Response Latency to Lingual Taste Stimulation Distinguishes Neuron Types Within the Geniculate Ganglion

Breza, Joseph M.; Nikonov, Alexander A.; Contreras, Robert J.

doi:10.1152/jn.00785.2009

Cited by 51 publications

(101 citation statements)

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“…This study adds a new layer to the dynamic coding hypothesis, demonstrating that quality-related temporal information is actively shaped by the animal's sampling behavior at the periphery. Although the anatomical segregation and sequential activation of receptive fields during licking likely account for much of the difference seen in reaction times between taste qualities, other sources of peripheral processing, such as transduction cascades and complex synaptic dynamics among taste receptor cells and primary afferent neurons, may also contribute (Breza et al, 2010;Roper, 2013). The results support and add important insights to previous work regarding the role of Figure 9.…”

Section: Discussionmentioning

confidence: 99%

“…As a control for the taste of salt, wild-type mice were initially trained in a salt-detection version of the task in which the no-stop stimulus was water and the stop stimulus was 100 mM NaCl. After reaching Ͼ80% correct performance levels for 3-4 d in a row, these mice were tested in the same task but with 20 M amiloride added to the stimulus solutions to block sodium taste transduction in taste receptor cells (Heck et al, 1984; Hill et al, 1990;Chandrashekar et al, 2010;Oka et al, 2013). Amiloride dropped performance levels in mice to chance levels, demonstrating that mice required the taste of salt to perform the task (Fig.…”

Section: Gustatory Stop-signal Task Is Learned Rapidly and Requires Tmentioning

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: Gustatory Stop-signal Task Is Learned Rapidly and Requires Tmentioning

confidence: 99%

Temporal Signatures of Taste Quality Driven by Active Sensing

2014

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“…Prior studies on peripheral neurons by Marowitz and Halpern (1977) and Breza et al (2010) showed that latency to response to sodium salts inversely followed concentration. The present analysis revealed an inverse relationship between concentration and response latency to sucrose in central neurons, and showed that this relationship was temperature dependent.…”

Section: Temperature and Timingmentioning

confidence: 98%

“…For one, latency was proposed to convey neural information used to represent taste stimuli (Breza et al 2010;Hallock and Di Lorenzo 2006). However, the present data introduce complications for this hypothesis for sucrose.…”

Section: Temperature and Timingmentioning

confidence: 99%

“…Analysis of neural data focused on the effect of temperature on the slope of the sucrose concentration-response function, which indexes rate of growth in response with concentration, and on latency to first spike to sucrose. The latency of a gustatory response could conceivably influence the evolution of taste perceptions during the time course of flavor (Green and Frankmann 1988) and contribute information about gustatory stimuli (Breza et al 2010;Graham et al 2014; Hallock and Di Lorenzo 2006). Results showed that change in temperature induced systematic change in both the slope and latency parameters of neural responses to the sucrose concentration series.…”

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Temperature systematically modifies neural activity for sweet taste

Wilson

Lemon

2014

Journal of Neurophysiology

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Wilson DM, Lemon CH. Temperature systematically modifies neural activity for sweet taste. J Neurophysiol 112: 1667-1677, 2014. First published June 25, 2014 doi:10.1152 doi:10. /jn.00368.2014 can modify neural and behavioral responses to taste stimuli that elicit "sweetness," a perception linked to intake of calorie-laden foods. However, the role of temperature in the neural representation of sweet taste is poorly understood. Here we made electrophysiological recordings from gustatory neurons in the medulla of inbred mice to study how adjustments in taste solution temperature to cool (18°C), ambient (22°C), and warm (30°C and 37°C) values changed the magnitude and latency of gustatory activity to sucrose (0, 0.05, 0.1, 0.17, 0.31, and 0.56 M). Analysis of 22 sucrose-best neurons revealed that temperature markedly influenced responses to sucrose, which, across concentrations, were largest when solutions were warmed to 30°C. However, reducing solution temperature from warm to ambient to cool progressively steepened the slope of the sucrose concentrationresponse function computed across cells (P Ͻ 0.05), indicating that mean activity to sucrose increased more rapidly with concentration steps under cooling than with warming. Thus the slope of the sucrose concentration-response function shows an inverse relation with temperature. Temperature also influenced latency to the first spike of the sucrose response. Across neurons, latencies were shorter when sucrose solutions were warmed and longer, by hundreds of milliseconds, when solutions were cooled (P Ͻ 0.05), indicating that temperature is also a temporal parameter of sucrose activity. Our findings reveal that temperature systematically modifies the timing of gustatory activity to sucrose in the mammalian brain and how this activity changes with concentration. Results further highlight how oral somatosensory cues function as physiological modulators of gustatory processing. taste; sucrose; temperature; latency; coding THE STUDY OF NEURAL CODING involves, in part, relating features of sensory stimuli to neural activity. For taste, this pursuit has largely focused on two stimulus features: the perceptual quality of the taste chemical and its concentration while dissolved in solution. Taste quality is a descriptive characteristic of taste stimuli transmitted, in part, through substitution (cf. Stevens 1961) of responses by different neurons. For instance, exchanging a taste stimulus of one quality (e.g., "sweet") for another (e.g., "salty") can cause a substitutive change in the neurons that respond maximally to the stimulus, leading to an associated change in the evoked response pattern. Concentration, on the other hand, is a physical property of taste stimuli that guides the magnitude of gustatory responses.Temperature is an additional physical property of taste stimuli that can modulate gustatory processing. Temperature strongly influences neural and behavioral responses to sweet stimuli. Gustatory activity to sucrose in peripheral nerves carrying sensory input fro...

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A survey of oral cavity afferents to the rat nucleus tractus solitarii

Corson

Aldridge

Wilmoth

et al. 2011

J of Comparative Neurology

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Visualization of myelinated fiber arrangements, cytoarchitecture, and projection fields of afferent fibers in tandem revealed input target selectivity in identified subdivisions of the nucleus tractus solitarii (NTS). The central fibers of the chorda tympani (CT), greater superficial petrosal (GSP), and glossopharyngeal (IX) nerves, three nerves that innervate taste buds in the oral cavity, prominently occupy the gustatorysensitive rostrocentral subdivision. In addition, CT and IX innervate and overlap in rostrolateral subdivision, which is primarily targeted by the lingual branch of the trigeminal nerve (LV). In rostrocentral subdivision, compared to the CT terminal field in rostrocentral subdivision, GSP appeared more rostral and medial, and IX was more dorsal and caudal. While IX and LV filled the rostrolateral subdivision diffusely, CT projected only to the dorsal and medial portions. The intermediate lateral subdivision received input from IX and LV but not CT or GSP. In the caudal NTS, the ventrolateral subdivision received notable innervation from CT, GSP, and LV, but not IX. No caudal subnuclei medial to solitary tract contained labeled afferent fibers. The data indicate selectivity of fiber populations within each nerve for functionally distinct subdivisions of the NTS, highlighting the possibility of equally distinct functions for CT in the rostrolateral NTS, and CT and GSP in the caudal NTS. Further, this provides a useful anatomical template to study the role of oral cavity afferents in the taste-responsive subdivision of the NTS as well as in subdivisions that regulate ingestion and other oromotor behaviors.

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Response Latency to Lingual Taste Stimulation Distinguishes Neuron Types Within the Geniculate Ganglion

Cited by 51 publications

References 49 publications

Temporal Signatures of Taste Quality Driven by Active Sensing

Temporal Signatures of Taste Quality Driven by Active Sensing

Temperature systematically modifies neural activity for sweet taste

A survey of oral cavity afferents to the rat nucleus tractus solitarii

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