Macaque Pontine Omnipause Neurons Play No Direct Role in the Generation of Eye Blinks

Abstract

We recorded the activity of pontine omnipause neurons (OPNs) in two macaques during saccadic eye movements and blinks. As previously reported, we found that OPNs fire tonically during fixation and pause about 15 ms before a saccadic eye movement. In contrast, for blinks elicited by air puffs, the OPNs paused Ͻ2 ms before the onset of the blink. Thus the burst in the agonist orbicularis oculi motoneurons (OOMNs) and the pause in the antagonist levator palpabrae superioris motoneurons (LPSMNs) necessarily precede the OPN pause. For spontaneous blinks there was no correlation between blink and pause onsets. In addition, the OPN pause continued for 40 -60 ms after the time of the maximum downward closing of the eyelids, which occurs around the end of the OOMN burst of firing. LPSMN activity is not responsible for terminating the OPN pause because OPN resumption was very rapid, whereas the resumption of LPSMN firing during the reopening phase is gradual. OPN pause onset does not directly control blink onset, nor does pause offset control or encode the transition between the end of the OOMN firing and the resumption of the LPSMNs. The onset of the blink-related eye transients preceded both blink and OPN pause onsets. Therefore they initiated while the saccadic short-lead burst neurons were still fully inhibited by the OPNs and cannot be saccadic in origin. The abrupt dynamic change of the vertical eye transients from an oscillatory behavior to a single time constant exponential drift predicted the resumption of the OPNs.

Anatomical Evidence that the Superior Colliculus Controls Saccades through Central Mesencephalic Reticular Formation Gating of Omnipause Neuron Activity

“…These reticuloraphe neurons fell within the tectoreticular terminal field. They had a much more widespread mediolateral distribution than the medially confined cMRF neurons projecting to the cervical spinal cord Perkins et al, 2009). A small number of WGA-HRP-labeled neurons were also observed in the SC and PAG (Fig.…”

“…This was visualized using the chromagen DAB intensified with cobalt chloride and/or nickel ammonium sulfate (Fisher Scientific) to create a black reaction product. Details of these procedures can be found in Perkins et al (2009). Sections were counterstained with cresyl violet or cytochrome oxidase (WongRiley, 1979), dehydrated, and coverslipped for light microscopic (LM) inspection.…”

“…11), although our analysis was not extensive enough to allow division into the terminal subcategories observed by Büttner-Ennever et al (1999). Neurons in the rostral pole of the SC that display tonic activity during fixation have been described in cats and monkeys Guitton, 1989, 1991;Peck, 1989;Munoz and Wurtz, 1993a,b;Gandhi and Keller, 1999). This rostral SC area differs in several features from the rest of the colliculus; for instance, its tectotectal connections are mutually excitatory (Munoz and Istvan, 1998;Takahashi et al, 2005Takahashi et al, , 2007.…”

Interactions between gaze-evoked blinks and gaze shifts in monkeys

“…While these neurons gate saccadic eye movements by discharging at a tonic rate during fixation and ceasing activity during saccades (Keller 1974; Evinger et al 1982), they also become quiescent during the loopy eye movement induced by a blink (Fuchs et al 1991; Mays and Morrisse 1994; Schultz et al 2010). The reflexive blink is usually induced before the typical reaction time, when the animal is preparing a saccade.…”

Effects of mild to moderate sedation on saccadic eye movements

“…In alert monkeys, omnipause neurons (OPNs) have a high baseline firing rate and briefly stop during saccades [45] and blinks [46]. This cell group, which exerts a powerful inhibitory action on the saccadic burst neurons [47], has glycine as neurotransmitter [48,49] but it receives GABAergic, glycinergic, as well as glutaminergic afferents [48].…”