scholarly journals Dynamics of abducens nucleus neurons in the awake mouse

2012 ◽  
Vol 108 (9) ◽  
pp. 2509-2523 ◽  
Author(s):  
John S. Stahl ◽  
Zachary C. Thumser

The mechanics of the eyeball and orbital tissues (the “ocular motor plant”) are a fundamental determinant of ocular motor signal processing. The mouse is used increasingly in ocular motor physiology, but little is known about its plant mechanics. One way to characterize the mechanics is to determine relationships between extraocular motoneuron firing and eye movement. We recorded abducens nucleus neurons in mice executing compensatory eye movements during 0.1- to 1.6-Hz oscillation in the light. We analyzed firing rates to extract eye position and eye velocity sensitivities, from which we determined time constants of a viscoelastic model of the plant. The majority of abducens neurons were already active with the eye in its central rest position, with only 6% recruited at more abducted positions. Firing rates exhibited largely linear relationships to eye movement, although there was a nonlinearity consisting of increasing modulation in proportion to eye movement as eye amplitudes became small (due to reduced stimulus amplitude or reduced alertness). Eye position and velocity sensitivities changed with stimulus frequency as expected for an ocular motor plant dominated by cascaded viscoelasticities. Transfer function poles lay at approximately 0.1 and 0.9 s. Compared with previously studied animal species, the mouse plant is stiffer than the rabbit but laxer than cat and rhesus. Differences between mouse and rabbit can be explained by scaling for eye size (allometry). Differences between the mouse and cat or rhesus can be explained by differing ocular motor repertoires of animals with and without a fovea or area centralis.

1995 ◽  
Vol 73 (4) ◽  
pp. 1383-1395 ◽  
Author(s):  
J. S. Stahl ◽  
J. I. Simpson

1. We recorded abducens neurons, identified by electrical stimulation as internuclear neurons or motoneurons, in awake rabbits. The relationship of firing rate to eye movement was determined from responses during stable fixations, sinusoidal rotation in the light (0.05-0.8 Hz), and triangular optokinetic stimulation at 0.1 Hz. 2. All abducens neurons were excited during temporal movement of the ipsilateral eye. Temporal and nasal saccades were associated with bursts or pauses, respectively, in the firing rate. 3. Motoneurons and internuclear neurons are qualitatively indistinguishable. There was no significant quantitative difference between the phase and sensitivity of the two groups for 0.2-Hz sinusoidal rotation in the light. 4. On the basis of the response to stable eye positions, we determined static eye position sensitivity of the abducens neuron pool to be 8.2 +/- 2.5 (SD) spikes.s-1/0, with a static hysteresis of 8.9 spikes/s (1.14 +/- 0.37 degrees). 5. We determined apparent eye position sensitivity (k) and apparent eye velocity sensitivity (r) from the responses to sinusoidal rotation in the light. k increases and r decreases with stimulus frequency, which indicates that the simplest transfer function mediating conversion of abducens nucleus (VI) firing rate to eye position (E) has two poles and one zero. 6. The VI-->E relationship has an "amplitude nonlinearity," manifest as a tendency for k, r, and firing rate phase lead to decrease as eye movement amplitude increases at a fixed frequency. On a percentage basis, phase is less affected than are the sensitivities. The nonlinearity becomes less pronounced for stimulus amplitudes > 2.5 degrees, and consequently a linear model of the VI-->E transformation remains useful, provided that consideration is restricted to the appropriate range of stimulus/response amplitudes. 7. We determined time constants of the linear two-pole, one-zero transfer function from the variation of r/k versus stimulus frequency. The pole time constants were T1 = 3.4 s and T2 = 0.28 s, and the zero time constant (Tz) = 1.6 s. The magnitude of Tz was corroborated by measuring the time constant of the exponential decay in firing rate after step changes in eye position. This transient method yielded a Tz of 1.1 s. 8. The time constants of the VI-->E transfer function are roughly 10 times larger than those reported for the rhesus macaque. The difference is attributable to the reported 10-fold lower stiffness of the rabbit oculomotor plant, which may in turn relate to rabbits postulated lower degree of activation of extraocular muscles at any given position.(ABSTRACT TRUNCATED AT 400 WORDS)


1992 ◽  
Vol 68 (1) ◽  
pp. 319-332 ◽  
Author(s):  
J. L. McFarland ◽  
A. F. Fuchs

1. Monkeys were trained to perform a variety of horizontal eye tracking tasks designed to reveal possible eye movement and vestibular sensitivities of neurons in the medulla. To test eye movement sensitivity, we required stationary monkeys to track a small spot that moved horizontally. To test vestibular sensitivity, we rotated the monkeys about a vertical axis and required them to fixate a target rotating with them to suppress the vestibuloocular reflex (VOR). 2. All of the 100 units described in our study were recorded from regions of the medulla that were prominently labeled after injections of horseradish peroxidase into the abducens nucleus. These regions include the nucleus prepositus hypoglossi (NPH), the medial vestibular nucleus (MVN), and their common border (the “marginal zone”). We report here the activities of three different types of neurons recorded in these regions. 3. Two types responded only during eye movements per se. Their firing rates increased with eye position; 86% had ipsilateral “on” directions. Almost three quarters (73%) of these medullary neurons exhibited a burst-tonic discharge pattern that is qualitatively similar to that of abducens motoneurons. There were, however, quantitative differences in that these medullary burst-position neurons were less sensitive to eye position than were abducens motoneurons and often did not pause completely for saccades in the off direction. The burst of medullary burst position neurons preceded the saccade by an average of 7.6 +/- 1.7 (SD) ms and, on average, lasted the duration of the saccade. The number of spikes in the burst was well correlated with saccade size. The second type of eye movement neuron displayed either no discernible burst or an inconsistent one for on-direction saccades and will be referred to as medullary position neurons. Neither the burst-position nor the position neurons responded when the animals suppressed the VOR; hence, they displayed no vestibular sensitivity. 4. The third type of neuron was sensitive to both eye movement and vestibular stimulation. These neurons increased their firing rates during horizontal head rotation and smooth pursuit eye movements in the same direction; most (76%) preferred ipsilateral head and eye movements. Their firing rates were approximately in phase with eye velocity during sinusoidal smooth pursuit and with head velocity during VOR suppression; on average, their eye velocity sensitivity was 50% greater than their vestibular sensitivity. Sixty percent of these eye/head velocity cells were also sensitive to eye position. 5. The NPH/MVN region contains many neurons that could provide an eye position signal to abducens neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1978 ◽  
Vol 41 (3) ◽  
pp. 764-777 ◽  
Author(s):  
S. G. Lisberger ◽  
A. F. Fuchs

1. Extracellular recordings were obtained from 113 mossu fibers (MFs) in the flocculus of alert monkeys trained to perform a visual tracking task during sinusoidal, horizontal head rotation. The analysis of MF discharge patterns was designed to allow quantitative comparison of the discharge properties of flocculus MFs with brain stem cell populations from which the MFs might originate and with flocculus Purkinje cells (P-cells). Based on their firing patterns, MFs were divided into two classes. Vestibular MFs discharged in relation to head velocity and, in some cases, also in relation to eye movement. Eye movement MFs discharged only in relation to one or more components of eye movement. 2. Vestibular MFs were subdivided into three classes. Vestibular-only MFs (n = 15) displayed a modulation in firing rate during head rotation but exhibited no relationship to spontaneous eye movements. Vestibular-plus-saccade MFs (n = 14) displayed a modulation in firing rate during head rotation that quantitatively resembled the modulation in vestibular-only MFs. In addition, a pause in firing rate interrupted the vestibular modulation during saccades in one or more directions. Vestibular-plus-position MFs (n = 4) exhibited steady firing rates that were linearly related to horizontal eye position in the absence of vestibular stimulation. Sinusoidal head rotation evoked a modulation ofiring rate above and below the firing rate set by the eye position. 3. during sinusoidal head rotation, vestibular MF firing rate led head velocity by an average of 24 degrees. The amplitude of MF firing-rate modulation increased as a function of the frequency of head rotation and, hence, maximum head velocity. Since these characteristics are similar to those displayed by P-cells during suppression of the VOR, vestibular MFs probably transmit the head velocity component of P-cell firing rate to the flocculus. Based on evidence from other mammals and a quantitative comparison of population discharge characteristics, it is likely that vestibular MFs originate from the vestibular nerve and from cells in the medial vestibular nucleus. 4. Based on their discharge patterns, eye movement MFs were also subdivided into three classes. Burst MFs (n = 14) emitted a high-frequency burst of spikes prior to and during saccades in one or more direction, but were silent during steady fixation. Burst-tonic MFs (n = 53) emitted a burst of spikes prior to saccades in a preferred ("on") direction, ceased firing during saccades in the opposite ("off") direction, and exhibited steady firing rates that increased as steady gaze shifted in the on direction. Tonic MFs (n = 13) displayed steady firing rates that increased as the position of steady gaze shifted in the on direction, and either paused or exhibited step changes in firing rate during saccades. 5. During steady fixation, 64% of tonic and burst-tonic MFs were recruited into maintained firing within +/- 10 degrees of the primary direction of gaze...


1995 ◽  
Vol 73 (4) ◽  
pp. 1396-1413 ◽  
Author(s):  
J. S. Stahl ◽  
J. I. Simpson

1. We recorded single vestibular nucleus neurons shown by electrical stimulation to receive floccular inhibition [flocculus receiving neurons (FRNs)] and/or to project toward midbrain motoneuronal pools [midbrain projecting neurons (MPNs)] in awake, head-fixed rabbits during compensatory eye movements. Stimuli included head rotation in the light, head rotation in the dark, and rotation of an optokinetic drum about the animal. We employed sinusoidal and triangular position profiles in the 0.05- to 0.8-Hz frequency band. We also examined transient responses to step changes in eye position. 2. We found identified vestibular nucleus cells (i.e., FRN/non-MPNs, FRN/MPNs, and non-FRN/MPNs) in the parvocellular and magnocellular portions of the medial vestibular nucleus, at the rostrocaudal level of the dorsal acoustic stria. 3. All identified vestibular nucleus neurons were excited during ipsilateral (relative to side of recording) head rotation and contralateral eye rotation. 4. The neuronal firing rates could be related to eye position and its time derivatives, and that relationship could be approximated by a two-pole, one-zero linear transfer function. As with abducens neurons, a more detailed approximation requires inclusion of two nonlinearities-a hysteresis and a variable sensitivity term that increases as eye movement amplitude decreases. 5. When the vestibuloocular reflex is suppressed by a conflicting full-field visual stimulus [visual vestibular conflict condition (VVC)], vestibular nucleus neuron modulation is largely suppressed. The remaining modulation is motoric in nature, because it can be related to the residual eye movements. Cells with "sensory vestibular signals," i.e., cells whose modulation during VVC correlates better with head rotation than eye movement, were not encountered. 6. We examined the dependence of firing rate parameters on stimulus modality. All neurons exhibited increased phase lead with respect to abducens nucleus neurons during stimuli involving head rotation. This finding could indicate that vestibular-derived inputs are inhomogeneously distributed on premotor neurons and that the studied premotor population receives a stronger vestibular input than another premotor group, not recorded in the current experiments. 7. FRNs and non-FRNs were similar in their qualitative response to the fast phases, the applicability of the two-pole, one-zero transfer function, hysteresis, and the amplitude nonlinearity. 8. FRNs differed from non-FRNs in having a phase advanced firing rate at all stimulus frequencies during visual and vestibular stimuli. The phase difference suggests that one role of the rabbit flocculus is to regulate phase of the net premotor signal.


1993 ◽  
Vol 69 (2) ◽  
pp. 642-645 ◽  
Author(s):  
Y. Zhang ◽  
A. M. Partsalis ◽  
S. M. Highstein

1. Properties of superior vestibular nucleus (SVN) neurons and their projection to the cerebellar flocculus were studied in alert squirrel monkeys by using chronic unit and eye movement recording and microstimulation techniques. Twenty-three cells were antidromically activated from the ipsilateral flocculus, and seventeen of these were also orthodromically activated from the ipsilateral VIIth nerve at monosynaptic latencies. Only 1 of these 23 units was also inhibited by flocculus stimulation. According to their response properties, 9 of the cells were pure vestibular, 2 were vestibular-pause, and 12 were position-vestibular cells. The mean eye position sensitivity of these position-vestibular cells was significantly lower than that of cells projecting to the oculomotor nucleus (OMN). No eye movement-only neurons were antidromically activated from the flocculus. No cells could be antidromically activated from both the oculomotor nucleus and the flocculus.


1999 ◽  
Vol 82 (5) ◽  
pp. 2612-2632 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Kathleen E. Cullen

The mechanics of the eyeball and its surrounding tissues, which together form the oculomotor plant, have been shown to be the same for smooth pursuit and saccadic eye movements. Hence it was postulated that similar signals would be carried by motoneurons during slow and rapid eye movements. In the present study, we directly addressed this proposal by determining which eye movement–based models best describe the discharge dynamics of primate abducens neurons during a variety of eye movement behaviors. We first characterized abducens neuron spike trains, as has been classically done, during fixation and sinusoidal smooth pursuit. We then systematically analyzed the discharge dynamics of abducens neurons during and following saccades, during step-ramp pursuit and during high velocity slow-phase vestibular nystagmus. We found that the commonly utilized first-order description of abducens neuron firing rates (FR = b + kE + rE˙, where FR is firing rate, E and E˙ are eye position and velocity, respectively, and b, k, and r are constants) provided an adequate model of neuronal activity during saccades, smooth pursuit, and slow phase vestibular nystagmus. However, the use of a second-order model, which included an exponentially decaying term or “slide” (FR = b + kE + rE˙ + uË − c[Formula: see text]), notably improved our ability to describe neuronal activity when the eye was moving and also enabled us to model abducens neuron discharges during the postsaccadic interval. We also found that, for a given model, a single set of parameters could not be used to describe neuronal firing rates during both slow and rapid eye movements. Specifically, the eye velocity and position coefficients ( r and k in the above models, respectively) consistently decreased as a function of the mean (and peak) eye velocity that was generated. In contrast, the bias ( b, firing rate when looking straight ahead) invariably increased with eye velocity. Although these trends are likely to reflect, in part, nonlinearities that are intrinsic to the extraocular muscles, we propose that these results can also be explained by considering the time-varying resistance to movement that is generated by the antagonist muscle. We conclude that to create realistic and meaningful models of the neural control of horizontal eye movements, it is essential to consider the activation of the antagonist, as well as agonist motoneuron pools.


1998 ◽  
Vol 79 (3) ◽  
pp. 1461-1480 ◽  
Author(s):  
Markus Lappe ◽  
Martin Pekel ◽  
Klaus-Peter Hoffmann

Lappe, Markus, Martin Pekel, and Klaus-Peter Hoffmann. Optokinetic eye movements elicited by radial optic flow in the macaque monkey. J. Neurophysiol. 79: 1461–1480, 1998. We recorded spontaneous eye movements elicited by radial optic flow in three macaque monkeys using the scleral search coil technique. Computer-generated stimuli simulated forward or backward motion of the monkey with respect to a number of small illuminated dots arranged on a virtual ground plane. We wanted to see whether optokinetic eye movements are induced by radial optic flow stimuli that simulate self-movement, quantify their parameters, and consider their effects on the processing of optic flow. A regular pattern of interchanging fast and slow eye movements with a frequency of 2 Hz was observed. When we shifted the horizontal position of the focus of expansion (FOE) during simulated forward motion (expansional optic flow), median horizontal eye position also shifted in the same direction but only by a smaller amount; for simulated backward motion (contractional optic flow), median eye position shifted in the opposite direction. We relate this to a change in Schlagfeld typically observed in optokinetic nystagmus. Direction and speed of slow phase eye movements were compared with the local flow field motion in gaze direction (the foveal flow). Eye movement direction matched well the foveal motion. Small systematic deviations could be attributed to an integration of the global motion pattern. Eye speed on average did not match foveal stimulus speed, as the median gain was only ∼0.5–0.6. The gain was always lower for expanding than for contracting stimuli. We analyzed the time course of the eye movement immediately after each saccade. We found remarkable differences in the initial development of gain and directional following for expansion and contraction. For expansion, directional following and gain were initially poor and strongly influenced by the ongoing eye movement before the saccade. This was not the case for contraction. These differences also can be linked to properties of the optokinetic system. We conclude that optokinetic eye movements can be elicited by radial optic flow fields simulating self-motion. These eye movements are linked to the parafoveal flow field, i.e., the motion in the direction of gaze. In the retinal projection of the optic flow, such eye movements superimpose retinal slip. This results in complex retinal motion patterns, especially because the gain of the eye movement is small and variable. This observation has special relevance for mechanisms that determine self-motion from retinal flow fields. It is necessary to consider the influence of eye movements in optic flow analysis, but our results suggest that direction and speed of an eye movement should be treated differently.


1996 ◽  
Vol 18 (2-3) ◽  
pp. 201
Author(s):  
I. Gerdsen ◽  
J. Pinkert ◽  
R. Fötzsch ◽  
L. Oehme ◽  
O. Bach ◽  
...  

Author(s):  
Christopher Kennard

This chapter discusses motor disorders of the eye. The first part of the chapter describes the proper examination of eye movements to facilitate identification of ocular motor disorder pathology. The effects of nerve palsies on ocular motor function are then described.Eye movement disorders can also have their cause in the central nervous system; both the brainstem, and cerebellum have been implicated as causal factors in some eye movement disorders. Disorders of the pupil, which affect the pupillary light reflex, can be caused by lesions to central, afferent and efferent pupillary pathways as well as sympathetic pathways lesions.Finally, this chapter describes diseases of the eye orbits, including dysthyroid eye disease, idiopathic orbital inflammation, orbital tumours, vascular disorders and orbital infections.


1988 ◽  
Vol 60 (6) ◽  
pp. 1874-1895 ◽  
Author(s):  
A. F. Fuchs ◽  
C. A. Scudder ◽  
C. R. Kaneko

1. Single neurons in the abducens nucleus were recorded extracellularly in alert rhesus macaques trained to make a variety of eye movements. An abducens neurons was identified as a motoneuron (MN) if its action potentials triggered an averaged EMG potential in the lateral rectus muscle. Abducens internuclear neurons (INNs) that project to the oculomotor nucleus were identified by collision block of spontaneous with antidromic action potentials evoked with a stimulating electrode placed in the medial rectus subdivision of the contralateral oculomotor nucleus. 2. All abducens MNs and INNs had qualitatively similar discharge patterns consisting of a burst of spikes for lateral saccades and a steady firing whose rate increased with lateral eye position in excess of a certain threshold. 3. For both MNs and INNs the firing rates associated with different, constant eye positions could be described accurately by a straight line with slope, K (the eye position sensitivity in spikes.s-1.deg-1), and intercept, T (the eye position threshold for steady firing). For different MNs, K increased as T varied from more medial to more lateral values. In contrast, the majority of INNs already were active for values of T more medial than 20 degrees and showed little evidence of recruitment according to K. 4. During horizontal sinusoidal smooth-pursuit eye movements, both MNs and INNs exhibited a sinusoidal modulation in firing rate whose peak preceded eye position. From these firing rate patterns, the component of firing rate related to eye velocity, R (the eye velocity sensitivity in spikes.s-1.deg-1.s-1), was determined. The R for INNs was, on average, 78% larger than that for MNs. Furthermore, R increased with T for MNs, whereas INNs showed no evidence of recruitment according to R. If, as in the cat, the INNs of monkeys provide the major input to medial rectus MNs and if simian medial rectus MNs behave like our abducens MNs, then recruitment order, which is absent in INNs, must be established at the MN pool itself. 5. Unexpectedly, the R of MNs decreased with the frequency of the smooth-pursuit movement. Furthermore, the eye position sensitivity, K, obtained during steady fixations was usually less than that determined during smooth pursuit. Therefore, conclusions about the roles of MNs and premotor neurons based on how their R and K values differ must be viewed with caution if the data have been obtained under different tracking conditions.(ABSTRACT TRUNCATED AT 400 WORDS)


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