The hypothesis of the uniqueness of the oculomotor neural integrator: direct experimental evidence in the cat.

Abstract

1. As far as horizontal eye movements are concerned, the well-known hypothesis, not yet experimentally proved, of the common neural integrator states that the eye-position signal is generated by a common network, regardless of the type of versional movement. The aim of this study was to evaluate the validity of this hypothesis by checking whether the sensitivity to eye position of the neurones of the nucleus prepositus hypoglossi (NPH) (the main component of the system integrating the different incoming velocity signals) would be the same regardless of the type of versional movement. 2. The discharge of sixty-five NPH neurones was recorded in the alert cat during spontaneous eye movements made in the light and in response to sinusoidal rotations of the head in complete darkness. 3. For each NPH neurone, the sensitivity to eye position was determined from measurements carried out during intersaccadic fixation. The discharge rate of the studied neurone was plotted against eye position. The slope of the resulting regression line gave the sensitivity (measured during intersaccadic fixation in the light) of the neurone to eye position, which was termed Kf. 4. A new method was developed to measure the sensitivity to eye position (Kr) of neurones during vestibular slow phases. The difficulty came from the fact that, during slow phases, eye velocity and eye position changed simultaneously and that each of those two variables could influence neuronal activity. For each neurone, the instantaneous firing rate was measured each time the eye passed through a given position during any slow phase generated during any vestibulo-ocular reflex. At a given position, the discharge rate of the neurone under study was plotted against the eye velocity. From the resulting linear regression line, two interesting values were obtained: its slope, corresponding to the sensitivity of the neurone to eye velocity, R;, (at that given eye position) and its 'y'-intercept, F(O), the interpolated firing rate when the eye velocity was zero. This procedure was repeated for different eye positions. The values of F(O) were then plotted against the eye positions. The slope of the resulting regression line gave the sensitivity (measured during vestibular stimulation) of the neurone to eye position, which was termed K,. 5. The errors on the individual values of Kf and K, were assessed in order to allow a statistical comparison at the single unit level. 6. We found that, for each of our sixty-five neurones, the sensitivity to eye position measured during intersaccadic fixation in the light was equal to the sensitivity to eye position measured during the vestibulo-ocular reflex (VOR) elicited in complete darkness. We conclude that our results favour the hypothesis of a unique horizontal oculomotor integrator for all versional movements.

Mechanisms of Action and Targets of Nitric Oxide in the Oculomotor System

“…Thus, lesions in the PH and /or M V nuclei of cats and monkeys produced simultaneous alterations of integration in the different subsystems tested (Cheron et al, 1986a,b;C annon and Robinson, 1987). Furthermore, Godaux and Cheron (1996) have reported that in alert cats the eye position sensitivity of PH neurons during intersaccadic fixation was equal to that measured during VOR. However, some pharmacological results suggest that at least some of the subsystems may have separate integrators (Godaux and Laune, 1983;Pastor et al, 1994;Yokota et al, 1994).…”

“…Similarly, small permanent lesions of the primate marginal zone caused by ibotenic acid impaired the gaze-holding in the horizontal plane but not the integration of signals from vestibular sources (Kaneko, 1992(Kaneko, , 1997. The lateral location of this area, ϳ2 mm from the midline, may explain why Godaux and Cheron (1996), while exploring an area located 1.2-1.6 mm from the midline, did not record neurons with position sensitivity specific for postsaccadic fixations.…”

“…Depending on the target, velocity imbalance and/or integration deficit will occur, leading to well characterized abnormal eye movements (C annon and Robinson, 1987;Godaux et al, 1993;Mettens et al, 1994;Pastor et al, 1994;Godaux and Cheron, 1996), which are schematically represented in Figure 1. Each PH nucleus simultaneously receives excitatory and inhibitory signals from the contralateral and ipsilateral M V nuclei, respectively (Baker and Berthoz, 1975).…”

Self-selected modular recurrent neural networks with postural and inertial subnetworks applied to complex movements

“…This result is in accordance with biology: tonic and phasic neurons are also found in different brain nuclei (such as in the oculomotor system). For example, in the paramedian reticular formation, the majority of the neurons related to the control of eye movements are phasic neurons coding an eye velocity signal (excitatory or inhibitory burst neurons, Henn et al 1982) whereas in the prepositus hypoglossi nucleus, a group of tonic neurons encode a pure position-related signal of the eye (Escudero and Delgado-Garcia 1988;Escudero et al 1992;Pastor et al 1994;Godaux and Cheron 1996). The coding of movement parameters of the premotoneuronal cells recorded in the motor cortex of behaving animals (Fetz et al 1989) and in the red nucleus revealed that they exhibit at least a pure tonic, a phasic-tonic, or a pure phasic discharge pattern during a ramp-and-hold movement (Fetz 1992).…”

Gaze holding deficits discriminate early from late onset cerebellar degeneration

“…Horizontal gaze holding is provided by a brainstem horizontal neural velocity-to-position integrator [4,5] located in the nucleus prepositus hypoglossi and the medial vestibular nucleus [3,6]. Robinson proposed that the neural velocity-to-position integrator is inherently "leaky" and as a result requires cerebellar input to calibrate its output precisely in proportion to eye position [5].…”