Dynamics of Propofol-Induced Loss of Consciousness Across Primate Neocortex

Dynamics of Propofol-Induced Loss of Consciousness Across Primate Neocortex
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DOI:
10.1523/jneurosci.4577-15.2016
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发表时间:
2016-07-20
影响因子:
5.3
通讯作者:
Eskandar, Emad N.
Eskandar, Emad N.
中科院分区:
医学1区
文献类型:
--
作者:
Ishizawa, Yumiko;Ahmed, Omar J.;Eskandar, Emad N.

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意识与麻醉诱导的无意识之间转换的精确神经机制仍不清楚。在此,我们通过在从完全清醒到意识丧失(LOC)的逐渐行为转变过程中以及在更深的麻醉水平下,直接在功能上相互连接的躯体感觉(S1)和额叶腹侧前运动(PMv)网络中记录单神经元活动和局部场电位,研究了导致丙泊酚诱导的无意识的皮质内神经元动力学。猕猴接受了一项行为任务的训练,该任务旨在确定每次试验的警觉性以及对触觉和听觉刺激的神经元反应。我们表明,S1和PMv之间相干的β振荡的破坏先于LOC,但与LOC并不同步。LOC似乎对应于PMv中明显但短暂的γ/高β频段振荡(持续约3分钟),随后是S1中的γ峰值。我们还证明,慢振荡在S1中在LOC之后出现,然后在PMv中延迟出现,这共同表明在LOC期间S1和PMv的神经元动力学非常不同。最后,S1和PMv中的神经元从在LOC之前对双模式(触觉和听觉)刺激有反应转变为在无意识期间仅对触觉模式有反应,这与该网络中多感觉整合的抑制一致。我们的结果表明,丙泊酚诱导的LOC伴随着躯体感觉和前运动网络中时空上不同的振荡神经元动力学,并表明从清醒到无意识的过渡状态不是一个连续的过程,而是一系列离散的神经变化。
The precise neural mechanisms underlying transitions between consciousness and anesthetic-induced unconsciousness remain unclear. Here, we studied intracortical neuronal dynamics leading to propofol-induced unconsciousness by recording single-neuron activity and local field potentials directly in the functionally interconnecting somatosensory (S1) and frontal ventral premotor (PMv) network during a gradual behavioral transition from full alertness to loss of consciousness (LOC) and on through a deeper anesthetic level. Macaque monkeys were trained for a behavioral task designed to determine the trial-by-trial alertness and neuronal response to tactile and auditory stimulation. Weshow that disruption of coherent beta oscillations between S1 and PMv preceded, but did not coincide with, the LOC. LOC appeared to correspond to pronounced but brief gamma-/high-beta-band oscillations (lasting similar to 3 min) in PMv, followed by a gamma peak in S1. We also demonstrate that the slow oscillations appeared after LOC in S1 and then in PMv after a delay, together suggesting that neuronal dynamics are very different across S1 versus PMv during LOC. Finally, neurons in both S1 and PMv transition from responding to bimodal (tactile and auditory) stimulation before LOC to only tactile modality during unconsciousness, consistent with an inhibition of multisensory integration in this network. Our results show that propofol-induced LOC is accompanied by spatiotemporally distinct oscillatory neuronal dynamics across the somatosensory and premotor network and suggest that a transitional state from wakefulness to unconsciousness is not a continuous process, but rather a series of discrete neural changes.