The conjugacy of the vestibulo-ocular reflex evoked by single labyrinth stimulation in awake monkeys

Abstract

It is well known that the vestibulo-ocular reflex (VOR) is conjugate when measured in the dark with minimal vergence. But the neural basis of the VOR conjugacy remains to be identified. In the present study, we measured the VOR conjugacy during single labyrinth stimulation to examine whether the VOR conjugacy depends on reciprocal stimulation of the two labyrinths. There are conflicting views on this issue. First, since the vestibular signals carried by the ascending tract of Deiters' are distributed exclusively to the motoneurons of the ipsilateral eye, the neural innervations after single labyrinth stimulation are not symmetrical for the two eyes. Thus, single labyrinth stimulation may generate disjunctive VOR responses. Second, the only published study on this issue was an electrooculography (EOG) study that reported disjunctive VOR responses during unilateral caloric irrigation (Wolfe in Ann Otol 88:79-85, 1979). Third, the VOR during unilateral caloric stimulation performed in clinical vestibular tests is routinely perceived to be conjugate. To resolve these conflicting views, the present study examined the VOR conjugacy during single labyrinth stimulation by recording binocular eye position signals in awake monkeys with a search coil technique. In contradiction to the previous EOG study and the prediction based on the asymmetry of the unilateral brainstem VOR circuits, we found that the VOR during unilateral caloric irrigation was conjugate over a wide range of conditions. We conclude that the net neural innervations received by the two eyes are symmetrical after single labyrinth stimulation, despite the apparent asymmetry in the unilateral VOR pathways. A novel role for the ascending tract of Deiters' in the VOR conjugacy is proposed.

Fig. 1

Schematic illustration of the direct angular VOR pathways that are activated during unilateral caloric stimulation. Blue line is vestibular afferent, red line is excitatory VOR interneuron projection, green line is inhibitory ipsilateral VOR interneuron projection, and black line is motoneuron or internuclear neuron projection. For simplicity, this figure only draws the direct VOR pathways. However, V_ATD, V_C and V_I are the summed neural innervations received by motoneurons from both the direct and indirect VOR pathways. K_INT and K_M are the percentages of the abducens inputs that are distributed to the internuclear and motoneuron pathways, respectively. For simplicity, we assume the same K_INT and K_M are shared by the two abducens nuclei. The ipsilateral eye is driven by the neural innervations from three sources: an excitatory innervation from the ascending tract of Deiters' (V_ATD, red line), an excitatory innervation from the contralateral abducens internuclear neurons (K_INT*V_C) and an inhibitory innervation from the ipsilateral vestibular nuclei (K_M*V_I). The contralateral eye is driven by the neural innervations from two sources: an excitatory innervation from the contralateral vestibular nuclei (K_M*V_C) and an inhibitory innervation from the ipsilateral abducens internuclear neurons (K_INT*V_I)

Fig. 2

The conjugacy of the slow phase of the nystagmus induced by the traditional (low frequency) caloric stimulation in Monkey W (cold water irrigation in the left ear). a Binocular eye position signals. Black line is for the contralateral eye and gray line for the ipsilateral eye. The two eye position traces overlay very closely, indicating conjugate horizontal eye movement. b Binocular eye velocity signals. Black line is for the contralateral eye and gray line for the ipsilateral eye. The two eye velocity traces overlay very closely, indicating conjugate horizontal eye movement. c The conjugacy index of the slow phase, defined as the slope of the regression line of the contralateral eye velocity plotted against the ipsilateral eye velocity, is 0.969. R² is 0.991. Time zero is the onset of caloric irrigation

Fig. 3

The conjugacy of the slow phase of the nystagmus induced by the caloric step stimulation in Monkey W (warm water irrigation in the right ear). a Binocular eye position signals. Black line is for the right eye and gray line for the left eye. Head orientation with respect to gravity is displayed by the thick black line in the lower panel. The step in head orientation indicates a rapid 30° backward head tilt. The two eye position traces overlay very closely, indicating conjugate horizontal eye movement. b Binocular eye velocity signals. Black line is for the right eye and gray line for the left eye. The two eye velocity traces overlay very closely, indicating conjugate horizontal eye movement. c The conjugacy index of the slow phase, defined as the slope of the regression line of the right eye velocity plotted against the left eye velocity, is 0.960. R² is 0.992. Time zero is the onset of the head tilt that is delivered after a 2-min continuous caloric irrigation. For details, see “Methods”