Mapping the oculomotor system

Abstract:

Over the last three decades and together with Bernard Cohen, Volker Henn, Ulrich Büttner, and Anja Horn, it has been possible to morphologically identify several functional cell groups in the oculomotor system: the medium-sized horizontal excitatory and inhibitory burst neurons (EBNs, IBNs) in the paramedian pontine reticular formation (PPRF), the more sparsely scattered vertical EBNs in the rostral interstitial nucleus of the MLF (RIMLF), and the typically elongated omnipause neurons (OPNs) in nucleus raphé interpositus — all essential for the generation of saccades. In contrast, the role of the central mesencephalic reticular formation (cMRF) in saccades is more complex, as is the morphological outlining of its borders. A detailed study of the extraocular motoneurons showed that they can be divided into two separate types: those for singly innervated (twitch) muscle fibres (SIFs) and those for multiply innervated (non-twitch) muscle fibres (MIFs). The two motoneuron types receive different premotor afferents, proving that MIF and SIF motoneurons have different functions. The cell groups were outlined by different tract tracing methods including rabies virus. The localization and histochemical characterization of all these functional cell groups in monkey formed the basis for the identification of the homologous groups in the human brainstem. Taken together these studies provide a neuroanatomical background for understanding clinical eye movement disorders.

Introduction

In the early 1970s the introduction of two new techniques made a great impact on the understanding of the central nervous system. First, was the development of stable single-unit recordings in awake mammals, a technique pioneered by K.-P. Schaefer many years ago. Second, was the development of sensitive and reliable tract tracing techniques, based on retrograde and anterograde axonal transport of substances like horseradish peroxidase and radioactive leucine, that replaced the inaccurate degeneration techniques. At this time eye movements were generally considered to be a subfeature of the vestibular system rather than a field of their own. Clinical observations had shown that the paramedian pontine reticular formation (PPRF) was associated with the generation of horizontal conjugate eye movements but the reason for this, the functional cells groups or anatomical pathways involved, were all unknown. At Mount Sinai Hospital New York, Morris Bender and later Bernie Cohen started stimulation experiments in monkeys to locate the horizontal eye movement area more exactly (Bender and Shanzer, 1964; Goebel et al., 1971; Cohen and Komatsuzaki, 1972). With the advent of chronic unit recordings it became clear from several parallel studies of the PPRF that the pontine neurons encoded precisely the parameters of the subsequent eye movement, and from their activity one could predict the subsequent saccade (Cohen and Henn, 1972; Luschei and Fuchs, 1972; Keller, 1974). From this point on the analysis of the oculomotor system exploded into one of the most popular fields of investigation, in which physiologists, like Bernard Cohen, and system-modellers like David Robinson, worked together with clinicians and neuroanatomists to understand how the brain moved the eye. In this article I will describe some of the functional cell groups of the oculomotor system, which we have outlined over the last 30 years, in both monkey and man. These studies were only possible because of the long-standing support of Bernard Cohen, Volker Henn, Ulrich Buettner, and Anja Horn.