Morphology, Intrinsic Membrane Properties, and Rotation-Evoked Responses of Trochlear Motoneurons in the Turtle

Abstract

Jones MS, Ariel M. Morphology, intrinsic membrane properties, and rotation-evoked responses of trochlear motoneurons in the turtle. J Neurophysiol 99: 1187-1200, 2008. First published December 26, 2007 doi:10.1152/jn.01205.2007. Intrinsic properties and rotationevoked responses of trochlear motoneurons were investigated in the turtle using an in vitro preparation consisting of the brain stem with attached temporal bones that retain functional semicircular canals. Motoneurons were divided into two classes based on intrinsic properties. The first class exhibited higher impedance (123.0 Ϯ 11.0 M⍀), wider spikes (0.99 Ϯ 0.05 ms), a single spike afterhyperpolarization (AHP), little or no spike frequency adaptation (SFA), and anomalous rectification, characterized by an initial "sag" in membrane potential in response to hyperpolarizing current injection. The second class exhibited lower impedance (21.8 Ϯ 2.5 M⍀), narrower spikes (0.74 Ϯ 0.03 ms), a double AHP, substantial SFA, and little or no rectification. Vestibular responses were evoked by horizontal sinusoidal rotation (1/12-1/3 Hz; peak velocity: 30 -100°/s). Spiking in higher-impedance cells was recruited earlier in the response and exhibited a more limited dynamic range relative to that of lower impedance cells. Spiking evoked by injecting depolarizing current during rotation was blocked during contraversive motion and was consistent with a shunting inhibition. No morphological features were identified in neurobiotinfilled cells that correlated with the two physiological classes. Recovered motoneurons were multipolar but exhibited a less-complex dendritic morphology than ocular motoneurons of similarly sized mammals. The two physiologically defined cell classes have homologues in other vertebrates, suggesting that intrinsic membrane properties play an important role in oculomotor processing. I N T R O D U C T I O NMotoneurons in the oculomotor, trochlear, and abducens nuclei comprise the common final output pathway for the control of eye movement. A variety of descending and brain stem projections converge on these motoneurons (ButtnerEnnever and Horn 1997), which transform a complex spatiotemporal pattern of synaptic input into a rate-coded spike train that drives the extraocular muscles in a coordinated and precise fashion. These neurons are not only responsible for the generation of voluntary eye movements but also participate in critical brain stem reflexes such as the vestibuloocular reflex (VOR), a compensatory movement of the eyes during motion of the head that acts to stabilize the visual scene on the retina (Wilson and Melvill-Jones 1976).There has been intensive study of oculomotor physiology and the VOR over the last few decades, motivated not only by its clinical relevance but also the utility of the system as a model of neural control (Schwarz 1976;Young 1995). One issue that remains poorly understood is the role of intrinsic membrane properties in shaping motoneuron output. In the spinal cord, the role of intrinsic properties in influencing syna...

Role of the trochlear nerve in eye abduction and frontal vision of the red‐eared slider turtle (Trachemys scripta elegans)

“…Threshold currents, ranging from 5 to 25μA, are also within physiological range used for other studies, and the frequency, 91 Hz (Figs. ), which maximally activates fibers, aligns with those known for neurons that would communicate with trochlear motoneurons (Jones and Ariel, , ).…”

Muscarinic Modulation of Recruitment Threshold and Firing Rate in Rat Oculomotor Nucleus Motoneurons

“…The size principle dictates the order of recruitment, small Mns being recruited before large ones, and the crucial property determining systematic differences in recruitment is the input resistance. In trochlear Mns of the turtle, it has been reported that spiking in Mns of higher input resistance is recruited earlier (Jones and Ariel 2008). In oculomotor nucleus Mns of mammals (Nieto-Gonzalez et al 2007), we have found a poorly fitted linear regression between cell size and input resistance and a weak relationship between input resistance and I-F gain.…”

Topography and Response Timing of Intact Cerebellum Stained With Absorbance Voltage-Sensitive Dye

“…Second, this preparation uses the turtle's adaptive ability to lower its metabolism even further to survive long dives and a dormant state in water under frozen ponds for many winter months. Recordings from a variety of turtle brain stem regions have demonstrated the very low tonic synaptic and spike activity in this in vitro preparation (Fan et al , 1997Jones and Ariel 2008;Rosenberg and Ariel 1990). Responses in mammalian tissue are more active, even in vitro, so have exhibit more depolarized neuronal membranes on which inhibition can often be measured as a hyperpolarization (Cohen and Yarom 2000a).…”