GABA-mediated corticofugal inhibition of taste-responsive neurons in the nucleus of the solitary tract

Smith, David V.; Li, Chengshu

doi:10.1016/s0006-8993(99)02484-1

Cited by 80 publications

(59 citation statements)

References 46 publications

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“…This spontaneous release of inhibitory neurotransmitter would be an important source of rNST tonic inhibition reported by investigators using both intracellular and extracellular recordings in vivo and in brain slices (Smith and Li 1998;Wang and Bradley 1993). Synaptic activation of the tonically firing neurons would augment the tonic level of inhibition.…”

Section: Repetitive Firing Patterns and Membrane Propertiesmentioning

confidence: 93%

“…Finally, the slice preparation effectively eliminates all ascending and descending connections to rNST neurons. Investigators have shown using in vivo recording that stimulation of gustatory cortex results in the modulation of spontaneous activity and responses to chemicals of rNST neurons (Smith and Li 2000). Elimination of the ascending and descending input may possibly alter the response properties of the in vitro recordings, accounting for some of the discrepancies.…”

Section: Repetitive Firing Patterns and Membrane Propertiesmentioning

confidence: 99%

“…Taste buds on the larynx and pharynx, which do not have a gustatory function, are innervated by the superior laryngeal branch of the vagus (Xth) nerve (Smith and Hanamori 1991). The central projections of these afferent neurons enter the brain stem to form the solitary tract (ST) and synapse with neurons in the rostral nucleus of the solitary tract (rNST).…”

Section: Introductionmentioning

confidence: 99%

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Properties of GABAergic Neurons in the Rostral Solitary Tract Nucleus in Mice

Wang

Bradley

2010

Journal of Neurophysiology

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The rostral nucleus of the solitary tract (rNST) plays a pivotal role in taste processing. The rNST contains projection neurons and interneurons that differ in morphology and intrinsic membrane properties. Although characteristics of the projection neurons have been detailed, similar information is lacking on the interneurons. We determined the intrinsic properties of the rNST GABAergic interneurons using a transgenic mouse model that expresses enhanced green fluorescent protein under the control of a GAD67 promoter. Glutamic acid decarboxylase-green fluorescent protein (GAD67-GFP) neurons were distributed throughout the rNST but were concentrated in the ventral subdivision with minimal interaction with the terminal field of the afferent input. Furthermore, the density of the GAD67-GFP neurons decreased in more rostral areas of rNST. In whole cell recordings, GAD67-GFP neurons responded with either an initial burst (73%), tonic (18%), or irregular (9%) discharge pattern of action potentials (APs) in response to membrane depolarization. These three groups also differed in passive and AP characteristics. Initial burst neurons had small ovoid or fusiform cell bodies, whereas tonic firing neurons had large multipolar or fusiform cell bodies. Irregular firing neurons had larger spherical soma. Some of the initial burst and tonic firing neurons were also spontaneously active. The GAD67-GFP neurons could also be categorized in subgroups based on colocalization with somatostatin and parvalbumin immunolabeling. Initial burst neurons would transmit the early dynamic portion of the encoded sensory stimuli, whereas tonic firing neurons could respond to both dynamic and static components of the sensory input, suggesting different roles for GAD67-GFP neurons in taste processing.

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Section: Repetitive Firing Patterns and Membrane Propertiesmentioning

confidence: 93%

Section: Repetitive Firing Patterns and Membrane Propertiesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Properties of GABAergic Neurons in the Rostral Solitary Tract Nucleus in Mice

Wang

Bradley

2010

Journal of Neurophysiology

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“…We suggest that both properties may be used to encode changes in concentration. We speculate that, in response to concentration changes, such varied behavior could be a consequence of the fact that GC receives (and transmits) information from other cortical and subcortical areas (Smith and Li, 2000;Lundy and Norgren, 2004) and that these areas will respond differentially to different tastants and concentrations of tastants. In particular, tastants such as quinine and sucrose possess different hedonic valences, so additional networks may be recruited to reflect different palatabilities (Small et al, 2003;Sewards, 2004).…”

Section: Codingmentioning

confidence: 99%

Rapid Taste Responses in the Gustatory Cortex during Licking

Stapleton¹,

Lavine²,

Wolpert³

et al. 2006

J. Neurosci.

135

149

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Rapid tastant detection is necessary to prevent the ingestion of potentially poisonous compounds. Behavioral studies have shown that rats can identify tastants in ϳ200 ms, although the electrophysiological correlates for fast tastant detection have not been identified. For this reason, we investigated whether neurons in the primary gustatory cortex (GC), a cortical area necessary for tastant identification and discrimination, contain sufficient information in a single lick cycle, or ϳ150 ms, to distinguish between tastants at different concentrations. This was achieved by recording neural activity in GC while rats licked four times without a liquid reward, and then, on the fifth lick, received a tastant (FR5 schedule). We found that 34% (61 of 178) of GC units were chemosensitive. The remaining neurons were activated during some phase of the licking cycle, discriminated between reinforced and unreinforced licks, or processed task-related information. Chemosensory neurons exhibited a latency of 70 -120 ms depending on concentration, and a temporally precise phasic response that returned to baseline in tens of milliseconds. Tastant-responsive neurons were broadly tuned and responded to increasing tastant concentrations by either increasing or decreasing their firing rates. In addition, some responses were only evoked at intermediate tastant concentrations. In summary, these results suggest that the gustatory cortex is capable of processing multimodal information on a rapid timescale and provide the physiological basis by which animals may discriminate between tastants during a single lick cycle.

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“…Many rNST neurons contain GABA (Lasiter and Kachele 1988) and about half of the synaptic terminals in the rNST are GABAergic (Leonard et al 1999). In addition, both in vitro and in vivo application of GABA inhibits rNST neurons, and GABA is also involved in a corticofugal tonic inhibition of rNST neurons Li 1998, 2000;Wang and Bradley 1993).…”

Section: Introductionmentioning

confidence: 99%

Frequency-Dependent Properties of Inhibitory Synapses in the Rostral Nucleus of the Solitary Tract

Grabauskas

Bradley

2003

Journal of Neurophysiology

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Grabauskas, Gintautas and Robert M. Bradley. Frequency-dependent properties of inhibitory synapses in the rostral nucleus of the solitary tract. J Neurophysiol 89: 199 -211, 2003; 10.1152/jn.00963.2001. To explore the parameters that define the characteristics of either inhibitory postsynaptic potentials (IPSP) or currents (IPSC) in the gustatory nucleus of the solitary tract (rNST), whole cell patchclamp recordings were made in horizontal brain stem slices of newborn rats. Neurons were labeled with biocytin to confirm both their location and morphology. IPSPs or IPSCs were evoked by delivering either single, paired-pulse, or tetanic stimulus shocks (0.1-ms duration) via a bipolar stimulating electrode placed on the rNST. Pure IPSP/IPSCs were isolated by the use of glutamate receptor antagonists. For 83% of the single-stimulus-evoked IPSCs, the decay time course was fitted with two exponentials having average time constants of 38 and 181 ms, respectively, while the remainder could be fitted with one exponential of 59 ms. Paired-pulse stimulation resulted in summation of the amplitude of the conditioning and test-stimulus-evoked IPSCs. The decay time course of the test-stimulus-evoked IPSC was slower when compared to the decay time of the conditioning stimulus IPSC. Repeated stimulation resulted in an increase in the decay time of the IPSP/Cs where each consecutive stimulus contributed to prolongation of the decay time constant. Most of the IPSP/Cs resulting from a 1-s Ն 30-Hz tetanic stimulus exhibited an S-shaped decay time course where the amplitude of the IPSP/Cs after termination of the stimulus was initially sustained before starting to decay back to the resting membrane potential. Elevation of extracellular Ca 2ϩ concentration 10 mM resulted in an increase in the amplitude and decay time of single-stimulus shock-evoked IPSP/Cs. The benzodiazepine GABA A receptor modulator diazepam increased the decay time of single-stimulus shock-evoked IPSCs. However, application of diazepam did not affect the decay time of tetanicstimulation-evoked IPSP/Cs. These results suggest that the decay time of single-stimulus-evoked IPSCs is defined either by receptor kinetics or neurotransmitter clearance from the synaptic cleft or both, while the decay time course of the tetanic stimulus evoked IPSP/Cs is defined by neurotransmitter diffusion from the synaptic cleft. During repetitive stimulation, neurotransmitter accumulates in the synaptic cleft prolonging the decay time constant of the IPSCs. High-frequency stimulation elevates the GABA concentration in the synaptic cleft, which then oversaturates the postsynaptic receptors, and, as a consequence, after termination of the tetanic stimulus, the amplitude of IPSP/Cs is sustained resulting in an S shaped decay time course. This activity-dependent plasticity at GABAergic synapses in the rNST is potentially important in the encoding of taste responses because the dynamic range of stimulus frequencies that result in synaptic plasticity (0 -70 Hz) corresponds to the breadth of freq...

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GABA-mediated corticofugal inhibition of taste-responsive neurons in the nucleus of the solitary tract

Cited by 80 publications

References 46 publications

Properties of GABAergic Neurons in the Rostral Solitary Tract Nucleus in Mice

Properties of GABAergic Neurons in the Rostral Solitary Tract Nucleus in Mice

Rapid Taste Responses in the Gustatory Cortex during Licking

Frequency-Dependent Properties of Inhibitory Synapses in the Rostral Nucleus of the Solitary Tract

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