The feedback circuit connecting the superior colliculus and central mesencephalic reticular formation: a direct morphological demonstration

Abstract

The central mesencephalic reticular formation (cMRF) has been distinguished from the surrounding reticular formation due to its involvement in the control of saccades. A role in saccade function has been proposed for this region based on electrical-stimulation experiments, its neuronal activity, and its pattern of connections. The present study was undertaken in an attempt to further characterize the location of the central mesencephalic reticular formation by anatomical methods and to examine its connections with the superior colliculus at the neuronal level. Biotinylated dextran amine (BDA) was injected into the superior colliculus of two cynomolgus monkeys (Macaca fascicularis). This resulted in the retrograde labeling of a large number of neurons in a restricted area of the mesencephalic reticular formation. They were distributed bilaterally, with an ipsilateral predominance, forming a cellular band in the ventral half of the midbrain reticular formation that was 2.7 mm in its rostrocaudal extent. Its rostral pole lay dorsolateral to the red nucleus and ventrolateral to, but not immediately adjacent to, the interstitial nucleus of Cajal. The cell band was widest caudally, where it occupied an area of approximately 2.7 mm wide and 2 mm in depth. Labeled neurons displayed a wide variety of multipolar somatic shapes and sizes, with long, slightly tapering, sparsely branched dendrites. Tectal terminal arbors were also labeled within the mesencephalic reticular formation. They were concentrated bilaterally, with an ipsilateral predominance, in the same areas that contained retrogradely labeled neurons. Numerous, primarily en passant labeled boutons of various sizes and shapes were seen in close association with both labeled and unlabeled neurons. They formed axosomatic and, more commonly, axodendritic relationships with labeled neurons. The extensive relationship of labeled terminals and labeled cells suggests the existence of a strong interconnection between the deeper layers of the colliculus and the central mesencephalic reticular formation neurons projecting back to the tectum. The bidirectional neural circuit directly demonstrated in this study presumably provides an anatomical substrate for feedback modification of gaze signals generated in the colliculus. However, the presence of tectal terminals around unlabeled reticular neurons suggests that the collicular signal may also be fed forward to the downstream targets of the central mesencephalic reticular formation.