Taste Responses of Neurons in the Hamster Solitary Nucleus Are Modulated by the Central Nucleus of the Amygdala

Li, Chengshu; Cho, Young K.; Smith, David V.

doi:10.1152/jn.00239.2002

Cited by 64 publications

(60 citation statements)

References 54 publications

(47 reference statements)

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“…The overall baseline activity of the 114 taste-responsive PbN neurons recorded in the present study varied from 0 to 15.80 imp/s, with a mean of 3.58 Ϯ 0.34 imp/s. This mean firing rate was similar to that recorded previously in the PbN (e.g., 3.70 Ϯ 0.27 imp/s, t ϭ 0.266, df ϭ 229, P ϭ 0.791) (34) and was significantly higher than that recorded in the NST in our previous experiments (e.g., 2.12 Ϯ 0.27 imp/s, t ϭ 3.350, df ϭ 221, P Ͻ 0.001) (36).…”

Section: Histologycontrasting

confidence: 45%

“…Electrical stimulation of the BNST modulated taste responses in the NST and PbN (34,74). Activation of the CeA and LH also modulated taste responses of the neurons in the NST and PbN (8,35,36). Modulation of PbN neurons' taste responses by forebrain activation, including the CeA, LH, and GC, has also been demonstrated by Lundy and Norgren (39,40) in the rat.…”

Section: Discussionmentioning

confidence: 68%

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Modulation of activity of gustatory neurons in the hamster parabrachial nuclei by electrical stimulation of the ventroposteromedial nucleus of the thalamus

Mao¹,

Cho²,

Li³

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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(VPMpc) is positioned at the key site between the gustatory parabrachial nuclei (PbN) and the gustatory cortex for relaying and processing gustatory information via the thalamocortical pathway. Although neuroanatomical and electrophysiological studies have provided information regarding the gustatory projection from PbN to VPMpc, the exact relationship between PbN and VPMpc, especially the efferent projection involving VPMpc to PbN, is obscure. Here we investigated the reciprocal connection between these two gustatory relays in urethaneanesthetized hamsters. We recorded from 114 taste-responsive neurons in the PbN and examined their responsiveness to electrical stimulation of the VPMpc bilaterally. Stimulation of either or both of the ipsilateral or contralateral VPMpc antidromically activated 109 gustatory PbN neurons. Seventy-two PbN neurons were antidromically activated after stimulation of both sides of the VPMpc, indicating that taste neurons in the PbN project heavily to the bilateral VPMpc. Stimulation of VPMpc also orthodromically activated 110 of PbN neurons, including 106 VPMpc projection neurons. Seventyeight neurons were orthodromically activated bilaterally. Among orthodromic activations of the PbN cells, the inhibitory response was the dominant response; 106 cells were inhibited, including 10 neurons that were also excited contralaterally, indicating that taste neurons in the PbN are subject to strong inhibitory control from VPMpc. Moreover, stimulation of VPMpc altered taste responses of the neurons in the PbN, indicating that VPMpc modulates taste responses of PbN neurons. These results may provide functional insight of neural circuitry for taste processing and modulation involving these two nuclei.central gustatory pathway; pons; electrophysiology THE PARABRACHIAL NUCLEI (PbN) and the parvicellular part of the ventroposteromedial nucleus of the thalamus (VPMpc) are the second and tertiary central relays for taste information processing in rodents, respectively (4,13,17,28,45,49,51). Gustatory information elicited from the tongue and oropharyngeal cavity is initially carried to the rostral portion of the nucleus of the solitary tract (NST) by the VIIth, IXth, and Xth cranial nerves, and these terminals are distributed in a topographic fashion with rostral-caudal sequence in the rostral NST (2,9,23,24,89). From the NST, ascending gustatory fibers project to third-order taste cells within the PbN of the pons (7,22,42,46,(53)(54)(55)87). Two separate routes carry taste information from the PbN further to the forebrain taste areas and cortex: the ventral forebrain pathway that involves the central nucleus of the amygdala (CeA), the lateral hypothalamus (LH), the bed nucleus of the stria terminalis (BNST), the substantia innominata (3,12,16,21,31,33,34,41,47,63,64,71); and the thalamocortical pathway that is characterized by the involvement of the bilateral VPMpc, which, in turn, carries taste information to the gustatory cortex (GC) (5,25,45,48,51).The PbN is a critical neural substrate for a number...

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Section: Histologycontrasting

confidence: 45%

Section: Discussionmentioning

confidence: 68%

Modulation of activity of gustatory neurons in the hamster parabrachial nuclei by electrical stimulation of the ventroposteromedial nucleus of the thalamus

Mao¹,

Cho²,

Li³

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Somatostatin immunoreactive neurons have been demonstrated in the central nucleus of the amygdala (CeA) (Wray and Hoffman 2007) and microinjection of retrograde tracer labels fibers that differentially distribute throughout the rostral caudal extent of the NST (Halsell 1998;Saha et al 2000). Moreover, orthodromic activation by electrical stimulation of the CeA results in modulation of the responses of rNST neurons to taste stimuli applied to the oral cavity (Li et al 2002), suggesting a role of the somatostatin fibers and the GAD67-GFP neurons in the centrifugal control of taste processing.…”

Section: Subpopulations Of Gad67-gfp Rnst Neuronsmentioning

confidence: 99%

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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“…In the medullary nucleus of the solitary tract (NST), electrical stimulation of the LH and CeA is known to modulate both background discharge and taste-evoked responses (Bereiter et al 1980;Cho et al 2002a;Li et al 2002;Matsuo et al 1984;Murzi et al 1986). Cortex stimulation also modulates the spontaneous activity of taste responsive cells, but the effects on sapid stimulus responsiveness have not been tested (Smith and Li 2000).…”

Section: Introductionmentioning

confidence: 99%

Activity in the Hypothalamus, Amygdala, and Cortex Generates Bilateral and Convergent Modulation of Pontine Gustatory Neurons

Lundy

Norgren

2004

Journal of Neurophysiology

101

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Lundy, Robert F., Jr. and Ralph Norgren. Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. J Neurophysiol 91: 1143-1157, 2004. First published November 19, 2003 10.1152/jn.00840.2003. Evidence suggests that centrifugal modulation of brain stem gustatory cells might play a role in the elaboration of complex taste-guided behaviors like conditioned taste aversion and sodium appetite. We previously showed that activity in one forebrain area, the central nucleus of the amygdala (CeA), increased the chemical selectivity of taste cells in the parabrachial nucleus (PBN). The present study investigates how activity in 2 other similarly interconnected forebrain sites, the lateral hypothalamus (LH) and gustatory cortex (GC), might influence PBN gustatory processing in rats. The potential convergence of descending inputs from these sites, as well as the CeA, was also evaluated. After anesthesia (35 mg/kg Nembutal ip), 70 PBN gustatory neurons were tested before, during, and after electrical stimulation of these forebrain sites, while responding to 0.3 M sucrose, 0.1 M NaCl, 0.01 M citric acid, and 0.003 M QHCl. Although each forebrain site modulated taste-evoked responses, more PBN neurons were influenced by stimulation of the GC (67%) and CeA (73%) than of the LH (48%). Activation of cortex (71%) and amygdala (85%) most often produced inhibition, whereas inhibition and excitation occurred equally often during hypothalamic stimulation. Of the neurons tested for convergence (n ϭ 60), 88% were influenced by Ն1 of the 3 sites. Twenty were modulated by stimulation at all 3 sites and another 17 by 2 of the 3 sites. The net effect of centrifugal modulation was to sharpen the across-stimulus response profiles of PBN cells, particular with regard to the NaCl-and citric acid-best cells.

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Taste Responses of Neurons in the Hamster Solitary Nucleus Are Modulated by the Central Nucleus of the Amygdala

Cited by 64 publications

References 54 publications

Modulation of activity of gustatory neurons in the hamster parabrachial nuclei by electrical stimulation of the ventroposteromedial nucleus of the thalamus

Modulation of activity of gustatory neurons in the hamster parabrachial nuclei by electrical stimulation of the ventroposteromedial nucleus of the thalamus

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

Activity in the Hypothalamus, Amygdala, and Cortex Generates Bilateral and Convergent Modulation of Pontine Gustatory Neurons

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