Two dynamically distinct inhibitory networks in layer 4 of the neocortex

Two dynamically distinct inhibitory networks in layer 4 of the neocortex
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DOI:
10.1152/jn.00283.2003
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发表时间:
2003-11-01
影响因子:
2.5
通讯作者:
Connors, BW
Connors, BW
中科院分区:
医学3区
文献类型:
--
作者:
Beierlein, M;Gibson, JR;Connors, BW

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新皮层的正常运作主要依赖于几种类型的抑制性中间神经元,但每种类型的具体功能尚不清楚。一种可能性是,中间神经元被不同频率和时间的活动模式所不同地参与。为了探索这一点,我们研究了大鼠桶状皮层第4层的两种抑制性中间神经元:快速spike (FS)细胞和低阈值spike (LTS)细胞,连接局部兴奋性神经元(常规spike,或RS细胞)的化学突触的强度和短期动力学。我们还测试了通往中间神经元的另外两条通路:丘脑皮质连接和第6层皮质丘脑投射神经元的循环侧支。连接RS细胞和FS细胞的兴奋性和抑制性突触对单一刺激的反应高度可靠,并表现出强烈的短期抑制。相反,连接RS和LTS细胞的兴奋性和抑制性突触在最初激活时不太可靠。RS细胞对LTS细胞的兴奋性突触表现出显著的短期易化,而LTS细胞对RS细胞的抑制性突触表现出中度或轻度易化。丘脑皮质输入对RS细胞和FS细胞均有强烈的刺激作用,但对LTS细胞的刺激作用很少且仅微弱。这两种类型的中间神经元都被皮质丘脑神经元轴突侧侧的便利突触强烈激发。我们得出结论,在新皮层的第4层有两个平行但动态不同的突触抑制系统,每个系统都由其固有的尖峰特性、化学突触的短期可塑性和(如前所述)一组独特的电突触来定义。由于其独特的动态特性,每个抑制网络将被皮层活动的不同时间模式所招募。
Normal operations of the neocortex depend critically on several types of inhibitory interneurons, but the specific function of each type is unknown. One possibility is that interneurons are differentially engaged by patterns of activity that vary in frequency and timing. To explore this, we studied the strength and short-term dynamics of chemical synapses interconnecting local excitatory neurons (regular-spiking, or RS, cells) with two types of inhibitory interneurons: fast-spiking (FS) cells, and low-threshold spiking (LTS) cells of layer 4 in the rat barrel cortex. We also tested two other pathways onto the interneurons: thalamocortical connections and recurrent collaterals from corticothalamic projection neurons of layer 6. The excitatory and inhibitory synapses interconnecting RS cells and FS cells were highly reliable in response to single stimuli and displayed strong short-term depression. In contrast, excitatory and inhibitory synapses interconnecting the RS and LTS cells were less reliable when initially activated. Excitatory synapses from RS cells onto LTS cells showed dramatic short-term facilitation, whereas inhibitory synapses made by LTS cells onto RS cells facilitated modestly or slightly depressed. Thalamocortical inputs strongly excited both RS and FS cells but rarely and only weakly contacted LTS cells. Both types of interneurons were strongly excited by facilitating synapses from axon collaterals of corticothalamic neurons. We conclude that there are two parallel but dynamically distinct systems of synaptic inhibition in layer 4 of neocortex, each defined by its intrinsic spiking properties, the short-term plasticity of its chemical synapses, and (as shown previously) an exclusive set of electrical synapses. Because of their unique dynamic properties, each inhibitory network will be recruited by different temporal patterns of cortical activity.