taste system are not only concerned with encoding flavors, but also with non-gustatory information related to food and the eating experience.small, 2012). For example, stimuli from sensory modalities other than taste, such as texture, temperature, and odor, can effectively recruit neurons into the taste system.wilson and lemon, 2013;Escanilla et al., 2015;Maier et al., 2015;Vincis and Fontanini, 2016a;Li and Lemon, 2018). In addition to other sensory modalities, neurons in the taste system are also sensitive to visceral signals related to the effects of food after pregnancy.Oliveira-Maia et al., 2012), as well as homeostatic signals that convey the subject's metabolic state (from Araujo et al., 2006). Finally, neurons throughout the taste system can encode psychological, affective, and cognitive states associated with the present and past experience of eating.Simon and others, 2006;Fontanini Winners, 2016b). This function of the taste system depends on its close relationship with areas dedicated to interoceptive signal processing and reward-related functions (Haley et al., 2016;Livneh et al., 2017).

Although numerous chemosensory coding theories have been proposed, less attention has been paid to how taste areas represent and integrate information from non-taste sources. Evidence from electrophysiological recordings suggests that individual neurons may encode multiple taste and non-taste variables.Gardner y Fontanini, 2014;Escanilla et al., 2015;Liu y Fontanini, 2015;Vincis and Fontanini, 2016a;Livneh et al., 2017), a feat known as "multiplexing". Information multiplexing is thought to occur through time-varying changes in firing rates (Katz et al., 2002;Parabucki and Netser, 2014). This ability to represent various signals is modulated and enhanced by learning (Grossman et al., 2008;Moran y Katz, 2014;Vincis and Fontanini, 2016a). According to this relatively recent perspective, the taste system is not just an analyzer of chemical information, but an adaptive system that integrates all the information necessary to adequately shape and contextualize the eating experience.

In this chapter, we review the basic organization of the taste system, its connectivity, and its ability to represent pure taste information and complex signals related to food consumption. By necessity, the focus is primarily on non-human mammalian forms, primarily rodents, although whenever possible, information on humans and other primates is provided.