Ushimaru Mika, Kawaguchi Yasuo
Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki 444-8787, Japan, Japan Science and Technology Agency, Core Research for Evolutional Science and Technology, Tokyo 102-0076, Japan.
Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki 444-8787, Japan, Department of Physiological Sciences, SOKENDAI (Graduate University for Advanced Studies), Okazaki 444-8787, Japan, and Japan Science and Technology Agency, Core Research for Evolutional Science and Technology, Tokyo 102-0076, Japan
J Neurosci. 2015 Aug 26;35(34):11988-2001. doi: 10.1523/JNEUROSCI.5074-14.2015.
Slow-wave oscillations, the predominant brain rhythm during sleep, are composed of Up/Down cycles. Depolarizing Up-states involve activity in layer 5 (L5) of the neocortex, but it is unknown how diverse subtypes of neurons within L5 participate in generating and maintaining Up-states. Here we compare the in vivo firing patterns of corticopontine (CPn) pyramidal cells, crossed-corticostriatal (CCS) pyramidal cells, and fast-spiking (FS) GABAergic neurons in the rat frontal cortex, with those of thalamocortical neurons during Up/Down cycles in the anesthetized condition. During the transition from Down- to Up-states, increased activity in these neurons was highly temporally structured, with spiking occurring first in thalamocortical neurons, followed by cortical FS cells, CCS cells, and, finally, CPn cells. Activity in some FS, CCS, and CPn neurons occurred in phase with Up-nested gamma rhythms, with FS neurons showing phase delay relative to pyramidal neurons. These results suggest that thalamic and cortical pyramidal neurons are activated in a specific temporal sequence during Up/Down cycles, but cortical pyramidal cells are activated at a similar gamma phase. In addition to Up-state firing specificity, CCS and CPn cells exhibited differences in activity during cortical desynchronization, further indicating projection- and state-dependent information processing within L5.
Patterned activity in neocortical electroencephalograms, including slow waves and gamma oscillations, is thought to reflect the organized activity of neocortical neurons that comprises many specialized neuron subtypes. We found that the timing of action potentials during slow waves in individual cortical neurons was correlated with their laminar positions and axonal targets. Within gamma cycles nested in the slow-wave depolarization, cortical pyramidal cells fired earlier than did interneurons. At the start of slow-wave depolarizations, activity in thalamic neurons receiving inhibition from the basal ganglia occurred earlier than activity in cortical neurons. Together, these findings reveal a temporally ordered pattern of output from diverse neuron subtypes in the frontal cortex and related thalamic nuclei during neocortical oscillations.
慢波振荡是睡眠期间的主要脑节律，由上升/下降周期组成。去极化上升状态涉及新皮质第5层（L5）的活动，但尚不清楚L5内不同亚型的神经元如何参与上升状态的产生和维持。在这里，我们比较了大鼠额叶皮质中皮质脑桥（CPn）锥体细胞、交叉皮质纹状体（CCS）锥体细胞和快发放（FS）GABA能神经元在麻醉状态下上升/下降周期中的体内放电模式，以及丘脑皮质神经元的放电模式。在从下降状态到上升状态的转变过程中，这些神经元活动的增加在时间上具有高度的结构性，丘脑皮质神经元首先放电，随后是皮质FS细胞、CCS细胞，最后是CPn细胞。一些FS、CCS和CPn神经元的活动与上升嵌套伽马节律同步发生，FS神经元相对于锥体细胞表现出相位延迟。这些结果表明，在上升/下降周期中，丘脑和皮质锥体细胞按特定的时间顺序被激活，但皮质锥体细胞在相似的伽马相位被激活。除了上升状态放电特异性外，CCS和CPn细胞在皮质去同步化期间的活动也表现出差异，进一步表明L5内存在投射和状态依赖的信息处理。
新皮质脑电图中的模式化活动，包括慢波和伽马振荡，被认为反映了由许多专门神经元亚型组成的新皮质神经元的有组织活动。我们发现，单个皮质神经元在慢波期间动作电位的时间与其层位和轴突靶点相关。在慢波去极化嵌套的伽马周期内，皮质锥体细胞比中间神经元更早放电。在慢波去极化开始时，接受基底神经节抑制的丘脑神经元的活动比皮质神经元的活动更早出现。总之，这些发现揭示了新皮质振荡期间额叶皮质和相关丘脑核中不同神经元亚型输出的时间有序模式。
