Dickman J David, Angelaki Dora E
Department of Research, Central Institute for the Deaf, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
J Neurophysiol. 2002 Dec;88(6):3518-33. doi: 10.1152/jn.00518.2002.
Sensory signal convergence is a fundamental and important aspect of brain function. Such convergence may often involve complex multidimensional interactions as those proposed for the processing of otolith and semicircular canal (SCC) information for the detection of translational head movements and the effective discrimination from physically congruent gravity signals. In the present study, we have examined the responses of primate rostral vestibular nuclei (VN) neurons that do not exhibit any eye movement-related activity using 0.5-Hz translational and three-dimensional (3D) rotational motion. Three distinct neural populations were identified. Approximately one-fourth of the cells exclusively encoded rotational movements (canal-only neurons) and were unresponsive to translation. The canal-only central neurons encoded head rotation in SCC coordinates, exhibited little orthogonal canal convergence, and were characterized with significantly higher sensitivities to rotation as compared to primary SCC afferents. Another fourth of the neurons modulated their firing rates during translation (otolith-only cells). During rotations, these neurons only responded when the axis of rotation was earth-horizontal and the head was changing orientation relative to gravity. The remaining one-half of VN neurons were sensitive to both rotations and translations (otolith + canal neurons). Unlike primary otolith afferents, however, central neurons often exhibited significant spatiotemporal (noncosine) tuning properties and a wide variety of response dynamics to translation. To characterize the pattern of SCC inputs to otolith + canal neurons, their rotational maximum sensitivity vectors were computed using exclusively responses during earth-vertical axis rotations (EVA). Maximum sensitivity vectors were distributed throughout the 3D space, suggesting strong convergence from multiple SCCs. These neurons were also tested with earth-horizontal axis rotations (EHA), which would activate both vertical canals and otolith organs. However, the recorded responses could not be predicted from a linear combination of EVA rotational and translational responses. In contrast, one-third of the neurons responded similarly during EVA and EHA rotations, although a significant response modulation was present during translation. Thus this subpopulation of otolith + canal cells, which included neurons with either high- or low-pass dynamics to translation, appear to selectively ignore the component of otolith-selective activation that is due to changes in the orientation of the head relative to gravity. Thus contrary to primary otolith afferents and otolith-only central neurons that respond equivalently to tilts relative to gravity and translational movements, approximately one-third of the otolith + canal cells seem to encode a true estimate of the translational component of the imposed passive head and body movement.
感觉信号汇聚是脑功能的一个基本且重要的方面。这种汇聚通常可能涉及复杂的多维相互作用，就像处理耳石和半规管（SCC）信息以检测头部平移运动以及有效区分物理上一致的重力信号时所提出的那样。在本研究中，我们使用0.5赫兹的平移和三维（3D）旋转运动，研究了灵长类动物吻侧前庭核（VN）中那些不表现出任何与眼动相关活动的神经元的反应。识别出了三个不同的神经群体。大约四分之一的细胞专门编码旋转运动（仅半规管神经元），对平移无反应。仅半规管的中枢神经元以SCC坐标编码头部旋转，几乎没有正交半规管汇聚，并且与初级SCC传入纤维相比，其对旋转的敏感性显著更高。另外四分之一的神经元在平移过程中调节其放电频率（仅耳石细胞）。在旋转过程中，这些神经元仅在旋转轴为地平面且头部相对于重力改变方向时做出反应。其余一半的VN神经元对旋转和平移都敏感（耳石 + 半规管神经元）。然而，与初级耳石传入纤维不同，中枢神经元通常表现出显著的时空（非余弦）调谐特性以及对平移的多种反应动力学。为了表征半规管输入到耳石 + 半规管神经元的模式，仅使用地垂直轴旋转（EVA）期间的反应来计算它们的旋转最大敏感性向量。最大敏感性向量分布在整个3D空间中，表明来自多个SCC的强烈汇聚。还用地水平轴旋转（EHA）对这些神经元进行了测试，EHA会激活垂直半规管和耳石器官。然而，记录的反应无法从EVA旋转和平移反应的线性组合中预测出来。相比之下，三分之一的神经元在EVA和EHA旋转期间反应相似，尽管在平移过程中存在显著的反应调制。因此，这个耳石 + 半规管细胞亚群，包括对平移具有高通或低通动力学的神经元，似乎选择性地忽略了由于头部相对于重力的方向变化而导致的耳石选择性激活成分。因此，与对相对于重力的倾斜和平移运动做出等效反应的初级耳石传入纤维和仅耳石的中枢神经元相反，大约三分之一的耳石 + 半规管细胞似乎编码了施加的被动头部和身体运动的平移成分的真实估计。
