Edwin Gilland

Evolutionary Patterns of Cranial Nerve Efferent Nuclei in Vertebrates

All vertebrates have a similar series of rhombomeric hindbrain segments within which cranial nerve efferent nuclei are distributed in a similar rostrocaudal sequence. The registration between these two morphological patterns is reviewed here to highlight the conserved vs. variable aspects of hindbrain organization contributing to diversification of efferent sub-nuclei. Recent studies of segmental origins and migrations of branchiomotor, visceromotor and octavolateral efferent neurons revealed more segmental similarities than differences among vertebrates. Nonetheless, discrete variations exist in the origins of trigeminal, abducens and glossopharyngeal efferent nuclei. Segmental variation of the abducens nucleus remains the sole example of efferent neuronal homeosis during vertebrate hindbrain evolution. Comparison of cranial efferent segmental variations with surrounding intrinsic neurons will distinguish evolutionary changes in segment identity from lesser transformations in expression of unique neuronal types. The diversification of motoneuronal subgroups serving new muscles and functions appears to occur primarily by elaboration within and migration from already established segmental efferent pools rather than by de novo specification in different segmental locations. Identifying subtle variations in segment-specific neuronal phenotypes requires studies of cranial efferent organization within highly diverse groups such as teleosts and mammals.

Preservation of segmental hindbrain organization in adult frogs.

To test for possible retention of early segmental patterning throughout development, the cranial nerve efferent nuclei in adult ranid frogs were quantitatively mapped and compared with the segmental organization of these nuclei in larvae. Cranial nerve roots IV–X were labeled in larvae with fluorescent dextran amines. Each cranial nerve efferent nucleus resided in a characteristic segmental position within the clearly visible larval hindbrain rhombomeres (r). Trochlear motoneurons were located in r0, trigeminal motoneurons in r2–r3, facial branchiomotor and vestibuloacoustic efferent neurons in r4, abducens and facial parasympathetic neurons in r5, glossopharyngeal motoneurons in r6, and vagal efferent neurons in r7–r8 and rostral spinal cord. In adult frogs, biocytin labeling of cranial nerve roots IV–XII and spinal ventral root 2 in various combinations on both sides of the brain revealed precisely the same rostrocaudal sequence of efferent nuclei relative to each other as observed in larvae. This indicates that no longitudinal migratory rearrangement of hindbrain efferent neurons occurs. Although rhombomeres are not visible in adults, a segmental map of adult cranial nerve efferent nuclei can be inferred from the strict retention of the larval hindbrain pattern. Precise measurements of the borders of adjacent efferent nuclei within a coordinate system based on external landmarks were used to create a quantitative adult segmental map that mirrors the organization of the larval rhombomeric framework. Plotting morphologically and physiologically identified hindbrain neurons onto this map allows the physiological properties of adult hindbrain neurons to be linked with the underlying genetically specified segmental framework. J. Comp. Neurol. 494:228–245, 2006.

Otolith ocular reflex function of the tangential nucleus in teleost fish.

Abstract: In teleost fish, the tangential nucleus can be identified as a compact, separate cell group lying ventral to the VIIIth nerve near the middle of the vestibular complex. Morphological analysis of larval and adult hindbrains utilizing biocytin and fluorescent tracers showed the tangential nucleus to be located entirely within rhombomeric segment 5 with all axons projecting into the contralateral MLF. Combined single‐cell electrophysiology and morphology in alert goldfish found three classes of neurons whose physiological sensitivity could be readily correlated with rotational axes about either the anterior (45°), posterior (135°), or horizontal (vertical axis) semicircular canals. Tangential neurons could be distinguished from those in semicircular‐canal specific subnuclei by an irregular, spontaneous background of 10‐15 sp/s and sustained static sensitivity after ±4° head displacements. Each axis‐specific tangential subtype terminated appropriately onto oculomotor subnuclei responsible for either vertical, torsional, or horizontal eye movements and, in a few cases, axon collaterals descended in the MLF toward the spinal cord. We hypothesize, therefore, that the tangential nucleus consists of 3 axis‐specific phenotypes that process gravitoinertial signals largely responsible for controlling oculomotor function, but that also in part, maintain body posture.

Segmental Organization of Vestibular and Reticular Projections to Spinal and Oculomotor Nuclei in the Zebrafish and Goldfish

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Instrumentation for Measuring Oculomotor Performance and Plasticity in Larval Organisms

Publisher Summary This chapter highlights instrumentation for measuring the oculomotor performance and plasticity in larval organisms. The oculomotor system is ideal as it has been extensively utilized for quantitative analysis; however, no complete apparatus exists to both elicit and measure the eye movements in small genetic model organisms in real time. Instrumentation designed for much larger animals must be scaled to accommodate animals only a few millimeters in length, while accurately quantifying the motion of the minuscule eyes. This instrumentation permits high resolution ontogenetic analysis of oculomotor function in small animals as illustrated for larval zebrafish. Moreover, the miniaturized vestibular turntable and optokinetic drum, combined with the novel approach to larval animal immobilization and real-time eye position measurement, represent significant advances in the ability to study eye movements in several species of larval and juvenile animals. Classical physiological methods, combined with imaging approaches, allow structural changes to neuronal architecture as well as genetic mis-expression to be effectively and quantitatively linked with the functional changes in oculomotor behavior.

Central pathways mediating oculomotor reflexes in an elasmobranch, Scyliorhinus canicula.

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