Morphological and physiological evidence of a synaptic connection between the lateral parabrachial nucleus and neurons in the A7 catecholamine cell group in rats

Journal of Biomedical Science

Hsiu-Wen Yang⁵  Ming-Yuan Min¹  Chuan-Mu Chen³  Chi-Sheng Yang⁴  Meng-Lam Lee⁵  Chia-Yi Liu² 

[1] Department of Life Sciences, College of Life Science, National Taiwan University, Taipei, Taiwan;Department of Nursing, Jen-Teh Junior College of Medicine, Nursing and Management, Miaoli, Taiwan;Rong Hsing Research Center for Translational Medicine, and the iEGG Center, National Chung Hsing University, Taichung, Taiwan;Department of Nursing, Hungkuang University, Taichung, Taiwan;Department of Medical Research, Chung Shan Medical University, Taichung, Taiwan

关键词: Catecholamine;    Nociception;    A7;    Lateral parabrachial nucleus;   

Others  :  1230512
DOI  :  10.1186/s12929-015-0179-2

 received in 2015-04-14, accepted in 2015-08-20,  发布年份 2015

【 摘 要 】

Background

The descending noradrenergic (NAergic) system is one of the important endogenous analgesia systems. It has been suggested that noxious stimuli could activate descending NAergic system; nevertheless, the underlying neuronal circuit remains unclear. As NAergic neurons in the A7 catecholamine cell group (A7) are a part of the descending NAergic system and the lateral parabrachial nucleus (LPB) is an important brainstem structure that relays ascending nociceptive signal, we aimed to test whether LPB neurons have direct synaptic contact with NAergic A7 neurons.

Results

Stereotaxic injections of an anterograde tracer, biotinylated dextran-amine (BDA), were administered to LPB in rats. The BDA-labeled axonal terminals that have physical contacts with tyrosine hydroxylase-positive (presumed noadrenergic) neurons were identified in A7. Consistent with these morphological observations, the excitatory synaptic currents (EPSCs) were readily evoked in NAergic A7 neurons by extracellular stimulation of LPB. The EPSCs evoked by LPB stimulation were blocked by CNQX, a non-NMDA receptor blocker, and AP5, a selective NMDA receptor blocker, showing that LPB-A7 synaptic transmission is glutamatergic. Moreover, the amplitude of LPB-A7 EPSCs was significantly attenuated by DAMGO, a selective μ-opioid receptor agonist, which was associated with an increase in paired-pulse ratio.

Conclusions

Taken together, the above results showed direct synaptic connections between LPB and A7 catecholamine cell group, the function of which is subject to presynaptic modulation by μ-opioid receptors.

【 授权许可】

   
2015 Liu et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

【 参考文献 】

• [1]Pertovaara A. Noradrenergic pain modulation. Prog Neurobiol. 2006; 80:53-83.
• [2]North RA, Yoshimura M. The actions of noradrenaline on neurones of the rat substantia gelatinosa in vitro. J Physiol. 1984; 349:43-55.
• [3]Danzebrink RM, Gebhart GF. Antinociceptive effects of intrathecal adrenoceptor agonists in a rat model of visceral nociception. J Pharmacol Exp Ther. 1990; 253:698-705.
• [4]Carlsson A, Falck B, Fuxe K, Hillarp NA. Cellular localization of monoamines in the spinal cord. Acta Physiol Scand. 1964; 60:112-119.
• [5]Clark FM, Proudfit HK. The projection of noradrenergic neurons in A7 catecholamine cell group to the spinal cord in rat demonstrated by antrograde tracing combined immunohistochemistry. Brain Res. 1991; 547:279-288.
• [6]Kwiat GC, Basbaum AI. The origin of brainstem noradrenergic and serotonergic projections to the spinal cord dorsal horn in the rat. Somatosens Mot Res. 1992; 9:157-173.
• [7]Proudfit HK, Clark FM. The projection of locus coeruleus neurons to the spinal cord. Prog Brain Res. 1991; 88:123-141.
• [8]Westlund KN, Coulter JD. Descending projections of the locus coeruleus and subcoeruleus/medial parabrachial nuclei in monkey: axonal transport studies and dopamine-b-hydroxylase immunocytochemistry. Brain Res Rev. 1980; 2:235-264.
• [9]Holden JE, Schwartz EJ, Proudfit HK. Microinjection of morphine in the A7 catecholamine cell group produces opposing effects on nociception that are mediated by alpha1- and alpha2- adrenoceptors. Neuroscience. 1999; 83:979-990.
• [10]Yeomans DC, Clark FM, Paice JA, Proudfit PH. Antinociception induced by electrical stimulation of spinally projecting noradrenergic neurons in the A7 catecholamine cell group of the rat. Pain. 1992; 48:449-461.
• [11]Dennis SG, Melzack R, Gutman S, Boucher F. Pain modulationby adrenergic agents and morphine as measured by three pain tests. Life Sci. 1980; 26:1247-1259.
• [12]Min MY, Wu YW, Shih PY, Lu HW, Lin CC, Wu Y, Li MJ, Yang HW. Physiological and morphological properties of, and effect of substance P on, neurons in the A7 catecholamine cell group in rats. Neuroscience. 2008; 153:1020-1033.
• [13]Min MY, Wu YW, Shih PY, Lu HW, Wu Y, Hsu CL, Li MJ, Yang HW. Roles of A-type potassium currents in tuning spike frequency and integrating synaptic transmission in noradrenergic neurons of the A7 catecholamine cell group in rats. Neuroscience. 2010; 168:633-645.
• [14]Min MY, Shih PY, Wu YW, Lu HW, Lee ML, Yang HW. Neurokinin 1 receptor activates transient receptor potential-like currents in noradrenergic A7 neurons in rats. Mol Cell Neurosci. 2008; 42:56-65.
• [15]Wu YW, Wang HW, Lin CC, Lu HW, Cheng SJ, Yang HW, Min MY. GABA B receptor-mediated tonic inhibition of noradrenergic A7 neurons in the cat. J Neurophysiol. 2011; 105:2715-2728.
• [16]Sugiyama D, Hur S, Pickering AE, Kase D, Kim S, Kawamata M, Imoto K. Furue, In vivo patch-clamp recording from locus coeruleus neurons in the rat brainstem. J Physiol. 2012; 590:2225-2231.
• [17]Takagi H, Shiomi H, Kuraishi Y, Fukui K, Ueda H. Pain and the bulbospinal noradrenergic system: pain-induced increase in normetanephrine content in the spinal cord and its modification by morphine. Eur J Pharmacol. 1979; 54:99-107.
• [18]Tyce GM, Yaksh TL. Monoamine release from cat spinal cord by somatic stimuli: an intrinsic modulatory system. J Physiol. 1981; 314:513-529.
• [19]Bernard JF, Alden M, Besson JM. The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaseolus vulgaris leucoagglutionin (PHA-L) study in the rat. J Comp Neurol. 1993; 329:201-229.
• [20]Gauriau C, Bernard JF. Pain pathways and parabrachial circuits in the rat. Exp Physiol. 2002; 87:251-258.
• [21]Sarhan M, Freund-Mercier MJ, Veinante P. Branching patters of parabrachial neurons projecting to the central extended amgydala: single axonal reconstructions. J Comp Neurol. 2005; 491:418-442.
• [22]Paxinos G, Watson C. The Rat brain in stereotaxic coordinates. hth ed. Academic, San Diego; 1998.
• [23]Ding YQ, Kaneko T, Nomura S, Mizuno N. Immunohistochemical localization of mu-opioid receptors in the central nervous system of the rat. J Comp Neurol. 1996; 367:375-402.
• [24]Mansour A, Fox CA, Burke S, Akil H, Watson SJ. Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS. J Chem Neuroanat. 1995; 8:283-305.
• [25]Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Re. Physiol. 2002; 64:355-405.
• [26]Bajic D, Proudfit HK. Projections of neurons in the periaqueductal gray to pontine and medullary catecholamine cell groups involved in the modulation of nociception. J Comp Neurol. 1999; 405:359-379.
• [27]Bajic D, Van Bockstaele EJ, Proudfit HK. Ultrastructural analysis of ventrolateral periaqueductal gray projections to the A7 catecholamine cell group. Neuroscience. 2001; 104:181-197.
• [28]Holden JE, Pizzi JA. The challenge of chronic pain. Adv Drug Deliv Rev. 2003; 55:935-948.
• [29]Holden JE, Proudfit HK. Enkephalin neurons that project to the A7 catecholamine cell group are located in nuclei that modulate nociception: ventromedial medulla. Neuroscience. 1998; 83:929-947.
• [30]Nuseir K, Proudfit HK. Bidirectional modulation of nociception by GABA neurons in the dorsolateral pontine tegmentum that tonically inhibit spinally projecting noradrenergic A7 neurons. Neuroscience. 2000; 96:773-783.
• [31]Guthmann A, Fritschy JM, Ottersen OP, Torp R, Herbert H. GABA, GABA transporters, GABA(A) receptor subunits, and GAD mRNAs in the rat parabrachial and Kölliker-Fuse nuclei. J Comp Neurol. 1998; 400:229-243.
• [32]Yokota S, Oka T, Tsumori T, Nakamura S, Yasui Y. Glutamatergic neurons in the Kolliker-Fuse nucleus project to the rostral ventral respiratory group and phrenic nucleus: a combined retrograde tracing and in situ hybridization study in the rat. Neurosci Res. 2007; 59:341-346.
• [33]Jonas P, Major G, Sakmann B. Quantal component of unitary EPSCs at the mossy fibre synapses on CA3 pyramidal cells of rat hippocampus. J Physiol. 1993; 472:615-663.
• [34]Stern P, Edwards FA, Sakmann B. Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. J Physiol. 1992; 449:247-278.
• [35]Chamberlin NL, Saper CB. Topographic organization of respiratory responses to glutamate microstimulation of the parabrachial nucleus in the rat. J Neurosci. 1994; 14:6500-6510.
• [36]Felder RB, Mifflin SW. Modulation of carotid sinus afferent input to nucleus tractus solitarius by parabrachial nucleus stimulation. Circulation Rese. 1988; 63:35-49.
• [37]Jia HG, Rao ZR, Shi JW. An indirect projection from the nucleus of the solitary tract to the central nucleus of the amygdala via the parabrachial nucleus in the rat. A light and electron microscopic study. Brain Res. 1994; 663:181-190.
• [38]Takayama K, Miura M. Respiratory responses to microinjection of excitatory amino acid agonist in ventrolateral regions of the lateral parabrachial nucleus in the cat. Brain Res. 1993; 604:217-223.
• [39]Craig AD. Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J Comp Neurol. 1995; 361:225-248.
• [40]Hylden JL, Anton F, Nahin RL. Spinal lamina I projection neurons in the rat: collateral innervation of parabrachial area and thalamus. Neuroscience. 1989; 28:27-37.
• [41]Klop EM, Mouton LJ, Hulsebosch R, Boers J, Holstege G. In cat four times as many lamina I neurons project to the parabrachial nuclei and twice as many to the periaqueductal gray as to the thalamus. Neuroscience. 2005; 134:189-197.