Viscerosensory signalling to the nucleus accumbens via the solitary tract nucleus.
CCK
TH
patch clamp electrophysiology
satiety
tyrosine hydroxylase
vagus
Journal
Journal of neurochemistry
ISSN: 1471-4159
Titre abrégé: J Neurochem
Pays: England
ID NLM: 2985190R
Informations de publication
Date de publication:
20 Jul 2024
20 Jul 2024
Historique:
revised:
21
06
2024
received:
04
02
2024
accepted:
21
06
2024
medline:
20
7
2024
pubmed:
20
7
2024
entrez:
20
7
2024
Statut:
aheadofprint
Résumé
The nucleus of the solitary tract (NTS) receives direct viscerosensory vagal afferent input that drives autonomic reflexes, neuroendocrine function and modulates behaviour. A subpopulation of NTS neurons project to the nucleus accumbens (NAc); however, the function of this NTS-NAc pathway remains unknown. A combination of neuroanatomical tracing, slice electrophysiology and fibre photometry was used in mice and/or rats to determine how NTS-NAc neurons fit within the viscerosensory network. NTS-NAc projection neurons are predominantly located in the medial and caudal portions of the NTS with 54 ± 7% (mice) and 65 ± 3% (rat) being TH-positive, representing the A2 NTS cell group. In horizontal brainstem slices, solitary tract (ST) stimulation evoked excitatory post-synaptic currents (EPSCs) in NTS-NAc projection neurons. The majority (75%) received low-jitter, zero-failure EPSCs characteristic of monosynaptic ST afferent input that identifies them as second order to primary sensory neurons. We then examined whether NTS-NAc neurons respond to cholecystokinin (CCK, 20 μg/kg ip) in vivo in both mice and rats. Surprisingly, there was no difference in the number of activated NTS-NAc cells between CCK and saline-treated mice. In rats, just 6% of NTS-NAc cells were recruited by CCK. As NTS TH neurons are the primary source for NAc noradrenaline, we measured noradrenaline release in the NAc and showed that NAc noradrenaline levels declined in response to cue-induced reward retrieval but not foot shock. Combined, these findings suggest that high-fidelity afferent information from viscerosensory afferents reaches the NAc. These signals are likely unrelated to CCK-sensitive vagal afferents but could interact with other sensory and higher order inputs to modulate learned appetitive behaviours.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Australian Research Council
ID : 170104861
Organisme : Australian Research Council
ID : 200102576
Organisme : Australian Research Council
ID : 210103929
Organisme : National Health and Medical Research Council
ID : 1079891
Organisme : National Health and Medical Research Council
ID : 2009851
Organisme : National Health and Medical Research Council
ID : 2011753
Informations de copyright
© 2024 The Author(s). Journal of Neurochemistry published by John Wiley & Sons Ltd on behalf of International Society for Neurochemistry.
Références
Altschuler, S. M., Bao, X. M., Bieger, D., Hopkins, D. A., & Miselis, R. R. (1989). Viscerotopic representation of the upper alimentary tract in the rat: Sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. Journal of Comparative Neurology, 283(2), 248–268.
Andresen, M. C., & Paton, J. F. (2011). The nucleus of the solitary tract: Processing information from viscerosensory afferents. In I. J. Llewellyn‐Smith & A. J. Verberne (Eds.), Central regulation of autonomic functions (Vol. 2, pp. 23–46). Oxford.
Appleyard, S. M., Marks, D., Kobayashi, K., Okano, H., Low, M. J., & Andresen, M. C. (2007). Visceral afferents directly activate catecholamine neurons in the solitary tract nucleus. Journal of Neuroscience, 27(48), 13292–13302.
Azdad, K., Gall, D., Woods, A. S., Ledent, C., Ferre, S., & Schiffmann, S. N. (2009). Dopamine D2 and adenosine A2A receptors regulate NMDA‐mediated excitation in accumbens neurons through A2A‐D2 receptor heteromerization. Neuropsychopharmacology, 34(4), 972–986.
Bankhead, P., Loughrey, M. B., Fernández, J. A., Dombrowski, Y., McArt, D. G., Dunne, P. D., McQuaid, S., Gray, R. T., Murray, L. J., Coleman, H. G., James, J. A., Salto‐Tellez, M., & Hamilton, P. W. (2017). QuPath: Open source software for digital pathology image analysis. Scientific Reports, 7(1), 16878.
Bassi, J. K., Connelly, A. A., Butler, A. G., Liu, Y., Ghanbari, A., Farmer, D. G. S., Jenkins, M. W., Melo, M. R., McDougall, S. J., & Allen, A. M. (2022). Analysis of the distribution of vagal afferent projections from different peripheral organs to the nucleus of the solitary tract in rats. Journal of Comparative Neurology, 530, 3072–3103.
Berridge, K. C., & Kringelbach, M. L. (2013). Neuroscience of affect: Brain mechanisms of pleasure and displeasure. [review]. Current Opinion in Neurobiology, 23(3), 294–303.
Briski, K. P., & Marshall, E. S. (2000). Caudal brainstem Fos expression is restricted to periventricular catecholamine neuron‐containing loci following intraventricular administration of 2‐deoxy‐d‐glucose. Experimental Brain Research, 133(4), 547–551.
Carlezon, W. A., Jr., & Thomas, M. J. (2009). Biological substrates of reward and aversion: A nucleus accumbens activity hypothesis. Neuropharmacology, 56(Suppl 1), 122–132.
Chaudhri, O., Small, C., & Bloom, S. (2006). Gastrointestinal hormones regulating appetite. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 361(1471), 1187–1209.
Ch'ng, S. S., Fu, J., Brown, R. M., Smith, C. M., Hossain, M. A., McDougall, S. J., & Lawrence, A. J. (2019). Characterization of the relaxin family peptide receptor 3 system in the mouse bed nucleus of the stria terminalis. Journal of Comparative Neurology, 527(16), 2615–2633.
Choi, E. A., Jean‐Richard‐Dit‐Bressel, P., Clifford, C. W. G., & McNally, G. P. (2019). Paraventricular thalamus controls behavior during motivational conflict. Journal of Neuroscience, 39(25), 4945–4958.
Cui, R. J., Roberts, B. L., Zhao, H., Zhu, M., & Appleyard, S. M. (2012). Serotonin activates catecholamine neurons in the solitary tract nucleus by increasing spontaneous glutamate inputs. Journal of Neuroscience, 32(46), 16530–16538.
Delaney, A. J., Crane, J. W., & Sah, P. (2007). Noradrenaline modulates transmission at a central synapse by a presynaptic mechanism. Neuron, 56(5), 880–892.
Delfs, J. M., Zhu, Y., Druhan, J. P., & Aston‐Jones, G. S. (1998). Origin of noradrenergic afferents to the shell subregion of the nucleus accumbens: Anterograde and retrograde tract‐tracing studies in the rat. Brain Research, 806(2), 127–140.
Deng, H., Xiao, X., Yang, T., Ritola, K., Hantman, A., Li, Y., Huang, Z. J., & Li, B. (2021). A genetically defined insula‐brainstem circuit selectively controls motivational vigor. Cell, 184(26), 6344–6360. e6318.
Fraser, K. A., & Davison, J. S. (1992). Cholecystokinin‐induced c‐fos expression in the rat brain stem is influenced by vagal nerve integrity. Experimental Physiology, 77(1), 225.
Gabbott, P. L., Warner, T., & Busby, S. J. (2007). Catecholaminergic neurons in medullary nuclei are among the post‐synaptic targets of descending projections from infralimbic area 25 of the rat medial prefrontal cortex. [research support, non‐U.S. Gov't]. Neuroscience, 144(2), 623–635.
Gasparini, S., Resch, J. M., Gore, A. M., Peltekian, L., & Geerling, J. C. (2021). Pre‐locus coeruleus neurons in rat and mouse. American Journal of Physiology, 320, R342–R361.
Heimer, L., Alheid, G. F., de Olmos, J. S., Groenewegen, H. J., Haber, S. N., Harlan, R. E., & Zahm, D. S. (1997). The accumbens: Beyond the core‐shell dichotomy. The Journal of Neuropsychiatry and Clinical Neurosciences, 9(3), 354–381.
Inoue, W., Baimoukhametova, D. V., Fuzesi, T., Cusulin, J. I., Koblinger, K., Whelan, P. J., Pittman, Q. J., & Bains, J. S. (2013). Noradrenaline is a stress‐associated metaplastic signal at GABA synapses. Nature Neuroscience, 16, 605–612.
Jänig, W. (2008). Integrative action of the autonomic nervous system: Neurobiology of homeostasis. Cambridge University Press.
Jean‐Richard‐Dit‐Bressel, P., Clifford, C. W. G., & McNally, G. P. (2020). Analyzing event‐related transients: Confidence intervals, permutation tests, and consecutive thresholds. Frontiers in Molelcular Neuroscience, 13, 14.
Keller, B. N., Hajnal, A., Browning, K. N., Arnold, A. C., & Silberman, Y. (2022). Involvement of the dorsal vagal complex in alcohol‐related behaviors. Frontiers in Behavioural Neuroscience, 16, 801825.
Kerfoot, E. C., & Williams, C. L. (2011). Interactions between brainstem noradrenergic neurons and the nucleus accumbens shell in modulating memory for emotionally arousing events. Learning and Memory, 18(6), 405–413.
Kirouac, G. J., & Ciriello, J. (1997). Medullary inputs to nucleus accumbens neurons. The American Journal of Physiology, 273(6 Pt 2), R2080–R2088.
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., & Pennartz, C. M. (2010). Fast‐spiking interneurons of the rat ventral striatum: Temporal coordination of activity with principal cells and responsiveness to reward. European Journal of Neuroscience, 32(3), 494–508.
Li, J., Rao, Z.‐R., & Shi, J.‐W. (1990). Substance P like immunoreactive neurons in the nucleus tractus solitarii of the rat send their axons to the nucleus accumbens. Neuroscience Letters, 120, 194–196.
Manz, K. M., Coleman, B. C., Grueter, C. A., Shields, B. C., Tadross, M. R., & Grueter, B. A. (2021). Noradrenergic signaling disengages feedforward transmission in the nucleus Accumbens Shell. Journal of Neruoscience, 41(17), 3752–3763.
Matsushita, N., Okada, H., Yasoshima, Y., Takahashi, K., Kiuchi, K., & Kobayashi, K. (2002). Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. Journal of Neurochemistry, 82, 295–304.
McCann, M. J., & Rogers, R. C. (1992). Impact of antral mechanoreceptor activation on the vago‐vagal reflex in the rat: Functional zonation of responses. The Journal of Physiology, 453, 401–411.
McDougall, S. J., Guo, H., & Andresen, M. C. (2017). Dedicated C‐fibre viscerosensory pathways to central nucleus of the amygdala. Journal of Physiology, 595(3), 901–917.
Moran, T. H., Ladenheim, E. E., & Schwartz, G. J. (2001). Within‐meal gut feedback signaling. International Journal of Obesity and Related Metabolic Disorders, 25(Suppl 5), S39–S41.
Murphy, S., Collis Glynn, M., Dixon, T. N., Grill, H. J., McNally, G. P., & Ong, Z. Y. (2022). Nucleus of the solitary tract A2 neurons control feeding behaviors via projections to the paraventricular hypothalamus. Neuropsychopharmacology, 48, 351–361.
Ong, Z. Y., Bongiorno, D. M., Hernando, M. A., & Grill, H. J. (2017). Effects of endogenous oxytocin receptor signaling in nucleus Tractus Solitarius on satiation‐mediated feeding and Thermogenic control in male rats. Endocrinology, 158(9), 2826–2836.
Reynolds, S. M., & Berridge, K. C. (2001). Fear and feeding in the nucleus accumbens shell: Rostrocaudal segregation of GABA‐elicited defensive behavior versus eating behavior. Journal of Neuroscience, 21(9), 3261–3270.
Reynolds, S. M., & Berridge, K. C. (2002). Positive and negative motivation in nucleus accumbens shell: Bivalent rostrocaudal gradients for GABA‐elicited eating, taste “liking”/“disliking” reactions, place preference/avoidance, and fear. Journal of Neuroscience, 22(16), 7308–7320.
Rhodes, S. E., & Killcross, S. (2004). Lesions of rat infralimbic cortex enhance recovery and reinstatement of an appetitive Pavlovian response. Learning and Memory, 11(5), 611–616.
Rinaman, L. (2003). Hindbrain noradrenergic lesions attenuate anorexia and alter central cFos expression in rats after gastric viscerosensory stimulation. Journal of Neuroscience, 23(31), 10084–10092.
Rinaman, L., Baker, E. A., Hoffman, G. E., Stricker, E. M., & Verbalis, J. G. (1998). Medullary c‐Fos activation in rats after ingestion of a satiating meal. American Journal of Physiology, 275(1 Pt 2), R262–R268.
Rinaman, L., Hoffman, G. E., Dohanics, J., Le, W. W., Stricker, E. M., & Verbalis, J. G. (1995). Cholecystokinin activates catecholaminergic neurons in the caudal medulla that innervate the paraventricular nucleus of the hypothalamus in rats. Jouranal of Comparative Neurology, 360(2), 246–256.
Rinaman, L., Verbalis, J. G., Stricker, E. M., & Hoffman, G. E. (1993). Distribution and neurochemical phenotypes of caudal medullary neurons activated to express cFos following peripheral administration of cholecystokinin. Journal of Comparative Neurology, 338(4), 475–490.
Roberts, B. L., Zhu, M., Zhao, H., Dillon, C., & Appleyard, S. M. (2017). High glucose increases action potential firing of catecholamine neurons in the nucleus of the solitary tract by increasing spontaneous glutamate inputs. American Journal of Physiology, 313(3), R229–R239.
Shapiro, R. E., & Miselis, R. R. (1985). The central organization of the vagus nerve innervating the stomach of the rat. Journal of Comparative Neurology, 238(4), 473–488.
Simonian, S. X., & Herbison, A. E. (1997). Differential expression of estrogen receptor and neuropeptide Y by brainstem A1 and A2 noradrenaline neurons. Neuroscience, 76(2), 517–529.
Tenorio, G., Connor, S. A., Guevremont, D., Abraham, W. C., Williams, J., O'Dell, T. J., & Nguyen, P. V. (2010). 'Silent' priming of translation‐dependent LTP by ss‐adrenergic receptors involves phosphorylation and recruitment of AMPA receptors. Learning and Memory, 17(12), 627–638.
Thomas, M. J., Moody, T. D., Makhinson, M., & O'Dell, T. J. (1996). Activity‐dependent beta‐adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron, 17(3), 475–482.
van der Kooy, D., Koda, L. Y., McGinty, J. F., Gerfen, C. R., & Bloom, F. E. (1984). The organization of projections from the cortex, amygdala, and hypothalamus to the nucleus of the solitary tract in rat. Journal of Comparative Neurology, 224(1), 1–24.
Wang, Z.‐J., Rao, Z.‐R., & Shi, J.‐W. (1992). Tyrosine hydroxylase‐, neurotesin‐, or cholecystokinin‐ containing neurons in the nucleus tractus solitarii send projection fibers to the nucleus accumbens in the rat. Brain Research, 578, 347–350.
Weller, K. L., & Smith, D. A. (1982). Afferent connections to the bed nucleus of the stria terminalis. Brain Research, 232(2), 255–270.
Wichmann, R., Fornari, R. V., & Roozendaal, B. (2012). Glucocorticoids interact with the noradrenergic arousal system in the nucleus accumbens shell to enhance memory consolidation of both appetitive and aversive taste learning. [research support, non‐U.S. Gov't]. Neurobiology of Learning and Memory, 98(2), 197–205.
Wilson, C. J. (1993). The generation of natural firing patterns in neostriatal neurons. Progress in Brain Research, 99, 277–297.
Wilson, C. J., & Groves, P. M. (1981). Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Research, 220(1), 67–80.
Yau, J. O., Chaichim, C., Power, J. M., & McNally, G. P. (2021). The roles of basolateral amygdala Parvalbumin neurons in fear learning. Journal of Neuroscience, 41(44), 9223–9234.
Yettefti, K., Orsini, J. C., & Perrin, J. (1997). Characteristics of glycemia‐sensitive neurons in the nucleus tractus solitarii: Possible involvement in nutritional regulation. Physiology & Behavior, 61(1), 93–100.
Zhang, W. T., Chao, T. H., Yang, Y., Wang, T. W., Lee, S. H., Oyarzabal, E. A., Zhou, J., Nonneman, R., Pegard, N. C., Zhu, H., Cui, G., & (2022). Spectral fiber photometry derives hemoglobin concentration changes for accurate measurement of fluorescent sensor activity. Cell Reports Methods, 2(7), 100243.