Organization of the cerebellum in the pigeon (Columba livia): III. Corticovestibular connections with eye and neck premotor areas

Abstract

The connections of the cerebellar cortex with vestibular premotor neurons of the oculomotor and collimotor systems in the pigeon were delineated in experiments using WGA-HRP as an anterograde and retrograde tracer. Putative premotor neuron pools were identified by injections into the oculomotor (mIII) and trochlear nuclei (mIV) and into the most rostral portion of the cervical neck motor nucleus, nucleus supraspinalis (SSp). The retrograde data indicate that ipsilateral projections upon oculomotor neurons arise from the medial portions of the superior (VeS) and tangential (Ta) nuclei. Contralateral projections originate from the infracerebellar nucleus, the interstitial vestibular region including the main (lateral) portion of the tangential nucleus, and from the descending and medial vestibular nuclei (VeD, VeM). These projections were confirmed in anterograde studies that also defined the connections of these vestibular premotor regions with specific subnuclear divisions of the pigeon's "oculomotor" nuclei (mIII, mIV, mVI). The organization of projections from the vestibular nuclei to the pigeon's extraocular motoneurons is similar to that reported in mammals. Projections upon neck premotor neurons arise primarily from neurons in the interstitial region of the vestibular nuclear complex. After injections in SSp, retrogradely labeled neurons were found, contralaterally, in the lateral part of the tangential and superior vestibular nuclei and in the dorsolateral vestibular nucleus (VDL). Ipsilateral labeling was seen in the medial interstitial region (VeM, VeD, and medial Ta). These projections were confirmed in anterograde experiments. With the exception of VDL, vestibular nuclei projecting to neck motoneurons also project to extraocular motoneurons. Thus the infracerebellar nucleus projects exclusively, and the superior vestibular nucleus predominantly, upon oculomotor (mIII, mIV) nuclei; VDL projects predominantly upon the neck motor nucleus, whereas the interstitial vestibular regions (medial Ta, rostral VeD, intermediate VeM) project upon both collimotor and oculomotor neurons. The pattern of retrograde labeling seen in the cerebellar cortex after injections into vestibular premotor nuclei was used to define the projections of specific cerebellar cortical zones upon vestibular eye and neck premotor neurons. Corticovestibular projections upon these regions arise from the auricle and lateral unfoliated cortex, the posterior lobe components of cortical zones B and E, and from the vestibulocerebellum. Each of these cortical zones projects upon components of the vestibular nuclear complex, which are premotor to either oculomotor nuclei or collimotor nuclei. The hodological findings are related to the functional organization of the oculomotor and collimotor systems in the pigeon and compared with the mammalian data.