MIF versus SIF Motoneurons, What Are Their Respective Contribution in the Oculomotor Medial Rectus Pool?

Abstract

Multiply-innervated muscle fibers (MIFs) are peculiar to the extraocular muscles as they are non-twitch but produce a slow build up in tension on repetitive stimulation. The motoneurons innervating MIFs establish en grappe terminals along the entire length of the fiber, instead of the typical en plaque terminals that singly-innervated muscle fibers (SIFs) motoneurons establish around the muscle belly. MIF motoneurons have been proposed to participate only in gaze holding and slow eye movements. We aimed to discern the function of MIF motoneurons by recording medial rectus motoneurons of the oculomotor nucleus. Single-unit recordings in awake cats demonstrated that electrophysiologically-identified medial rectus MIF motoneurons participated in different types of eye movements, including fixations, rapid eye movements or saccades, convergences, and the slow and fast phases of the vestibulo-ocular nystagmus, the same as SIF motoneurons did. However, MIF medial rectus motoneurons presented lower firing frequencies, were recruited earlier and showed lower eye position (EP) and eye velocity (EV) sensitivities than SIF motoneurons. MIF medial rectus motoneurons were also smaller, had longer antidromic latencies and a lower synaptic coverage than SIF motoneurons. Peristimulus time histograms (PSTHs) revealed that electrical stimulation to the myotendinous junction, where palisade endings are located, did not recurrently affect the firing probability of medial rectus motoneurons. Therefore, we conclude there is no division of labor between MIF and SIF motoneurons based on the type of eye movement they subserve.

Investigation of Selective Innervation of Extraocular Muscle Compartments

“… 2 , 43 – 45 However, recent studies suggest that all motoneurons fire for all types of eye movement, albeit at different rates for MIF and SIF motoneurons. 46 , 47 A systematic difference in the type and size of the muscle fibers in the EOM regions/compartments could explain the differential contractility. For example, a compartment with considerably more of the fiber type suited for a specific type of eye movement may exhibit more contraction than a compartment with less suited fibers, even if they receive the same innervation during that eye movement.…”

Impaired Extraocular Muscle Innervation Is Present Before Eye Opening in a Mouse Model of Infantile Nystagmus Syndrome

“…Slow and fast myofibers are innervated by different types of motor neurons, which have different function properties. 8 , 10 , 11 , 48 EOMs and OMNs are dependent on each other for trophic support. Muscle-derived cues promote OMN survival, 49 and cell death significantly increases in the absence of normal muscle targets, 19 consistent with the theory that muscles provide trophic support for developing motor neurons.…”

“…It has thus been proposed that SIF and MIF motor neurons control distinct types of eye movements, 8 , 9 but recent recordings from cats indicate that both motor neuron types contribute to all types of eye movements, although with differing physiologic properties, indicating that they may serve different functions. 10 , 11 …”

Saccadic premotor burst neurons and histochemical correlates of their firing patterns in rhesus monkey

“…The former population lacks PN and Kv3.1, and expresses reduced Kv1.1, compared to PNpositive SIF motoneurons with strong Kv1.1 and Kv3.1b expression. It is likely that this reflects the different firing characteristics expressed by these motoneuron populations [6,21,43]. Additionally, expression of CR in itself could be related to excitability [16,40,53].…”

“…The EBNs of the vertical and the IBNs of the horizontal saccadic circuitry exhibited similar HCN1-HCN2-and Cav3.2-3.3-immunoreactivity (Figs. [4][5][6], which indicates they have the capacity for PIR bursting, given that the prerequisite for this phenomenon is provided by the sustained tonic inhibition from OPNs [35,41]. Punctate HCN1-andHCN2-labeling on the BN somatic and dendritic membranes could correspond to the synaptic terminals of glycinergic input from the OPNs, where PIR phenomenon would take place on the post-synaptic membrane of BNs.…”