Electroanatomy of tectal efferent connections related to eye movements in the horizontal plane

1. Excitatory and inhibitory oligosynaptic pathways from the superior colliculus (CS) to ocular motoneurons engaged in horizontal eye movements were investigated in cats using acute and chronic brain stem transections in combination with intracellular recordings. 2. Isolation of the medial ponto-bulbar tegmentum from vestibular nuclei and adjacent lateral tegmental structures did not impair short-latency EPSPs and IPSPs induced by collicular stimulation in lateral rectus motoneurons (LR-MNs). On the contrary, responses were enhanced after chronic de-efferentation of vestibular nuclei. This suggests compensatory synaptic rearrangement in the tecto-reticulo-abducens pathways. 3. Midsagittal mesencephalic transections eliminated not only crossed excitatory but also ipsilateral inhibitory CS action on LR-MNs indicating that underlying pathways undergo decussation within the midbrain. 4. Midsagittal transections at different pontine and bulbar levels were performed to locate the second decussation of the inhibitory pathway. Ipsilateral IPSPs were eliminated only by deep lesions extending for about 1.5 mm rostral and caudal to the 6th nuclei. 5. Investigation of medial rectus motoneurons (MR-MNs) revealed two types of excitatory responses to CS-stimulation: (a) di- or trisynaptic EPSPs characterized by a fast rising phase and pronounced frequency potentiation; (b) slowly rising EPSPs displaying little or no frequency potentiation. 'Fast' EPSPs were abolished by all types of pontine lesions interrupting transmission through the contralateral 'abducens region' and may thus be relayed by internuclear neurons within or adjacent to the 6th nucleus. 'Slow' EPSPs persisted after transverse sections at midpontine and rostral pontine levels. 6. The trajectory of tectofugal inhibitory pathway to MR-MNs could not be followed due to a marked suppression of IPSPs under pentobarbital anesthesia. Persistence of IPSPs in LR-MNs under same conditions indicated that reciprocal inhibition of LR- and MR-MNs is mediated by different populations of inhibitory interneurons.