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

Abstract

(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...

Gustatory Neural Circuitry in the Hamster Brain Stem

“…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).…”

“…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). In contrast, a substantial proportion of the gustatory PbN cells send axons to the LH, CeA, or VPMpc in the hamster or in the rat (Bester et al 1997;Hayama and Ogawa 1987;Li et al 2005;Mao et al 2008;Norgren 1976;Norgren and Leonard 1973). These results confirm that the majority of taste information is carried to the ipsilateral PbN from the gustatory NST before it is further transferred to the higher taste centers in the rodent.…”

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

“…It is likely that projections from the NAcSh form an inhibitory synapse with pontine gustatory cells, whereas they form an excitatory synaptic contact with medullary taste neurons, which can be composed of interneurons or gustatory neurons. Nonetheless, brain stem gustatory neurons are capable of responding in opposite ways to descending inputs from the NAcSh, similar to the VPM modulation of gustatory responses in the NST and PbN Mao et al 2008). The significance of altering taste processing in the brain stem is not clear.…”

Parabrachial-hypothalamic interactions are required for normal conditioned taste aversions

“…They can retain a CTA learned prior to the lesions but fail to learn new CTAs (4, 34 -36). The PBN has reciprocal neural connections to the LH, central nucleus of the amygdala (CNA), and the bed nucleus of the stria terminalis (BNST) (11,12,14,16,17,(21)(22)(23)(24)43).Electrolytic lesions of the LH can damage the fibers of passage that link the PBN to the CNA and BNST (23,24,33). Thus, the CTA deficits displayed by rats with electrolytic LH lesions (LHx) could be due to the involvement of the intrinsic neurons of the LH or the functional isolation of PBN from the CNA, the BNST, or other anterior forebrain sites.…”

“…They can retain a CTA learned prior to the lesions but fail to learn new CTAs (4, 34 -36). The PBN has reciprocal neural connections to the LH, central nucleus of the amygdala (CNA), and the bed nucleus of the stria terminalis (BNST) (11,12,14,16,17,(21)(22)(23)(24)43).…”