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A Taste of What to Expect: Top-Down Modulation of Neural Coding in Rodent Gustatory Cortex

2012; Cell Press; Volume: 74; Issue: 2 Linguagem: Inglês

10.1016/j.neuron.2012.04.008

1097-4199

Christina Zelano, Jay A. Gottfried,

Multisensory perception and integration

A central aspect of sensory perception is the anticipation of forthcoming stimuli, allowing for a faster and more accurate assessment of the surrounding environment. A new study by Samuelsen et al., 2012Samuelsen C.L. Gardner M.P.H. Fontanini A. Neuron. 2012; 74 (this issue): 410-422Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar in this issue of Neuron highlights the neural mechanisms underlying the expectation of an imminent taste. A central aspect of sensory perception is the anticipation of forthcoming stimuli, allowing for a faster and more accurate assessment of the surrounding environment. A new study by Samuelsen et al., 2012Samuelsen C.L. Gardner M.P.H. Fontanini A. Neuron. 2012; 74 (this issue): 410-422Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar in this issue of Neuron highlights the neural mechanisms underlying the expectation of an imminent taste. In the 1998 film The Truman Show, a group of television producers labors with Herculean passion to manufacture an artificial but believable world for an insurance salesman, Truman Burbank (played by actor Jim Carrey), who unwittingly stars in his own reality show. As each new day dawns, or is meant to dawn, in the town of Seahaven, the order is shouted within the TV control room to "cue the sun!" The well-timed appearance of a heavenly orb—perhaps the most reliable and dependable sensory cue known to roosters and humans alike—signals morning and launches Truman out of bed. Hollywood actors notwithstanding, human and nonhuman animals of all sorts readily utilize sensory cues to predict events and guide behavior. External cues, typically arriving in visual, olfactory, auditory, or verbal format, may announce a general state-based change in behavior or in the environmental milieu, for example, the sound of a dinner bell signaling that food is imminent. Alternatively, external cues may forecast more specific information about the identity of an upcoming event, enhancing sensory discrimination, response speed, and perceptually based decisions. The roasted smell of coffee in the morning sets up an expectation of coffee flavor that is met upon sipping from your breakfast mug. Not infrequently, an external cue can be uninformative or misinformative, or absent altogether. Having learned to predict the presence of something that is actually not there has adverse behavioral consequences, reducing discrimination and response speed, and creating cognitive dissonance. Finding that the same coffee smell leads not to coffee but, unexpectedly, to black tea (sipping from the wrong mug, for example) may result in breakfast dismay. The majority of neuroscientific research on sensory expectation, awareness, and prediction has focused on the visual system (Gilbert and Sigman, 2007Gilbert C.D. Sigman M. Neuron. 2007; 54: 677-696Abstract Full Text Full Text PDF PubMed Scopus (594) Google Scholar, Kouider and Dehaene, 2007Kouider S. Dehaene S. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2007; 362: 857-875Crossref PubMed Scopus (492) Google Scholar, Summerfield and Egner, 2009Summerfield C. Egner T. Trends Cogn. Sci. (Regul. Ed.). 2009; 13: 403-409Abstract Full Text Full Text PDF PubMed Scopus (601) Google Scholar), whereas comparable studies of the chemical senses—smell and taste—are, well, to be unexpected. In this issue of Neuron, Samuelsen et al., 2012Samuelsen C.L. Gardner M.P.H. Fontanini A. Neuron. 2012; 74 (this issue): 410-422Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar systematically explore how prestimulus cues can modulate network properties of the rodent gustatory system to shape sensory responsiveness at the perceptual level. By bringing together electrophysiological recordings in awake behaving rats, an elegant psychophysical paradigm, and pharmacological inactivation techniques, these investigators were able to show that cue-triggered expectation modulates activity in gustatory cortex (GC) in an amygdala-dependent manner, with consequent enhancement of taste coding. On each trial, rats were trained to wait ∼40 s for an auditory tone, which indicated the availability of one of four tastants, either sucrose, NaCl, citric acid, or quinine. The rat then had 3 s to press a lever that resulted in the self-administration of aqueous tastant directly into the mouth via an intraoral cannula. Behavioral responses were compared to a control, "unexpected" condition, in which tastants were delivered via the cannula at random times during the pretone period. Delivery of expected and unexpected tastes were intermingled throughout the experiment (rather than presented in separate blocks) to eliminate any attentional shifts or satiety-related confounds that might have developed over time. Note that on "expected" trials, the tone signaled only the general availability of tastant; there was no predictive information regarding specific tastant identities. Simultaneously with the behavioral task, single-unit responses in GC were recorded from movable bundles of 16 extracellular electrodes, providing a way to examine not only single-neuron activity, but also firing patterns across neural ensembles. Findings revealed faster and more accurate coding in GC in the earliest phase of the task when taste delivery had been expected: in the first 125 ms following taste onset, ensemble activity patterns allowed better stimulus discrimination of expected (versus unexpected) tastes. Both a sharpening of taste-specific response tuning as well as a reduction in response variability were observed in this earliest posttastant time bin, further accentuating the robust effect of cueing on gustatory information processing. In the absence of cueing, taste coding and classification were delayed. Analysis of post-stimulus activity in GC was complemented by an analysis of prestimulus activity, with a focus on the expectation period preceding taste delivery. Notably, on expected trials, spike firing rates in GC progressively increased upon presentation of the cue, peaking in the last time-bin before delivery of tastant. As might be predicted, these effects were not observed in the period preceding delivery of unexpected tastants, and response differences between expected and unexpected trials were maximal in the prestimulus period before tastant had reached the tongue. Using both correlation analyses and principal components analysis (PCA), the investigators also found that GC activity in the first 125 ms bin following the cue (on expected trials) roughly resembled activity in the first 125 ms bin following tastant (on unexpected trials). These latter findings raise the intriguing idea that cue-evoked states of gustatory expectation may generate a "preplay" of early information coding in response to unexpected taste. Well-designed control experiments helped rule out the possibility that cue-evoked responses in GC could have arisen from expectation-related differences in motor activity, including lever pressing, mouth movements, or other oromotor reactions. To the extent that the prestimulus, cue-related effects in GC are in fact anticipatory, it reasonably follows that these responses might be under top-down control. In order to test this hypothesis, the investigators performed dual recordings from GC and from the basolateral amygdala (BLA), a region that has been implicated in network processing of taste coding (Grossman et al., 2008Grossman S.E. Fontanini A. Wieskopf J.S. Katz D.B. J. Neurosci. 2008; 28: 2864-2873Crossref PubMed Scopus (124) Google Scholar) and anticipatory states (Roesch et al., 2010Roesch M.R. Calu D.J. Esber G.R. Schoenbaum G. J. Neurosci. 2010; 30: 2464-2471Crossref PubMed Scopus (126) Google Scholar), and sends direct projections to rodent GC (Saper, 1982Saper C.B. J. Comp. Neurol. 1982; 210: 163-173Crossref PubMed Scopus (494) Google Scholar). Like GC, the BLA responded to the auditory cues, but even more quickly, such that the average latency of cue-induced activity in BLA was on average 16 ms shorter than that of GC, a significant effect. These data, along with the finding of a cue-dependent strengthening of cross-correlation values between BLA and GC, are consistent with a modulatory influence of BLA on anticipatory activity in GC. Finally, to confirm whether BLA played a causal role in GC response dynamics, cue-evoked activity was examined before and after inactivation of the BLA, through local bilateral injection of NBQX, an AMPA receptor antagonist. This manipulation impressively abolished the cue-evoked activity in GC, highlighting the direct involvement of BLA in establishing gustatory states of cortical expectation. Together these findings extend the traditional role of BLA in enriching sensory codes with emotional value. The findings presented here mark an important first step in understanding how expectation influences circuit activity in rodent GC, and add important information to the small but growing body of work exploring the neurocognitive interactions among attention, expectation, and chemosensory processing (Kerfoot et al., 2007Kerfoot E.C. Agarwal I. Lee H.J. Holland P.C. Learn. Mem. 2007; 14: 581-589Crossref PubMed Scopus (45) Google Scholar, Nitschke et al., 2006Nitschke J.B. Dixon G.E. Sarinopoulos I. Short S.J. Cohen J.D. Smith E.E. Kosslyn S.M. Rose R.M. Davidson R.J. Nat. Neurosci. 2006; 9: 435-442Crossref PubMed Scopus (157) Google Scholar, Saddoris et al., 2009Saddoris M.P. Holland P.C. Gallagher M. J. Neurosci. 2009; 29: 15386-15396Crossref PubMed Scopus (45) Google Scholar, Stapleton et al., 2007Stapleton J.R. Lavine M.L. Nicolelis M.A. Simon S.A. Front Neurosci. 2007; 1: 161-174Crossref PubMed Scopus (26) Google Scholar, Veldhuizen et al., 2007Veldhuizen M.G. Bender G. Constable R.T. Small D.M. Chem. Senses. 2007; 32: 569-581Crossref PubMed Scopus (142) Google Scholar, Veldhuizen et al., 2011Veldhuizen M.G. Douglas D. Aschenbrenner K. Gitelman D.R. Small D.M. J. Neurosci. 2011; 31: 14735-14744Crossref PubMed Scopus (61) Google Scholar, Zelano et al., 2005Zelano C. Bensafi M. Porter J. Mainland J. Johnson B. Bremner E. Telles C. Khan R. Sobel N. Nat. Neurosci. 2005; 8: 114-120Crossref PubMed Scopus (195) Google Scholar, Zelano et al., 2011Zelano C. Mohanty A. Gottfried J.A. Neuron. 2011; 72: 178-187Abstract Full Text Full Text PDF PubMed Scopus (122) Google Scholar). The intriguing demonstration of gustatory information playback in GC during taste expectation raises an important question: what exactly is being played back prior to taste delivery? In the experimental design, the cue signaled to the rat that taste was imminent, but contained no information about stimulus identity or valence. Therefore the anticipatory activity in GC cannot be said to be playing back sensory-specific information about a particular stimulus. In this manner, the results differ from recent work in the olfactory system, suggesting that sensory-specific predictive templates are encoded in piriform cortex in advance of stimulus receipt (Zelano et al., 2011Zelano C. Mohanty A. Gottfried J.A. Neuron. 2011; 72: 178-187Abstract Full Text Full Text PDF PubMed Scopus (122) Google Scholar). The results also fundamentally differ from recent findings in human GC, in which breaches of taste identity expectation result in modulatory effects in primary taste cortex (Nitschke et al., 2006Nitschke J.B. Dixon G.E. Sarinopoulos I. Short S.J. Cohen J.D. Smith E.E. Kosslyn S.M. Rose R.M. Davidson R.J. Nat. Neurosci. 2006; 9: 435-442Crossref PubMed Scopus (157) Google Scholar, Veldhuizen et al., 2011Veldhuizen M.G. Douglas D. Aschenbrenner K. Gitelman D.R. Small D.M. J. Neurosci. 2011; 31: 14735-14744Crossref PubMed Scopus (61) Google Scholar). Rather, the new results suggest that cue-induced GC activity—which resembles stimulus-induced GC activity during delivery of uncued tastes—reflects a preparatory signal that readies or primes the gustatory system to initiate oral exploration and taste detection. More broadly, the signal generated during taste expectancy may relate to attention or arousal to gustatory inputs, as shown by Veldhuizen et al., 2007Veldhuizen M.G. Bender G. Constable R.T. Small D.M. Chem. Senses. 2007; 32: 569-581Crossref PubMed Scopus (142) Google Scholar in human GC. Achieving robust modulation of expectancy states, especially in such a way that allows for accurate stimulus control, is no trivial feat when it comes to rats (nor when it comes to Truman Burbank for that matter). In this respect, the use of an intraoral cannula to delineate cognitive influences on taste coding is an invaluable tool, with the further advantage of reducing somatosensory-related confounds associated with other taste stimulation methods. It is worth noting that these benefits do come at the price of a relatively atypical mode of stimulus delivery. Apart from slack-jawed filter feeders combing for sea crumbs, most animals are not caught unawares with a food suddenly appearing in their mouths. Put differently: because our taste-sensing organs (tongues) reside behind closed lips, we always control our decision to taste, either sticking out the tongue or putting food inside the mouth. Thus, the experience of encountering an unannounced taste through an intraoral cannula is not only unexpected, but possibly also quite bewildering. In the current study, such complications were minimized, first, because expected and unexpected tastants were both delivered via the cannula, and second, because the rats were habituated to receive fluids through the cannula for at least a month before the main experiment. Going forward, it will be interesting to explore how variations in taste sampling influence neural coding in the gustatory system. Irrespective of taste delivery methods, it will be important to consider the circuit physiology of the gustatory network when the animal is cued to expect specific tastes. Will expectation of a specific taste, compared to general taste, produce faster coding in GC? Will neural ensemble patterns evoked by taste-specific cues resemble patterns evoked by the specific tastants themselves? And finally, will the BLA play an equivalent top-down role, or might other cortical regions be more critical for the emergence of sensory-specific gustatory representations prior to actual stimulus delivery? Future work will undoubtedly bring clarity to these questions, and hopefully will help identify common neurobiological ground across human and animal studies of the taste system. Effects of Cue-Triggered Expectation on Cortical Processing of TasteSamuelsen et al.NeuronApril 26, 2012In BriefSamuelsen et al. examine the effects of expectation on gustatory processing and find that tastants are processed more rapidly if expected. This enhanced processing relates to anticipatory priming of gustatory cortical networks by auditory cues. Full-Text PDF Open Archive