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

Abstract

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.

Influences of ethanol and temperature on sucrose-evoked response of gustatory neurons in the hamster solitary nucleus

“…Sections were stained with Neutral Red. These markings were located in the rostral NST which coincided with the area of recording sites in the previous studies [26][27][28].…”

“…Activity was monitored in the rostral regions of the NST, where the dorsal cochlear nucleus is appeared. This region is often used to record taste-responsive neurons [ 27 , 28 , 31 ]. The vast majority of gustatory cells in this area project to the next taste relay, the PbN in hamsters [ 26 ].…”

“…The NAcc is a key neural structure involved in reinforcement and motivational behavior [ 38 , 41 ]; specifically, the NAcc shell region plays a significant role in encoding the hedonic value of orosensory stimuli and motivated behaviors [ 41 , 45 ]. We previously demonstrated that electrical stimulation of the NAcc shell region enhanced the spontaneous and taste-evoked neuronal firing of NST taste cells, whereas inhibiting neuronal activity of pontine gustatory neurons in the hamster [ 28 , 46 ]. Altogether, these findings suggest that the gustatory neural pathway may be involved in the appetitive aspects associated with alcohol consumption.…”

“…It is well known that medullary taste neurons are under influence of many physiological aspects, such as sodium appetite, blood glucose level, or taste-related learning [ 8 , 11 , 57 ]. The stimulation of gustatory nuclei in the forebrain, including the NAcc, modulates taste responses in the NST [ 27 , 28 , 58 , 59 ], suggesting that these descending inputs can be involved in inducing plasticity of the taste response in the NTS. Further studies are needed to examine whether EtOH or thermal stimulation also exert an influence on gustatory responses in more rostral taste relay nuclei, such as the PbN or the gustatory cortex.…”

“…Each animal was tracheotomized and mounted in a stereotaxic instrument (SR-6N; Narishige, Tokyo, Japan) using a non-traumatic head holder. The surgical procedures to expose the brainstem for in vivo recording were described in detaril in previous studies [ 26 - 28 ].…”