Taste-responsive neurons in the nucleus of the solitary tract receive gustatory information from both sides of the tongue in the hamster

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Li CS, Lu DP, Cho YK. Descending projections from the nucleus accumbens shell excite activity of taste-responsive neurons in the nucleus of the solitary tract in the hamster. J Neurophysiol 113: 3778-3786, 2015. First published March 5, 2015 doi:10.1152/jn.00362.2014.-The nucleus of the solitary tract (NST) and the parabrachial nuclei (PbN) are the first and second relays in the rodent central taste pathway. A series of electrophysiological experiments revealed that spontaneous and taste-evoked activities of brain stem gustatory neurons are altered by descending input from multiple forebrain nuclei in the central taste pathway. The nucleus accumbens shell (NAcSh) is a key neural substrate of reward circuitry, but it has not been verified as a classical gustatory nucleus. A recent in vivo electrophysiological study demonstrated that the NAcSh modulates the spontaneous and gustatory activities of hamster pontine taste neurons. In the present study, we investigated whether activation of the NAcSh modulates gustatory responses of the NST neurons. Extracellular single-unit activity was recorded from medullary neurons in urethane-anesthetized hamsters. After taste response was confirmed by delivery of sucrose, NaCl, citric acid, and quinine hydrochloride to the anterior tongue, the NAcSh was stimulated bilaterally with concentric bipolar stimulating electrodes. Stimulation of the ipsilateral and contralateral NAcSh induced firings from 54 and 37 of 90 medullary taste neurons, respectively. Thirty cells were affected bilaterally. No inhibitory responses or antidromic invasion was observed after NAcSh activation. In the subset of taste cells tested, high-frequency electrical stimulation of the NAcSh during taste delivery enhanced taste-evoked neuronal firing. These results demonstrate that two-thirds of the medullary gustatory neurons are under excitatory descending influence from the NAcSh, which is a strong indication of communication between the gustatory pathway and the mesolimbic reward pathway. medullary neuron; gustatory neuron; reward; modulation; in vivo electrophysiology GUSTATORY NEURONS in the nucleus of the solitary tract (NST) in the medulla receive taste information from peripheral taste cells and transfer it to the parabrachial nuclei (PbN) in the pons of rodents (Cho et al.

Section: Histologysupporting

confidence: 85%

Descending projections from the nucleus accumbens shell excite activity of taste-responsive neurons in the nucleus of the solitary tract in the hamster

Cho

2015

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“…The descending influence from the NAcSh to gustatory PbN cells was characterized by its extensiveness (88 of 98 cells, 90%) and by its exclusively inhibitory nature. In previous electrophysiological studies, we demonstrated that gustatory neurons in the hamster brain stem are under descending influences from the VPM, gustatory cortex, and various forebrain nuclei, including the LH, CeA, and BNST Cho et al 2002aCho et al , 2002bCho et al , 2003Li and Cho 2006;Li et al 2002Li et al , 2005Li et al , 2008Mao et al 2008). The influences from these forebrain nuclei to gustatory cells in the PbN and NST showed different characteristics.…”

Section: Discussionmentioning

confidence: 87%

Descending projections from the nucleus accumbens shell suppress activity of taste-responsive neurons in the hamster parabrachial nuclei

Chung

et al. 2012

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The parabrachial nuclei (PbN), the second central relay for the gustatory pathway, transfers taste information to various forebrain gustatory nuclei and to the gustatory cortex. The nucleus accumbens is one of the critical neural substrates of the reward system, and the nucleus accumbens shell region (NAcSh) is associated with feeding behavior. Taste-evoked neuronal responses of PbN neurons are modulated by descending projections from the gustatory nuclei in the forebrain. In the present study, we investigated whether taste-responsive neurons in the PbN project to the NAcSh and whether pontine gustatory neurons are subject to modulatory influence from the NAcSh in urethane-anesthetized hamsters. Extracellular single-unit activity was recorded in the PbN, and taste responses were confirmed by the delivery of 32 mM sucrose, NaCl, quinine hydrochloride, and 3.2 mM citric acid to the anterior tongue. The NAcSh was then stimulated (0.5 ms, ≤100 μA) bilaterally using concentric bipolar stimulating electrodes. A total of 98 taste neurons were recorded from the PbN. Eighteen neurons were antidromically invaded from the NAcSh, mostly the ipsilateral NAcSh (n = 16). Stimulation of the ipsilateral and contralateral NAcSh suppressed the neuronal activity of 88 and 55 neurons, respectively; 52 cells were affected bilaterally. In a subset of pontine neurons tested, electrical stimulation of the NAcSh during taste stimulation also suppressed taste-evoked neuronal firing. These results demonstrated that taste-responsive neurons in the PbN not only project to the NAcSh but also are under substantial descending inhibitory influence from the bilateral NAcSh.

“…Note that the diagrams were based on the left (ipsilateral) side of the networks. A: projections from the recorded neuron to the stimulating site: 1: Li et al 2008;Norgren et al 1989;Smith et al 1983; 2: present experiment; 3: Cho et al 2002a;Monroe and Di Lorenzo 1995;Ogawa et al 1984b, present experiment;4: Cho et al 2002b4: Cho et al , 20035: Li et al 2005;Norgren 1974Norgren , 19766: Hayama and Ogawa 1987;Mao et al 2008;Norgren 1974Norgren , 19767: Li and Cho 2006;8: Ogawa and Nomura 1988;9: Cho et al 2008. B: projections from the stimulating site to the recorded neuron via synapse(s): 1: Li et al 2008, present experiment;2: present experiment;3: Cho et al 2002a, present experiment;4: Cho et al 2002b4: Cho et al , 2003Li et al 2002;5: Li et al 2005 Previous investigations in the hamster showed that a few NST taste neurons projected to the ipsilateral lateral hypothalamus (LH), but not to the contralateral LH; bilateral central nucleus of the amygdala (CeA); or bed nucleus of the stria terminalis (BNST) (Cho et al 2002b(Cho et al , 2003Li et al 2002;Smith et al 2005).…”

Section: Reciprocal Connections Of Nst Taste Neurons With Bilateral Gmentioning

confidence: 83%

Gustatory Neural Circuitry in the Hamster Brain Stem

Cho

Li²

2008

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Cho YK, Li C-S. Gustatory neural circuitry in the hamster brain stem. J Neurophysiol 100: 1007-1019. First published June 4, 2008 doi:10.1152/jn.01364.2007. The nucleus of the solitary tract (NST) and the parabrachial nuclei (PbN) are the first and second central relays for the taste pathway, respectively. Taste neurons in the NST project to the PbN, which further transmits taste information to the rostral taste centers. Nevertheless, details of the neural connections among the brain stem gustatory nuclei are obscure. Here, we investigated these relationships in the hamster brain stem. Three electrode assemblies were used to record the activity of taste neurons extracellularly and then to electrically stimulate these same areas in the order: left PbN, right PbN, and right NST. A fourth electrode, a glass micropipette, was used to record from gustatory cells in the left NST. Results showed extensive bilateral communication between brain stem nuclei at the same level: 1) 10% of 96 NST neurons projected to the contralateral NST and 58% received synaptic input from the contralateral NST; and 2) 12% of 43 PbN neurons projected to the contralateral PbN and 21% received synaptic input from the contralateral PbN. Results also showed extensive communication between levels: 1) as expected, the majority of 119 NST neurons, 82%, projected to the ipsilateral PbN, but 85% of the 20 NST neurons tested received synaptic input from the ipsilateral PbN, as did 59% of 22 NST neurons that did not project to the PbN; and 2) although few, 3%, of 119 NST cells projected to the contralateral PbN and 38% received synaptic input from the contralateral PbN. These results demonstrated that taste neurons in the NST not only project to, but also receive descending input from the bilateral PbN and that gustatory neurons in the NST and PbN also communicate with the corresponding nucleus on the contralateral side.