Ishizawa Yumiko, Ahmed Omar J, Patel Shaun R, Gale John T, Sierra-Mercado Demetrio, Brown Emery N, Eskandar Emad N
Department of Anesthesia, Critical Care and Pain Medicine,
Department of Neurology, and.
J Neurosci. 2016 Jul 20;36(29):7718-26. doi: 10.1523/JNEUROSCI.4577-15.2016.
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. We show 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 ∼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.
How information is processed by the brain during awake and anesthetized states and, crucially, during the transition is not clearly understood. We demonstrate that neuronal dynamics are very different within an interconnecting cortical network (primary somatosensory and frontal premotor area) during the loss of consciousness (LOC) induced by propofol in nonhuman primates. Coherent beta oscillations between these regions are disrupted before LOC. Pronounced but brief gamma-band oscillations appear to correspond to LOC. In addition, neurons in both of these cortices transition from responding to both tactile and auditory stimulation before LOC to only tactile modality during unconsciousness. We demonstrate that propofol-induced LOC is accompanied by spatiotemporally distinctive neuronal dynamics in this network with concurrent changes in multisensory processing.
意识与麻醉诱导的无意识状态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，以及在更深麻醉水平下，直接记录功能上相互连接的体感（S1）和额腹侧运动前区（PMv）网络中的单神经元活动和局部场电位，研究了导致丙泊酚诱导无意识的皮质内神经元动力学。猕猴接受了一项行为任务训练，该任务旨在确定逐次试验的警觉性以及对触觉和听觉刺激的神经元反应。我们发现，S1和PMv之间连贯的β振荡在LOC之前被破坏，但并非与LOC同时发生。LOC似乎对应于PMv中明显但短暂的γ/高β波段振荡（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的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中的神经元都从LOC之前对双峰（触觉和听觉）刺激有反应转变为无意识期间仅对触觉模态有反应，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伴随着体感和运动前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过程，而是一系列离散的神经变化。
大脑在清醒和麻醉状态下，以及至关重要的是在过渡过程中如何处理信息尚不清楚。我们证明，在非人灵长类动物中，丙泊酚诱导意识丧失（LOC）期间，在一个相互连接的皮质网络（初级体感区和额运动前区）内，神经元动力学非常不同。这些区域之间连贯的β振荡在LOC之前被破坏。明显但短暂的γ波段振荡似乎对应于LOC。此外，这两个皮质中的神经元都从LOC之前对触觉和听觉刺激都有反应转变为无意识期间仅对触觉模态有反应。我们证明，丙泊酚诱导的LOC伴随着该网络中时空上独特的神经元动力学以及多感觉处理的同时变化。
