The effect of multisensory context and experience on flavor preference decisions in rats.

Flavor is perceived through multiple senses, including gustation and olfaction. Previous studies have shown that different sensory qualities that make up flavor are integrated to inform perceptual judgements. Psychophysical work in humans further suggests a prominent role for congruency (i.e., the learnt correspondence between taste and odor components of flavor through eating experience) in shaping multisensory interactions underlying perceptual judgments of flavor. However, eating experience cannot be controlled in humans, and depending on the type of judgement, these studies yielded mixed findings. Here, we used rats to test how experimentally-controlled experience with specific flavor mixtures (OdorA+TasteA and OdorB +TasteB) from weaning to adulthood affects subsequent flavor preference judgements in a series of two-bottle preference tests. In unisensory conditions, animals made odor or taste preference decisions (i.e., OdorA versus OdorB and TasteA versus TasteB, respectively). In multisensory conditions, animals made identical decisions, but the addition of the other modality rendered one solution congruent; the other one incongruent (e.g., OdorA+TasteA versus OdorB+TasteA). The results show that animals effectively learned congruency associations between the taste and smell components of experienced flavor mixtures. Comparing unisensory and multisensory conditions revealed no systematic effect of congruency on the magnitude of flavor preference, but preferences were less variable in multisensory compared to unisensory conditions. Results from a second group of naïve animals further demonstrate that increased reliability of preference judgements in multisensory conditions was independent of experience.

Early development of olfactory circuit function.

During early development, brains undergo profound changes in structure at the molecular, synaptic, cellular and circuit level. At the same time, brains need to perform adaptive function. How do structurally immature brains process information? How do brains perform stable and reliable function despite massive changes in structure? The rodent olfactory system presents an ideal model for approaching these poorly understood questions. Rodents are born deaf and blind, and rely completely on their sense of smell to acquire resources essential for survival during the first 2 weeks of life, such as food and warmth. Here, we review decades of work mapping structural changes in olfactory circuits during early development, as well as more recent studies performing in vivo electrophysiological recordings to characterize functional activity patterns generated by these circuits. The findings demonstrate that neonatal olfactory processing relies on an interacting network of brain areas including the olfactory bulb and piriform cortex. Circuits in these brain regions exhibit varying degrees of structural maturity in neonatal animals. However, despite substantial ongoing structural maturation of circuit elements, the neonatal olfactory system produces dynamic network-level activity patterns that are highly stable over protracted periods during development. We discuss how these findings inform future work aimed at elucidating the circuit-level mechanisms underlying information processing in the neonatal olfactory system, how they support unique neonatal behaviors, and how they transition between developmental stages.

Taste-Odor Association Learning Alters the Dynamics of Intraoral Odor Responses in the Posterior Piriform Cortex of Awake Rats.

How an odor is perceived is to a large extent dependent on the context in which that odor is (or has been) experienced. For example, experiencing an odor in mixture with taste during consumption can instill taste qualities in the percept of that odor (e.g., vanilla, an odor, has a gustatory quality: sweet). How associative features of odors are encoded in the brain remains unknown, but previous work suggests an important role for ongoing interactions between piriform cortex and extraolfactory systems. Here, we tested the hypothesis that piriform cortex dynamically encodes taste associations of odors. Rats were trained to associate one of two odors with saccharin; the other odor remained neutral. Before and after training, we tested preferences for the saccharin-associated odor versus the neutral odor, and recorded spiking responses from ensembles of neurons in posterior piriform cortex (pPC) to intraoral delivery of small drops of the same odor solutions. The results show that animals successfully learned taste-odor associations. At the neural level, single pPC neuron responses to the saccharin-paired odor were selectively altered following conditioning. Altered response patterns appeared after 1 s following stimulus delivery, and successfully discriminated between the two odors. However, firing rate patterns in the late epoch appeared different from firing rates early in the early epoch (<1 s following stimulus delivery). That is, in different response epoch, neurons used different codes to represent the difference between the two odors. The same dynamic coding scheme was observed at the ensemble level.

Multisensory integration of orally-sourced gustatory and olfactory inputs to the posterior piriform cortex in awake rats.

Flavour refers to the sensory experience of food, which is a combination of sensory inputs sourced from multiple modalities during consumption, including taste and odour. Previous work has demonstrated that orally-sourced taste and odour cues interact to determine perceptual judgements of flavour stimuli, although the underlying cellular- and circuit-level neural mechanisms remain unknown. We recently identified a region of the piriform olfactory cortex in rats that responds to both taste and odour stimuli. Here, we investigated how converging taste and odour inputs to this area interact to affect single neuron responsiveness ensemble coding of flavour identity. To accomplish this, we recorded spiking activity from ensembles of single neurons in the posterior piriform cortex (pPC) in awake, tasting rats while delivering taste solutions, odour solutions and taste + odour mixtures directly into the oral cavity. Our results show that taste and odour inputs evoke highly selective, temporally-overlapping responses in multisensory pPC neurons. Comparing responses to mixtures and their unisensory components revealed that taste and odour inputs interact in a non-linear manner to produce unique response patterns. Taste input enhances trial-by-trial decoding of odour identity from small ensembles of simultaneously recorded neurons. Together, these results demonstrate that taste and odour inputs to pPC interact in complex, non-linear ways to form amodal flavour representations that enhance identity coding. KEY POINTS: Experience of food involves taste and smell, although how information from these different senses is combined by the brain to create our sense of flavour remains unknown. We recorded from small groups of neurons in the olfactory cortex of awake rats while they consumed taste solutions, odour solutions and taste + odour mixtures. Taste and smell solutions evoke highly selective responses. When presented in a mixture, taste and smell inputs interacted to alter responses, resulting in activation of unique sets of neurons that could not be predicted by the component responses. Synergistic interactions increase discriminability of odour representations. The olfactory cortex uses taste and smell to create new information representing multisensory flavour identity.

The role of viscosity in flavor preference: plasticity and interactions with taste.

The brain combines gustatory, olfactory, and somatosensory information to create our perception of flavor. Within the somatosensory modality, texture attributes such as viscosity appear to play an important role in flavor preference. However, research into the role of texture in flavor perception is relatively sparse, and the contribution of texture cues to hedonic evaluation of flavor remains largely unknown. Here, we used a rat model to investigate whether viscosity preferences can be manipulated through association with nutrient value, and how viscosity interacts with taste to inform preferences for taste + viscosity mixtures. To address these questions, we measured preferences for moderately viscous solutions prepared with xanthan gum using 2-bottle consumption tests. By experimentally exposing animals to viscous solutions with and without nutrient value, we demonstrate that viscosity preferences are susceptible to appetitive conditioning. By independently varying viscosity and taste content of solutions, we further show that taste and viscosity cues both contribute to preferences for taste + viscosity mixtures. How these 2 modalities are combined depended on relative palatability, with mixture preferences falling in between component preferences, suggesting that hedonic aspects of taste and texture inputs are centrally integrated. Together, these findings provide new insight into how texture aspects of flavor inform hedonic perception and impact food choice behavior.

Odor mixture perception during flavor consumption in rats.

Odor mixtures can be perceived as configural (i.e., different from their components) or elemental (i.e., similar to their components). Previous work demonstrates that these perceptual modes are determined by both peripheral and central interactions among mixture components. Flavor consumption is associated with unique peripheral and central odor processing mechanisms, but how this context affects perception of odor mixtures remains unknown. Here, we used a flavor consumption task in rats to measure preferences for solutions of binary odor mixtures and their components. In contrast to previous findings using identical mixtures in other contexts, our results demonstrate that rats employ elemental mixture processing strategies in the context of consumption. We discuss potential peripheral and central mechanisms that could explain unique mixture perception during consumption. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Network Dynamics in the Developing Piriform Cortex of Unanesthetized Rats.

The time course of changes in functional cortical activity during early development has been extensively studied in the rodent visual system. A key period in this process is the time of eye opening, which marks the onset of patterned visual input and active vision. However, vision differs from other systems in that it receives limited patterned sensory input before eye opening, and it remains unclear how findings from vision relate to other systems. Here, we focus on the development of cortical network activity in the olfactory system-which is crucial for survival at birth-by recording field potential and spiking activity from piriform cortex of unanesthetized rat pups from birth (P0) to P21. Our results demonstrate that odors evoke stable 10-15 Hz oscillations in piriform cortex from birth to P15, after which cortical responses undergo rapid changes. This transition is coincident with the emergence of gamma oscillations and fast sniffing behavior and preceded by an increase in spontaneous activity. Neonatal network oscillations and their developmental dynamics exhibit striking similarities with those previously observed in the visual, auditory, and somatosensory systems, providing insight into the network-level mechanisms underlying the development of sensory cortex in general and olfactory processing in particular.

Adaptive weighting of taste and odor cues during flavor choice.

Colloquially referred to as "taste," flavor is in reality a thoroughly multisensory experience. Yet, a mechanistic understanding of the multisensory computations underlying flavor perception and food choice is lacking. Here, we used a multisensory flavor choice task in rats to test specific predictions of the statistically optimal integration framework, which has previously yielded much insight into cue integration in other multisensory systems. Our results confirm three key predictions of this framework in the unique context of flavor choice behavior, providing novel mechanistic insight into multisensory flavor processing.NEW & NOTEWORTHY The authors demonstrate that rats make choices about which flavor solution (i.e., taste-odor mixture) to consume by weighting the individual taste and odor components according to the reliability of the information they provide about which solution is the preferred one. A similar weighting operation underlies multisensory cue combination in other domains and offers novel insight into the computations underlying multisensory flavor perception and food choice behavior.

Multisensory interactions underlying flavor consumption in rats: the role of experience and unisensory component liking.

The mechanisms by which taste and odor are combined in determining food choice behavior are poorly understood. Previous work in human subjects has yielded mixed results, potentially due to differences in task context across studies, and a lack of control over flavor experience. Here, we used rats as a model system to systematically investigate the role of experience and unisensory component liking in the multisensory interactions underlying consumption behavior. We demonstrate that taste-smell mixture consumption is best explained by a linear average of component liking. The observed pattern of results was not dependent on prior experience with specific taste-smell combinations, and unique for multisensory as opposed to unisensory mixture consumption. The results are discussed with respect to existing models of flavor integration, and a maximum-likelihood integration model previously described for multisensory judgments in other systems.

Retronasal Odor Perception Requires Taste Cortex, but Orthonasal Does Not.

Smells can arise from a source external to the body and stimulate the olfactory epithelium upon inhalation through the nares (orthonasal olfaction). Alternatively, smells may arise from inside the mouth during consumption, stimulating the epithelium upon exhalation (retronasal olfaction). Both ortho- and retronasal olfaction produce highly salient percepts, but the two percepts have very different behavioral implications. Here, we use optogenetic manipulation in the context of a flavor preference learning paradigm to investigate differences in the neural circuits that process information in these two submodalities of olfaction. Our findings support a view in which retronasal, but not orthonasal, odors share processing circuitry commonly associated with taste. First, our behavioral results reveal that retronasal odors induce rapid preference learning and have a potentiating effect on orthonasal preference learning. Second, we demonstrate that inactivation of the insular gustatory cortex selectively impairs expression of retronasal preferences. Thus, orally sourced (retronasal) olfactory input is processed by a brain region responsible for taste processing, whereas externally sourced (orthonasal) olfactory input is not.

Single-neuron responses to intraoral delivery of odor solutions in primary olfactory and gustatory cortex.

Smell plays a major role in our perception of food. Odorants released inside the mouth during consumption are combined with taste and texture qualities of a food to guide flavor preference learning and food choice behavior. Here, we built on recent physiological findings that implicated primary sensory cortex in multisensory flavor processing. Specifically, we used extracellular recordings in awake rats to characterize responses of single neurons in primary olfactory (OC) and gustatory cortex (GC) to intraoral delivery of odor solutions and compare odor responses to taste and plain water responses. The data reveal responses to olfactory, oral somatosensory, and gustatory qualities of intraoral stimuli in both OC and GC. Moreover, modality-specific responses overlap in time, indicating temporal convergence of multisensory, flavor-related inputs. The results extend previous work suggesting a role for primary OC in mediating influences of taste on smell that characterize flavor perception and point to an integral role for GC in olfactory processing.NEW & NOTEWORTHY Food perception is inherently multisensory, taking into account taste, smell, and texture qualities. However, the neural mechanisms underlying flavor perception remain unknown. Recording neural activity directly from the rat brain while animals consume multisensory flavor stimuli, we demonstrate that information about odor, taste, and mouthfeel of food converges on primary taste and smell cortex. The results suggest that processing of naturalistic, multisensory information involves an interacting network of primary sensory areas.

Sensory Cortical Activity Is Related to the Selection of a Rhythmic Motor Action Pattern.

UNLABELLED: Rats produce robust, highly distinctive orofacial rhythms in response to taste stimuli-responses that aid in the consumption of palatable tastes and the ejection of aversive tastes, and that are sourced in a multifunctional brainstem central pattern generator. Several pieces of indirect evidence suggest that primary gustatory cortex (GC) may be a part of a distributed forebrain circuit involved in the selection of particular consumption-related rhythms, although not in the production of individual mouth movements per se. Here, we performed a series of tests of this hypothesis. We first examined the temporal relationship between GC activity and orofacial behaviors by performing paired single-neuron and electromyographic recordings in awake rats. Using a trial-by-trial analysis, we found that a subset of GC neurons shows a burst of activity beginning before the transition between nondistinct and taste-specific (i.e., consumption-related) orofacial rhythms. We further showed that shifting the latency of consumption-related behavior by selective cueing has an analogous impact on the timing of GC activity. Finally, we showed the complementary result, demonstrating that optogenetic perturbation of GC activity has a modest but significant impact on the probability that a specific rhythm will be produced in response to a strongly aversive taste. GC appears to be a part of a distributed circuit that governs the selection of taste-induced orofacial rhythms. SIGNIFICANCE STATEMENT: In many well studied (typically invertebrate) sensorimotor systems, top-down modulation helps motor-control regions "select" movement patterns. Here, we provide evidence that gustatory cortex (GC) may be part of the forebrain circuit that performs this function in relation to oral behaviors ("gapes") whereby a substance in the mouth is rejected as unpalatable. We show that GC palatability coding is well timed to play this role, and that the latency of these codes changes as the latency of gaping shifts with learning. We go on to show that by silencing these neurons, we can change the likelihood of gaping. These data help to break down the sensory/motor divide by showing a role for sensory cortex in the selection of motor behavior.

Dynamic taste responses of parabrachial pontine neurons in awake rats.

The parabrachial nuclei of the pons (PbN) receive almost direct input from taste buds on the tongue and control basic taste-driven behaviors. Thus it is reasonable to hypothesize that PbN neurons might respond to tastes in a manner similar to that of peripheral receptors, i.e., that these responses might be narrow and relatively "dynamics free." On the other hand, the majority of the input to PbN descends from forebrain regions such as gustatory cortex (GC), which processes tastes with "temporal codes" in which firing reflects first the presence, then the identity, and finally the desirability of the stimulus. Therefore a reasonable alternative hypothesis is that PbN responses might be dominated by dynamics similar to those observed in GC. Here we examined simultaneously recorded single-neuron PbN (and GC) responses in awake rats receiving exposure to basic taste stimuli. We found that pontine taste responses were almost entirely confined to canonically identified taste-PbN (t-PbN). Taste-specificity was found, furthermore, to be time varying in a larger percentage of these t-PbN responses than in responses recorded from the tissue around PbN (including non-taste-PbN). Finally, these time-varying properties were a good match for those observed in simultaneously recorded GC neurons-taste-specificity appeared after an initial nonspecific burst of action potentials, and palatability emerged several hundred milliseconds later. These results suggest that the pontine taste relay is closely allied with the dynamic taste processing performed in forebrain.

A Multisensory Network for Olfactory Processing.

Primary gustatory cortex (GC) is connected (both mono- and polysynaptically) to primary olfactory (piriform) cortex (PC)-connections that might be hypothesized to underlie the construction of a "flavor" percept when both gustatory and olfactory stimuli are present. Here we use multisite electrophysiology and optical inhibition of GC neurons (GCx, produced via infection with ArchT) to demonstrate that, indeed, during gustatory stimulation, taste-selective information is transmitted from GC to PC. We go on to show that these connections impact olfactory processing even in the absence of gustatory stimulation: GCx alters PC responses to olfactory stimuli presented alone, enhancing some and eliminating others, despite leaving the path from nasal epithelium to PC intact. Finally, we show the functional importance of this latter phenomenon, demonstrating that GCx renders rats unable to properly recognize odor stimuli. This sequence of findings suggests that sensory processing may be more intrinsically integrative than previously thought.

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.

Neural dynamics in response to binary taste mixtures.

Taste stimuli encountered in the natural environment are usually combinations of multiple tastants. Although a great deal is known about how neurons in the taste system respond to single taste stimuli in isolation, less is known about how the brain deals with such mixture stimuli. Here, we probe the responses of single neurons in primary gustatory cortex (GC) of awake rats to an array of taste stimuli including 100% citric acid (100 mM), 100% sodium chloride (100 mM), 100% sucrose (100 mM), and a range of binary mixtures (90/10, 70/30, 50/50, 30/70, and 10/90%). We tested for the presence of three different hypothetical response patterns: 1) responses varying monotonically as a function of concentration of sucrose (or acid) in the mixture (the "monotonic" pattern); 2) responses increasing or decreasing as a function of degree of mixture of the stimulus (the "mixture" pattern); and 3) responses that change abruptly from being similar to one pure taste to being similar the other (the "categorical" pattern). Our results demonstrate the presence of both monotonic and mixture patterns within responses of GC neurons. Specifically, further analysis (that included the presentation of 50 mM sucrose and citric acid) made it clear that mixture suppression reliably precedes a palatability-related pattern. The temporal dynamics of the emergence of the palatability-related pattern parallel the temporal dynamics of the emergence of preference behavior for the same mixtures as measured by a brief access test. We saw no evidence of categorical coding.

Chemosensory convergence on primary olfactory cortex.

Food perception and preference formation relies on the ability to combine information from both the taste and olfactory systems. Accordingly, psychophysical investigations in humans and behavioral work in animals has shown that the taste system plays an integral role in odor processing. However, the neural basis for the influence of taste (gustation) on odor (olfaction) remains essentially unknown. Here we tested the hypothesis that gustatory influence on olfactory processing occurs at the level of primary olfactory cortex. We recorded activity from single neurons in posterior olfactory (piriform) cortex (pPC) of awake rats while presenting basic taste solutions directly to the tongue. A significant portion of pPC neurons proved to respond selectively to taste stimuli. These taste responses were significantly reduced by blockade of the gustatory epithelium, were unaffected by blockade of the olfactory epithelium, and were independent of respiration behavior. In contrast, responses to olfactory stimuli, recorded from the same area, were reduced by nasal epithelial deciliation and phase-locked to the respiration cycle. These results identify pPC as a likely site for gustatory influences on olfactory processing, which play an important role in food perception and preference formation.

Olfactory bulb: odor signals put into context.

In this issue, Doucette and colleagues demonstrate that information related to whether an odor is currently linked to reward can be observed uniquely in population activity in the olfactory bulb, changing our understanding both of what is coded by the first olfactory relay in the CNS and of how this coding is instantiated.

Audiovisual asynchrony detection in human speech.

Combining information from the visual and auditory senses can greatly enhance intelligibility of natural speech. Integration of audiovisual speech signals is robust even when temporal offsets are present between the component signals. In the present study, we characterized the temporal integration window for speech and nonspeech stimuli with similar spectrotemporal structure to investigate to what extent humans have adapted to the specific characteristics of natural audiovisual speech. We manipulated spectrotemporal structure of the auditory signal, stimulus length, and task context. Results indicate that the temporal integration window is narrower and more asymmetric for speech than for nonspeech signals. When perceiving audiovisual speech, subjects tolerate visual leading asynchronies, but are nevertheless very sensitive to auditory leading asynchronies that are less likely to occur in natural speech. Thus, speech perception may be fine-tuned to the natural statistics of audiovisual speech, where facial movements always occur before acoustic speech articulation.