Statistics of the Vestibular Input Experienced during Natural Self-Motion: Implications for Neural Processing

Statistics of the Vestibular Input Experienced during Natural Self-Motion: Implications for Neural Processing
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DOI:
10.1523/jneurosci.0692-14.2014
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发表时间:
2014-06-11
影响因子:
5.3
通讯作者:
Cullen, Kathleen E.
Cullen, Kathleen E.
中科院分区:
医学1区
文献类型:
--
作者:
Carriot, Jerome;Jamali, Mohsen;Cullen, Kathleen E.

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人们普遍认为,感觉系统针对自然环境中发生的刺激进行了优化。然而,这一原理是否适用于前庭系统仍不清楚,前庭系统有助于基本的大脑功能,从最自动的反射到空间感知和运动协调。在这里,我们首次量化了在典型的日常活动中自由移动的人类受试者所经历的自然前庭输入的统计数据。尽管之前的研究发现,跨感觉模式的自然信号的功率谱按照幂律(即 1/f(alpha))衰减,但我们发现这并不适用于自然前庭刺激。相反,对于所有运动维度,功率在较低频率下缓慢下降,在较高频率下更快下降。我们进一步确定这种独特的刺激结构是主动运动以及在任何神经处理之前发生的被动生物力学过滤的结果。值得注意的是,当受试者被动经历感官刺激时,转变频率(即功率开始迅速下降的频率)低于他们通过自己的运动主动控制刺激时的频率。与头部测量的信号相比,外部产生的(即被动的)环境运动的频谱内容确实遵循幂律。具体来说,运动控制和生物力学引起的转换在神经处理之前形成了自然前庭刺激的统计数据。我们认为,自然前庭刺激的独特结构将对这一基本感觉系统用来表示日常生活中自我运动的神经编码策略产生重要影响。
It is widely believed that sensory systems are optimized for processing stimuli occurring in the natural environment. However, it remains unknown whether this principle applies to the vestibular system, which contributes to essential brain functions ranging from the most automatic reflexes to spatial perception and motor coordination. Here we quantified, for the first time, the statistics of natural vestibular inputs experienced by freely moving human subjects during typical everyday activities. Although previous studies have found that the power spectra of natural signals across sensory modalities decay as a power law (i.e., as 1/f(alpha)), we found that this did not apply to natural vestibular stimuli. Instead, power decreased slowly at lower and more rapidly at higher frequencies for all motion dimensions. We further establish that this unique stimulus structure is the result of active motion as well as passive biomechanical filtering occurring before any neural processing. Notably, the transition frequency (i.e., frequency at which power starts to decrease rapidly) was lower when subjects passively experienced sensory stimulation than when they actively controlled stimulation through their own movement. In contrast to signals measured at the head, the spectral content of externally generated (i.e., passive) environmental motion did follow a power law. Specifically, transformations caused by both motor control and biomechanics shape the statistics of natural vestibular stimuli before neural processing. We suggest that the unique structure of natural vestibular stimuli will have important consequences on the neural coding strategies used by this essential sensory system to represent self-motion in everyday life.