Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104, USA.
J Neurosci. 2010 Feb 17;30(7):2418-27. doi: 10.1523/JNEUROSCI.5533-09.2010.
Neuronal circuits commonly receive simultaneous inputs from descending, ascending, and hormonal systems. Thus far, however, most such inputs have been studied individually to determine their influence on a given circuit. Here, we examine the integrated action of the hormone crustacean cardioactive peptide (CCAP) and the gastropyloric receptor (GPR) proprioceptor neuron on the biphasic gastric mill (chewing) rhythm driven by the projection neuron modulatory commissural neuron 1 (MCN1) in the isolated crab stomatogastric ganglion. In control saline, GPR stimulation selectively prolongs the gastric mill retractor phase, via presynaptic inhibition of MCN1. In the absence of GPR stimulation, CCAP does not alter retraction duration and modestly prolongs protraction. Here, we show, using computational modeling and dynamic-clamp manipulations, that the presence of CCAP weakens or eliminates the GPR effect on the gastric mill rhythm. This CCAP action results from its ability to activate the same modulator-activated conductance (G(MI)) as MCN1 in the gastric mill circuit neuron lateral gastric (LG). Because GPR prolongs retraction by weakening MCN1 activation of G(MI) in LG, the parallel G(MI) activation by CCAP reduces the impact of GPR regulation of this conductance. The CCAP-activated G(MI) thus counteracts the GPR-mediated decrease in the MCN1-activated G(MI) in LG and reduces the GPR ability to regulate the gastric mill rhythm. Consequently, although CCAP neither changes retraction duration nor alters GPR inhibition of MCN1, its activation of a modulator-activated conductance in a pivotal downstream circuit neuron enables CCAP to weaken or eliminate sensory regulation of motor circuit output.
神经元回路通常同时接收来自下行、上行和激素系统的输入。然而,到目前为止,大多数此类输入都是单独研究的,以确定它们对特定回路的影响。在这里,我们研究了激素甲壳动物心脏活性肽 (CCAP) 和胃幽门受体 (GPR) 本体感受神经元对分离螃蟹胃神经节中投射神经元调制性连合神经元 1 (MCN1) 驱动的双相胃磨(咀嚼)节律的综合作用。在对照盐水中,GPR 刺激通过对 MCN1 的突触前抑制选择性延长胃磨回缩相。在没有 GPR 刺激的情况下,CCAP 不会改变回缩持续时间,只会适度延长伸展。在这里,我们使用计算建模和动态钳位操作表明,CCAP 的存在削弱或消除了 GPR 对胃磨节律的影响。这种 CCAP 作用是由于其能够在胃磨回路神经元外侧胃 (LG) 中激活与 MCN1 相同的调制器激活电导 (G(MI))。由于 GPR 通过削弱 MCN1 在 LG 中对 G(MI)的激活来延长回缩,因此 CCAP 的平行 G(MI)激活会降低 GPR 对该电导的调节作用。因此,CCAP 激活的 G(MI) 抵消了 GPR 介导的 MCN1 激活的 G(MI) 在 LG 中的减少,并降低了 GPR 调节胃磨节律的能力。因此,尽管 CCAP 既不改变回缩持续时间,也不改变 GPR 对 MCN1 的抑制作用,但它在关键下游回路神经元中激活调制器激活的电导,使 CCAP 能够削弱或消除对运动回路输出的感觉调节。