Functional organization of eye velocity and eye position signals in abducens motoneurons of the frog

Summary

• 1. Eccentric eye positions evoked by constant velocity optokinetic stimuli, can be maintained in the dark over many minutes. Eye positions with similar eccentricities but evoked by vestibular velocity steps are maintained transiently and drift then rapidly back towards a neutral position. The motor organization of ‘move’ and ‘hold’ commands required for these behavioral responses were studied at the level of the abducens motor output.

• 2. Morphometrical studies of the somata of abducens motoneurons (ABM) and of retractor bulbi motoneurons (RBM) showed that cell diameters of RBM (30.61±4.5 μm;n=209) are significantly larger than those of ABM (20.8±5.4 μm;n=219). Axons of ABM, comprising about 60% (76±7) of the total number of abducens axons (125±13;n=10), have diameters with a major peak around 3 μm and a minor peak around 7–8 μm. The distribution of RBM axon diameters overlaps with that of the thicker ABM axons.

• 3. Physiological studies of antidromically identified ABM and RBM allowed a separation between the two, since RBM responded to tactile but not to optokinetic and vestibular stimuli. Differences in response characteristics between ABM to optokinetic stimuli in the open loop situation allowed further separation into three different subpopulations: the largest ABM mediate signals related to retinal image slip velocity; the smallest ABM mediate signals related to intended eye position and a third group of relatively large ABM mediates velocity plus position related signals. A wiring diagram is proposed, describing which types of ABM are connected with which types of fibers of the lateral rectus muscle.

• 4. From the position related signals of part of the ABM, the characteristics of the frog's velocity-to-position integrating network were deduced. Charge of the integrator depends on both duration and magnitude of stimulation. Discharge is approximately linear and has apparent time constants in the order of about 90 s. Optokinetic stimuli in the on- and off-direction interact algebraically. Vestibularly evoked motor signals abruptly decay after a period of time that is stimulus dependent. These differences suggest the presence of different integrating networks for optokinetically and vestibularly evoked activity.

• 5. The biological relevance of a position integrator, that has remarkably little ‘leakiness’ in comparison with that in mammals is discussed in conjunction with the frog's predatory strategy: ‘wait and see’.