Weizmann Institute of Science, Rehovot, Israel 7610001.
Weizmann Institute of Science, Rehovot, Israel 7610001
J Neurosci. 2021 Jun 2;41(22):4826-4839. doi: 10.1523/JNEUROSCI.1410-20.2021. Epub 2021 Apr 23.
Perception is an active process, requiring the integration of both proprioceptive and exteroceptive information. In the rat's vibrissal system, a classical model for active sensing, the relative contribution of the two information streams was previously studied at the peripheral, thalamic, and cortical levels. Contributions of brainstem neurons were only indirectly inferred for some trigeminal nuclei according to their thalamic projections. The current work addressed this knowledge gap by performing the first comparative study of the encoding of proprioceptive whisking and exteroceptive touch signals in the oralis (SpVo), interpolaris (SpVi), and paratrigeminal (Pa5) brainstem nuclei. We used artificial whisking in anesthetized male rats, which allows a systematic analysis of the relative contribution of the proprioceptive and exteroceptive information streams along the ascending pathways in the absence of motor or cognitive top-down modulations. We found that (1) neurons in the rostral and caudal parts of the SpVi convey whisking and touch information, respectively, as predicted by their thalamic projections; (2) neurons in the SpVo encode both whisking and (primarily) touch information; and (3) neurons of the Pa5 encode a complex combination of whisking and touch information. In particular, the Pa5 contains a relatively large fraction of neurons that are inhibited by active touch, a response observed so far only in the thalamus. Overall, our systematic characterization of afferent responses to active touch in the trigeminal brainstem approves the hypothesized functions of SpVi neurons and presents evidence that SpVo and Pa5 neurons are involved in the processing of active vibrissal touch. The present work constitutes the first comparative study of the encoding of proprioceptive (whisking) and exteroceptive (touch) information in the rat's brainstem trigeminal nuclei, the first stage of vibrissal processing in the CNS. It shows that (1) as expected, the rostral and caudal interpolaris neurons convey primarily whisking and touch information, respectively; (2) the oralis nucleus, whose function was previously unknown, encodes both whisking and (primarily) touch touch information; (3) a subtractive computation, reported at the thalamic level, already occurs at the brainstem level; and (4) a novel afferent pathway probably ascends via the paratrigeminal nucleus, encoding both proprioceptive and exteroceptive information.
感知是一个主动的过程，需要整合本体感觉和外感受信息。在大鼠的触须系统中，这是一个主动感知的经典模型，先前已经在周围、丘脑和皮质水平研究了这两种信息流的相对贡献。根据它们的丘脑投射，只有一些三叉神经核的脑干神经元的贡献是间接推断的。当前的工作通过对感觉运动刷动和外感受触摸信号在脑干的 oralis（SpVo）、interpolaris（SpVi）和 paratrigeminal（Pa5）核中的编码进行首次比较研究来解决这一知识空白。我们在麻醉雄性大鼠中使用人工刷动，这允许在没有运动或认知自上而下调制的情况下，沿上升通路系统地分析本体感觉和外感受信息流的相对贡献。我们发现：（1）SpVi 的头侧和尾侧部分的神经元分别传递刷动和触摸信息，这与它们的丘脑投射预测一致；（2）SpVo 中的神经元编码刷动和（主要）触摸信息；（3）Pa5 的神经元编码刷动和触摸信息的复杂组合。特别是，Pa5 包含相对较大比例的神经元，它们被主动触摸抑制，这种反应迄今为止仅在丘脑观察到。总的来说，我们对三叉神经脑干中主动触摸传入反应的系统表征证实了 SpVi 神经元的假设功能，并提供了证据表明 SpVo 和 Pa5 神经元参与了主动触须触觉的处理。本工作构成了大鼠脑干三叉神经核中本体感觉（刷动）和外感受（触摸）信息编码的首次比较研究，这是中枢神经系统中触须处理的第一阶段。它表明：（1）正如预期的那样，头侧和尾侧 interpolaris 神经元分别主要传递刷动和触摸信息；（2）oralis 核，其功能先前未知，编码刷动和（主要）触摸信息；（3）在脑干水平已经发生了减法计算，这在丘脑水平报道过；（4）可能通过 paratrigeminal 核上升的新传入通路，编码本体感觉和外感受信息。
