Direct cerebellar control over motor production in a species with extreme cerebellar enlargement

The cerebellum is thought to fine-tune movement without being required for its production. However, this textbook view derives mainly from studies of mammalian species with highly developed cerebral cortices. Here we examined cerebellar function in the elephant-nose fish, a member of a family of African weakly electric fish (Mormyridae) in which the cerebellum is massively enlarged, covering the entire dorsal surface of the brain 1-5. Although the microcircuitry and anatomical connections of the mormyrid “gigantocerebellum” have been well-characterized, its function(s) remains unknown 6-11. The elephant-nose fish is named for a flexible facial appendage, the schnauzenorgan (SO), used to probe surfaces and extract prey from substrate 8,12. Here we provide evidence from microstimulation, electrophysiological recordings, and lesions for a direct and essential role for the C1 region of the mormyrid cerebellum in the production of SO movement. These findings indicate that cerebellum may be capable of performing a wider range of functions than previously thought, including roles typically ascribed to the forebrain, and emphasize the importance of evolutionary history on the functional specialization of brain regions.

学界普遍认为，小脑仅负责对运动进行微调，而非运动产生的必需环节。然而，这一经典教科书式观点主要源自对大脑皮层高度发达的哺乳动物类群的研究。本研究以象鼻鱼为研究对象——这类鱼类隶属于非洲弱电鱼科（Mormyridae），其小脑显著肥大，覆盖了大脑的整个背侧表面[1-5]。尽管象鼻鱼“巨型小脑”的微回路结构与解剖连接已得到充分解析[6-11]，但其具体功能仍不明确。象鼻鱼因其可灵活活动的面部附属结构——施瑙岑器官（schnauzenorgan，简称SO）——得名，该结构用于探查物体表面并从底质中攫取猎物[8,12]。本研究通过微刺激、电生理记录以及脑区损毁实验，提供了确凿证据表明：象鼻鱼小脑C1区域在SO运动的产生过程中发挥直接且不可或缺的作用。本研究结果显示，小脑的功能范围可能远超此前认知，甚至可承担通常被归为前脑的功能；同时也凸显了进化历史对脑区功能特化的重要意义。