Neural Correlates of the Dependence of Compensatory Eye Movements During Translation on Target Distance and Eccentricity

Abstract

To stabilize objects of interest on the fovea during translation, vestibular-driven compensatory eye movements [translational vestibulo-ocular reflex (TVOR)] must scale with both target distance and eccentricity. To identify the neural correlates of these properties, we recorded from different groups of eye movement–sensitive neurons in the prepositus hypoglossi and vestibular nuclei of macaque monkeys during lateral and fore-aft displacements. All neuron types exhibited some increase in modulation amplitude as a function of target distance during high-frequency (4 Hz) lateral motion in darkness, with slopes that were correlated with the cell's pursuit gain, but not eye position sensitivity. Vergence angle dependence was largest for burst-tonic (BT) and contralateral eye-head (EH) neurons and smallest for ipsilateral EH and position-vestibular-pause (PVP) cells. On the other hand, the EH and PVP neurons with ipsilateral eye movement preferences exhibited the largest vergence-independent responses, which would be inappropriate to drive the TVOR. In addition to target distance, the TVOR also scales with target eccentricity, as evidenced during fore-aft motion, where eye velocity amplitude exhibits a “V-shaped ” dependence and phase shifts 180° for right versus left eye positions. Both the modulation amplitude and phase of BT and contralateral EH cells scaled with eye position, similar to the evoked eye movements during fore-aft motion. In contrast, the response modulation of ipsilateral EH and PVP cells during fore-aft motion was characterized by neither the V-shaped scaling nor the phase reversal. These results show that distinct premotor cell types carry neural signals that are appropriately scaled by vergence angle and eye position to generate the geometrically appropriate compensatory eye movements in the translational vestibulo-ocular reflex.

The horizontal angular vestibulo-ocular reflex: A non-linear mechanism for context-dependent responses

“…Despite assigning nonlinear computations only to EHV cells to modulate VOR gain, the depth of both EHV and PVP modulations varies linearly with vergence angle, consistent with experimental observations [22]. In fact, given central targets E R = E L , the non-linear surface embeds a line relating vergence with monocular angle (Fig .7), and the gain of EHV cells follows the line of E verg = −2E L on the nonlinear surface.…”

“…Moreover, the slope of vergence dependence is larger for both right and left EHV cells compared to PVP cells. As in [22] where type I PVP cells show a negative vergence slope, right PVPs in our model have a negative slope while the left PVPs show little increase in their firing modulations with vergence. This suggests that despite assigning nonlinear computations in the premotor circuit of our bilateral model, the characteristics of the model neurons are similar to experimental results using the same conditions and analysis method.…”

“…It should be noted that although the reported results [22] are from experiments on monkeys, here we are comparing the general characteristics from the VN cells, that is, linear variation of the depth of modulations in EHV cells and PVP cells with vergence and positive or negative slope of such variations. These general characteristics will hold regardless of species-dependent interocular distance.…”

“…Third, adding more projections and loops between more elements in a bilateral model will only affect the current assigned projection weights and not the general characteristics of the bilateral model. EHV cells are known to behave nonlinearly and also exhibit vergence dependent behavior [21], [5], [22]. In the former model [9], context dependency relied on a single nonlinearity applied after the sum of EHV afferent signals.…”

“…Experiments by Meng et. al [22] included single unit recordings from PVPs and EHVs in macaque monkeys during both translational and rotational VOR in the dark. According to their observations during 4 Hz rotations in the dark and after extinguishing the target at different distances, the modulation depth on EHV and PVP firing rates was shown to relate linearly to vergence angle (see Fig.…”