Spontaneous Multimodal Neural Transmission Suggests That Adult Spinal Networks Maintain an Intrinsic State of Readiness to Execute Sensorimotor Behaviors

Spontaneous Multimodal Neural Transmission Suggests That Adult Spinal Networks Maintain an Intrinsic State of Readiness to Execute Sensorimotor Behaviors
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DOI:
10.1523/jneurosci.0662-21.2021
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发表时间:
2021-09-22
影响因子:
5.3
通讯作者:
McPherson, Jacob G.
McPherson, Jacob G.
中科院分区:
医学1区
文献类型:
--
作者:
Bandres, Maria F.;Gomes, Jefferson;McPherson, Jacob G.

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自发动作电位放电(spAP)在神经发育过程中普遍存在且具有功能相关性。即使在无意识状态下,spAP 仍然是成熟的脊髓上网络的一个显着特征。有证据表明,在清醒期间,spAP 持续存在于成熟的脊柱网络中,并且 spAP 在这种情况下的一项功能可能是维持执行行为的“准备状态”。 spAP 在无意识状态下在成熟脊髓网络中持续存在的程度仍不清楚,其功能(如果有的话)同样尚未解决。在这里,我们试图解决目前成人脊柱 spAP 的不完整图像中出现的一些问题和矛盾。我们同时记录了雄性大鼠体内大量脊髓中间神经元,表征了腰椎增大中 spAP 的空间分布,并识别了自发活动神经元的亚群。我们发现 (1) 整个灰质背腹侧范围内同时存在 spAP,跨层神经元类型混合多样但惊人一致; (2) 较深的感觉运动整合区域表现出 spAP 的神经元比例与较浅的感觉主导区域相当; (3) 发射率随地区系统性地变化,但尖峰序列变异性除外; (4) spAP包括与执行脊髓介导的行为一致的多模式神经传递。这些发现表明,即使在无意识状态下,成人 spAP 也可能继续支持执行感觉运动行为的准备状态。这种功能对于我们理解感知如何转化为行动、依赖于经验的行为修正以及对伤害或疾病的(不良)适应反应具有重要意义。
Spontaneous action potential discharge (spAP) is both ubiquitous and functionally relevant during neural development. spAP remains a prominent feature of supraspinal networks in maturity, even during unconsciousness. Evidence suggests that spAP persists in mature spinal networks during wakefulness, and one function of spAP in this context could be maintenance of a "ready state" to execute behaviors. The extent to which spAP persists in mature spinal networks during unconsciousness remains unclear, and its function(s), if any, are likewise unresolved. Here, we attempt to reconcile some of the questions and contradictions that emerge from the disintegrated picture of adult spinal spAP currently available. We recorded simultaneously from large populations of spinal interneurons in vivo in male rats, characterizing the spatial distribution of spAP in the lumbar enlargement and identifying subgroups of spontaneously active neurons. We find (1) concurrent spAP throughout the dorsoventral extent of the gray matter, with a diverse yet strikingly consistent mixture of neuron types across laminae; (2) the proportion of neurons exhibiting spAP in deeper, sensorimotor integrative regions is comparable to that in more superficial, sensory-dominant regions; (3) firing rate, but not spike train variability, varies systematically with region; and (4) spAP includes multimodal neural transmission consistent with executing a spinally-mediated behavior. These findings suggest that adult spAP may continue to support a state of readiness to execute sensorimotor behaviors even during unconsciousness. Such functionality has implications for our understanding of how perception is translated into action, of experience-dependent modification of behavior, and (mal)adaptative responses to injury or disease.