Discharge properties of brain stem neurons projecting to the flocculus in the alert cat. II. Prepositus hypoglossal nucleus

Abstract

1. The aim of this study was to characterize the signals transmitted by the neurons of the nucleus prepositus hypoglossal (NPH) to the middle zone of the flocculus of the cat. The methods, the behavioral testing, and the animals used in this study were the same as those used in the accompanying paper on medial vestibular nucleus neurons. 2. The rostral two-thirds of the NPH was explored in alert animals with microelectrodes during stimulation of the middle zone of both flocculi. Discharges of neurons were analyzed during spontaneous eye movements (head fixed) and during horizontal vestibuloocular reflex (VOR) activity elicited by sinusoidal stimulation (10, 20, 30, or 40 degrees at 0.1 Hz). Forty neurons were found to be antidromically activated from only one or the other of the two flocculi (latency: 0.99 +/- 0.17 ms, mean +/- SD): 37 from the contralateral flocculus and 3 from the ipsilateral one. None of the neurons could be activated antidromically from both flocculi. Floccular stimulation never resulted in direct inhibition of these NPH neurons. 3. Of the 37 units antidromically activated from the contralateral flocculus, 26 were recorded sufficiently long to allow full quantitative analysis. Most of these (20 neurons) were classified as burst-tonic (BT) neurons. The BT neurons exhibited during each saccade made in one direction (the ON direction) a burst of spikes, and during postsaccadic fixation a tonic activity that increased with gaze displacement in the ON direction. The mean sensitivity of the neurons to eye velocity during the "ON" saccades was 3.3 +/- 1.6 spikes.s-1.deg-1.s-1. During intersaccadic fixation, the mean sensitivity to eye position was 3.6 +/- 2.5 spikes.s-1.deg-1. During the VOR, the majority showed modulation in relation to both eye position and eye velocity. The mean sensitivity to eye position during the VOR was 3.4 +/- 2.6 spikes.s-1.deg-1 (range: 0.2-8.1 spikes.s-1.deg-1). The mean sensitivity to eye velocity during the VOR was 2.1 +/- 1.3 spikes.s-1.deg-1.s-1. The mean phase lead of with respect to eye position was 16.4 +/- 6.8 degrees (range: 6.0-28.9 degrees). Eighty percent of the BT neurons behaved as type I neurons. Forty-seven percent of the BT neurons also presented some head velocity sensitivity (1.48 +/- 0.6 spikes.s-1.deg-1.s-1, mean +/- SD). 4. Other NPH cells antidromically activated from the contralateral flocculus were classified in two groups: bidirectional burst (BB) neurons (n = 4) and burst-driving (BD) neurons (n = 2). The BB neurons were characterized by a burst discharge during every horizontal saccade or VOR quick phase, irrespective of the direction. The mean sensitivity of the BB neurons to eye velocity during saccades was 3.3 +/- 7.8 (SD) spikes.s-1.deg-1.s-1. Both BD neurons increased their firing rate during the slow VOR phases induced by an ipsilateral rotation (type I neurons) and exhibited high-frequency bursts in association with ipsilaterally directed quick phases. 5. The results indicate that the main projection of the NPH onto the middle zone of t...

A Reevaluation of the Inverse Dynamic Model for Eye Movements

“…Despite a continuing prevalence of models like those in Figure 1 that emphasize the concept of a neural coding of eye position, numerous studies have shown that a consistent internal estimate of E* might not be coded explicitly by any premotor cell type (Baker and Berthoz, 1975;Lopez-Barneo et al, 1982;DelgadoGarcia et al, 1989;Escudero et al, 1992Escudero et al, , 1996McFarland and Fuchs, 1992;Scudder and Fuchs, 1992;Cullen et al, 1993;Sylvestre et al, 2003). This inconsistency between neurophysiological findings and the predictions of conceptual models (Fig.…”

“…Desired eye velocity was proposed to be combined with a neurally computed eye position signal to construct a simplified (firstorder) inverse dynamic representation of the eye plant (Skavenski and Robinson, 1973;Robinson, 1981). This theoretical construct was solidified by demonstrating that burst-tonic/tonic neuron responses in the prepositus hypoglossi (PH) and adjacent medial vestibular nuclei (VN) (collectively referred to here as PH-BT) correlate closely with eye position during static fixation and low-frequency slow eye movements (Baker and Berthoz, 1975;Lopez-Barneo et al, 1982;Escudero et al, 1992Escudero et al, , 1996McFarland and Fuchs, 1992). Consequently, PH-BT neurons were thought to encode the eye position component of the inverse dynamic model.…”

Maturation of canal‐related brainstem neurons in the detection of horizontal angular acceleration in rats

“…PrH is also critical for neural integration of optokinetic, pursuit, and vestibular-induced eye movements on the horizontal plane (Escudero et al, 1996;Arnold et al, 1999;Kaneko, 1999). At P14, when eye-opening occurs in rats, canal-related Fos-ir PrH neurons exhibited a dramatic increase in number that remained stable until adulthood.…”

Biological Signals Identification by a Dynamic Recurrent Neural Network: from Oculomotor Neural Integrator to Complex Human Movements and Locomotion

“…units presenting eye position sensitivity) (Draye et al, 1997a), an interesting analogy between the artificial DRNN integrator and the electrophysiological recordings can be made. For example, clusters of position neurons have been found in the neural integrator of the cat (Delgado-Garcia et al, 1989;Escudero et al, 1992Escudero et al, , 1996. We can thus conclude that emergence of clusters in a DRNN performing a well-defined mathematical task (here a temporal integration) is due to computational constraints with a restricted space of solutions.…”