丘脑皮质神经元而非丘脑网状核神经元在紧张性放电和低阈值棘波爆发期间的可变动作电位反向传播。
Variable Action Potential Backpropagation during Tonic Firing and Low-Threshold Spike Bursts in Thalamocortical But Not Thalamic Reticular Nucleus Neurons.
作者信息
Connelly William M, Crunelli Vincenzo, Errington Adam C
机构信息
Neuroscience Division, School of Biosciences, Cardiff University, Cardiff CF10 3AX, United Kingdom.
Eccles Institute of Neuroscience, The John Curtin School of Medical Research, Australian National University, Acton ACT 2601, Australia.
出版信息
J Neurosci. 2017 May 24;37(21):5319-5333. doi: 10.1523/JNEUROSCI.0015-17.2017. Epub 2017 Apr 27.
Backpropagating action potentials (bAPs) are indispensable in dendritic signaling. Conflicting Ca-imaging data and an absence of dendritic recording data means that the extent of backpropagation in thalamocortical (TC) and thalamic reticular nucleus (TRN) neurons remains unknown. Because TRN neurons signal electrically through dendrodendritic gap junctions and possibly via chemical dendritic GABAergic synapses, as well as classical axonal GABA release, this lack of knowledge is problematic. To address this issue, we made two-photon targeted patch-clamp recordings from rat TC and TRN neuron dendrites to measure bAPs directly. These recordings reveal that "tonic"' and low-threshold-spike (LTS) "burst" APs in both cell types are always recorded first at the soma before backpropagating into the dendrites while undergoing substantial distance-dependent dendritic amplitude attenuation. In TC neurons, bAP attenuation strength varies according to firing mode. During LTS bursts, somatic AP half-width increases progressively with increasing spike number, allowing late-burst spikes to propagate more efficiently into the dendritic tree compared with spikes occurring at burst onset. Tonic spikes have similar somatic half-widths to late burst spikes and undergo similar dendritic attenuation. In contrast, in TRN neurons, AP properties are unchanged between LTS bursts and tonic firing and, as a result, distance-dependent dendritic attenuation remains consistent across different firing modes. Therefore, unlike LTS-associated global electrical and calcium signals, the spatial influence of bAP signaling in TC and TRN neurons is more restricted, with potentially important behavioral-state-dependent consequences for synaptic integration and plasticity in thalamic neurons. In most neurons, action potentials (APs) initiate in the axosomatic region and propagate into the dendritic tree to provide a retrograde signal that conveys information about the level of cellular output to the locations that receive most input: the dendrites. In thalamocortical and thalamic reticular nucleus neurons, the site of AP generation and the true extent of backpropagation remain unknown. Using patch-clamp recordings, this study measures dendritic propagation of APs directly in these neurons. In either cell type, high-frequency low-threshold spike burst or lower-frequency tonic APs undergo substantial voltage attenuation as they spread into the dendritic tree. Therefore, backpropagating spikes in these cells can only influence signaling in the proximal part of the dendritic tree.
反向传播动作电位(bAPs)在树突信号传导中不可或缺。相互矛盾的钙成像数据以及缺乏树突记录数据意味着丘脑皮质(TC)和丘脑网状核(TRN)神经元的反向传播程度仍然未知。由于TRN神经元通过树突 - 树突缝隙连接以及可能通过化学性树突GABA能突触进行电信号传递,同时还有经典的轴突GABA释放,这种知识的匮乏是个问题。为了解决这个问题,我们对大鼠TC和TRN神经元树突进行了双光子靶向膜片钳记录,以直接测量bAPs。这些记录表明,两种细胞类型中的“紧张性”和低阈值尖峰(LTS)“爆发性”动作电位总是先在胞体被记录到,然后反向传播到树突中,同时经历显著的距离依赖性树突幅度衰减。在TC神经元中,bAP衰减强度根据放电模式而变化。在LTS爆发期间,胞体动作电位半高宽随着尖峰数量的增加而逐渐增加,与爆发开始时出现的尖峰相比,使得爆发后期的尖峰能够更有效地传播到树突树中。紧张性尖峰与爆发后期尖峰具有相似的胞体半高宽,并经历相似的树突衰减。相比之下,在TRN神经元中,LTS爆发和紧张性放电之间的动作电位特性没有变化,因此,不同放电模式下距离依赖性树突衰减保持一致。因此,与LTS相关的全局电信号和钙信号不同,bAP信号在TC和TRN神经元中的空间影响更为受限,对丘脑神经元的突触整合和可塑性可能具有重要的行为状态依赖性后果。在大多数神经元中,动作电位(APs)在轴突 - 胞体区域起始并传播到树突树中,以提供一个逆行信号,将有关细胞输出水平的信息传递到接收大部分输入的位置:树突。在丘脑皮质和丘脑网状核神经元中,动作电位产生的部位以及反向传播的真实范围仍然未知。本研究使用膜片钳记录直接测量了这些神经元中动作电位的树突传播。在任何一种细胞类型中,高频低阈值尖峰爆发或低频紧张性动作电位在传播到树突树中时都会经历显著的电压衰减。因此,这些细胞中的反向传播尖峰只能影响树突树近端部分的信号传导。