Glossopharyngeal Nerve Regeneration Is Essential for the Complete Recovery of Quinine-Stimulated Oromotor Rejection Behaviors and Central Patterns of Neuronal Activity in the Nucleus of the Solitary Tract in the Rat

King, Camille Tessitore; Garcea, Mircea; Spector, Alan C.

doi:10.1523/jneurosci.20-22-08426.2000

Cited by 63 publications

(81 citation statements)

References 40 publications

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“…The gustatory stop-signal task also adds to the growing body of literature using head-restrained mouse behavioral paradigms for studying sensory processing (Komiyama et al, 2010;Smear et al, 2011). Although head restraint has been used by others for studying taste in rodents (Nakamura and Norgren, 1993;Katz et al, 2001;Samuelsen et al, 2012), our task differs significantly in stimulus delivery and in the ability to measure taste guided decisions with high temporal resolution.…”

Section: Discussionmentioning

confidence: 99%

“…6). Interestingly, Spector and colleagues provide convincing data in rat that elimination of the IX has little effect on bitter taste perception, but does influence gape responses and unconditioned licking to bitter stimuli (King et al, 1999;Markison et al, 1999;King et al, 2000;Geran and Travers, 2011), suggesting that taste buds other than those innervated by IX carry bitter taste signals to the brain.…”

Section: Brief-access Testing Of Quinine In Head-restrained Micementioning

confidence: 99%

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Temporal Signatures of Taste Quality Driven by Active Sensing

2014

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Animals actively acquire sensory information from the outside world, with rodents sniffing to smell and whisking to feel. Licking, a rapid motor sequence used for gustation, serves as the primary means of controlling stimulus access to taste receptors in the mouth. Using a novel taste-quality discrimination task in head-restrained mice, we measured and compared reaction times to four basic taste qualities (salt, sour, sweet, and bitter) and found that certain taste qualities are perceived inherently faster than others, driven by the precise biomechanics of licking and functional organization of the peripheral gustatory system. The minimum time required for accurate perception was strongly dependent on taste quality, ranging from the sensory-motor limits of a single lick (salt, ϳ100 ms) to several sampling cycles (bitter, Ͼ500 ms). Further, disruption of sensory input from the anterior tongue significantly impaired the speed of perception of some taste qualities, with little effect on others. Overall, our results show that active sensing may play an important role in shaping the timing of taste-quality representations and perception in the gustatory system. IntroductionAnimals acquire information about their environment through active sensing. Rodents use rapid stereotyped behaviors such as sniffing and whisking to sample olfactory and tactile stimuli, with neural activity in these systems precisely aligned to the cycles of sampling behavior (Hill et al., 2011;Shusterman et al., 2011; Wachowiak, 2011). In the gustatory system, taste stimuli are sensed through the active process of licking, a rapid and stereotyped behavior that is the gustatory analog of sniffing in olfaction (Travers et al., 1997). During licking, taste stimuli are actively pulled into the mouth by the animal, creating a natural and sequential flow of information beginning from the tip of the tongue and following throughout the oral cavity (Reis et al., 2010). Although a prerequisite for tasting, the role of licking in shaping sensory processing in the gustatory system is poorly understood due in part to the use of a variety of experimental methods for delivering liquid taste stimuli that circumvent or alter the natural sequence of events associated with licking and active sensing (Katz et al., 2002b;MacDonald et al., 2009). Injection of liquid stimuli into the mouth of alert animals via intra-oral cannulas (IOCs) or pressurized lick spouts provides a rapid and reliable method of stimulus delivery for studying taste coding and perception. However, pressurized lick spouts and IOCs add a degree of passivity into the active process of tasting, potentially obscuring important aspects of gustatory sensory processing. Unlike other sensory systems that transmit information from the receptor organ to the brain through a single nerve, neural information about taste is brought into the brain by three separate nerves with anatomically and functionally distinct receptive fields (Shingai and Beidler, 1985; Spector and Travers, 2005; Spector and Glendinning,...

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Section: Discussionmentioning

confidence: 99%

Section: Brief-access Testing Of Quinine In Head-restrained Micementioning

confidence: 99%

Temporal Signatures of Taste Quality Driven by Active Sensing

2014

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“…Although the latter functions have been the primary focus of GI chemoreceptor research to date, the presence of bitter (T2R) receptors in the postoral GI tract is consistent with a role for chemoreceptors in defensive GI functions as well (45). In the gustatory taste system, bitter taste receptors are wired to rejection responses to limit the ingestion of noxious foods (25), but, in the event that these foods are ingested, GI T2Rs may provide a second line of defense. Indeed, application of the bitter compound DB directly to GI cells stimulates the release of CCK and slows gastric emptying (8,17,18).…”

Section: Experiments 1: Rats Rapidly Suppress Ongoing Intake In Re-mentioning

confidence: 92%

Ongoing ingestive behavior is rapidly suppressed by a preabsorptive, intestinal “bitter taste” cue

Schier

Davidson

Powley

2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Schier LA, Davidson TL, Powley TL. Ongoing ingestive behavior is rapidly suppressed by a preabsorptive, intestinal "bitter taste" cue. Am J Physiol Regul Integr Comp Physiol 301: R1557-R1568, 2011. First published August 24, 2011 doi:10.1152/ajpregu.00344.2011.-The discovery that cells in the gastrointestinal (GI) tract express the same molecular receptors and intracellular signaling components known to be involved in taste has generated great interest in potential functions of such post-oral "taste" receptors in the control of food intake. To determine whether taste cues in the GI tract are detected and can directly influence behavior, the present study used a microbehavioral analysis of intake, in which rats drank from lickometers that were programmed to simultaneously deliver a brief yoked infusion of a taste stimulus to the intestines. Specifically, in daily 30-min sessions, thirsty rats with indwelling intraduodenal catheters were trained to drink hypotonic (0.12 M) sodium chloride (NaCl) and simultaneously self-infuse a 0.12 M NaCl solution. Once trained, in a subsequent series of intestinal taste probe trials, rats reduced licking during a 6-min infusion period, when a bitter stimulus denatonium benzoate (DB; 10 mM) was added to the NaCl vehicle for infusion, apparently conditioning a mild taste aversion. Presentation of the DB in isomolar lithium chloride (LiCl) for intestinal infusions accelerated the development of the response across trials and strengthened the temporal resolution of the early licking suppression in response to the arrival of the DB in the intestine. In an experiment to evaluate whether CCK is involved as a paracrine signal in transducing the intestinal taste of DB, the CCK-1R antagonist devazepide partially blocked the response to intestinal DB. In contrast to their ability to detect and avoid the bitter taste in the intestine, rats did not modify their licking to saccharin intraduodenal probe infusions. The intestinal taste aversion paradigm developed here provides a sensitive and effective protocol for evaluating which tastants-and concentrations of tastants-in the lumen of the gut can control ingestion. chemoreceptor; gastrointestinal; denatonium benzoate; food learning; cholecystokinin CHEMORECEPTORS ARE INDISPENSABLE to the control of food intake. As taste receptors on the tongue and in the oral cavity, they supply signals critical for accepting and rejecting foods for consumption, promoting intake of palatable foods, and preparing the digestive system for the arrival of nutrients. Complementary to this early oral sensory processing, chemoreceptors in the stomach and intestines transduce signals from the lumen to adjust motility, secrete digestive enzymes, and initiate satiation (cf., 24). Accordingly, the gastrointestinal (GI) tract has been conventionally considered to have a more or less continuous sensory surface for tracking meals to engage and revise apposite and coordinated responses particular to the properties of the food and the body's physiological state. Despite th...

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“…Previous studies demonstrated that bitter-elicited FLI is densest in the medial third of the NST (6,26,32,34,61). To evaluate whether this medial region was more effective for eliciting gaping, we compared placements in the medial onethird (n ϭ 13 for current series, n ϭ 11 for train duration) with those in the lateral two-thirds (n ϭ 12 for current series, n ϭ 11 for train duration) of the nucleus.…”

Section: Placements In the Nst: Medial Vs Lateralmentioning

confidence: 99%

“…In contrast, elimination of input from the IXth nerve has only minimal impact on operant behaviors involving bitter (and other) discriminations (51) but significantly reduces the number and abolishes the distinctive topographic pattern of bitterinduced Fos neurons of the NST (32)(33)(34). Despite minimal effects on operant behavior, IXth nerve transection profoundly impairs the unconditioned oral rejection reflex (gaping), a behavior preferentially elicited by bitter stimuli (19,33,57).…”

mentioning

confidence: 99%

Licking and gaping elicited by microstimulation of the nucleus of the solitary tract

Kinzeler¹,

Travers²

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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Intraoral infusions of bitter tastants activate expression of the immediate-early gene c-Fos in neurons located in the medial third of the rostral nucleus of the solitary tract (rNST). The distribution of these neurons is distinct from that activated by sour or sweet stimuli. Bitter stimuli are also distinctive because of their potency for eliciting gaping, an oral reflex that functions to actively reject potentially toxic substances. Glossopharyngeal nerve transection profoundly reduces, whereas decerebration spares, the bitter-evoked Fos-like immunoreactivity (FLI) pattern and gaping, implicating the medial rNST as a substrate for the sensory limb of oral rejection. The present experiment tested this hypothesis using microstimulation (100 Hz, 0.2 ms, 5-40 microA) to activate the rNST in awake rats. NST microstimulation elicited licking and gaping, and gaping was evoked from a restricted rNST region. The results indicated some topographic organization in sites effective for evoking gaping, but, in direct conflict with the hypothesis, lateral sites farther from bitter-evoked FLI were more effective than medial sites centered closer to FLI-expressing neurons. The gape-effective sites resemble locations of bitter-responsive neurons recently observed in neurophysiological recordings. These results indicate that bitter-responsive rNST neurons critical for triggering gaping may not express FLI and imply an alternate function for bitter-responsive neurons that do.

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Glossopharyngeal Nerve Regeneration Is Essential for the Complete Recovery of Quinine-Stimulated Oromotor Rejection Behaviors and Central Patterns of Neuronal Activity in the Nucleus of the Solitary Tract in the Rat

Cited by 63 publications

References 40 publications

Temporal Signatures of Taste Quality Driven by Active Sensing

Temporal Signatures of Taste Quality Driven by Active Sensing

Ongoing ingestive behavior is rapidly suppressed by a preabsorptive, intestinal “bitter taste” cue

Licking and gaping elicited by microstimulation of the nucleus of the solitary tract

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