Neurophysiology of the motoneurons of the external oculomotor nucleus in the waking cat

The spontaneous and visually induced activity of abducens motoneurons has been recorded in the alert cat. Motoneurons were identified by their antidromic activation from the ipsilateral abducens nerve. All identified motoneurons appeared related to both the position and velocity of the eye in the horizontal plane, although distributed in a wide range. Neural time constants were also measured, showing a mean value similar to that of the mechanical time constant of the oculomotor plant. According to present results, abducens motoneurons of cats and monkeys are very similar, notwithstanding some differences in their activities during saccadic movements.     

Frequency characteristics of the saccadic eye movement

Using a piecewise linear approach, individual saccadic eye movements have been Fourier decomposed in an attempt to determine the effect of saccadic amplitude on frequency characteristics. These characteristics were plotted in the traditional Bode plot form, showing gain and phase as a function of frequency for various eye movement amplitudes. Up to about one octave beyond the -3 db gain frequency, the limiting system dynamics represented by the saccadic trajectory of a given amplitude may be considered linear and second order. The -3 db gain frequency was used as a measure of bandwidth, and the -90 degrees phase crossover frequency was used as a measure of undamped natural frequency. These two quantities were used to calculate the damping factor. Both bandwidth and undamped natural frequency decrease with increasing saccadic eye movement amplitude. The damping factor shows no trend with amplitude and indicates approximate critical damping. When compared with the normal variation of characteristics for a given movement, the frequency characteristics of fixed-amplitude saccades showed no generalized trends with changes in direction or DC operating level of movement.     

Models of the saccadic eye movement control system

1. A sequence of four models is proposed for the saccadic eye movement control system. The models become increasingly complex as they are made to respond to increasingly more complicated target movements in accordance with experimental results. Compatibility with neurological structure and function is stressed in the formation of the models. In each case, the elements of the models are constructed to conform as closely as possible to neuroanatomical structures and behave in a way that has been established or suggested by neurophysiology.
2. The dynamic behavior of the mechanics of the extraocular muscles and eyeball suspensory tissues has been established by recording from oculomotoneurons in alert monkeys. The transfer function of this mechanical system is used in these models.
3. Recent experiments on the neural circuits in the brain stem that are responsible for saccadic eye movements suggest an arrangement of the premotor circuitry that contains two principal neural networks; an integrator and a pulse generator. This circuitry is used in the models.
4. When the above modifications are made to existing models of the saccadic system, they remove the necessity of supposing that the visual information is sampled by the nervous system. The models do not include a sampler although the saccadic pulse generator still makes the overall system behavior similar to that of a sampled-data system.
5. The basic model is modified to make its behavior agree with experimental eye movement responses to target ramps and step-ramps. This is done by using error and its rate of change to estimate the error that will exist one reaction time in the future.
6. Parallel processing of data is a well recognized property of the nervous system. By utilizing it in combination with a random decision threshold, the model is extended to produce results in agreement with experiments for double-step target movements in which the second step occurs less than 0.2 sec after the first.
7. Finally, a model is presented which incorporates a continuum of parallel processing to represent the retinotopic spatial organization of the visual system and the tecto-bulbar motor commands. The model is conceptual; it was not constructed or tested but is used to discuss more complex eye movement phenomena such as those that appear to occur when the decision process must shift between hemispheres and how the system might produce quick correcting saccades with latencies as short as 85 msec.

     

Effects of axotomy on the activity of the motor neurons of the external ocular motor nucleus during saccadic movements

The instantaneous firing frequency of cat abducens nucleus motoneurons (Mns) during spontaneous saccadic eye movements has been analyzed. Recordings were carried out from both control and axotomized Mns. Firing frequency of control Mns increased gradually during the first four to five interspike intervals, at which point maximum firing frequency was reached. Axotomized Mns showed an increase in firing frequency only up to the second or third interval, decreasing rapidly then. Linear relationships, with high correlation coefficients, were established between the first five intervals versus maximum frequency or peak eye velocity during saccades, in both control and axotomized Mns. However, the latter showed a decrease in the linear correlation from the third interval because of the decrease in the slope of the relationship. Functional implications of these results are discussed according to the present hypothesis on the effects of axotomy upon oculomotor neurons.     

The oculomotor system--simulation of physiologic and pathologic horizontal saccadic eye movements

Horizontal saccadic eye movements were analyzed by way of the input- and output-functions of the oculomotor system. On the basis of the parameters of the model, it was possible to simulate both physiological and pathological saccades. In this paper we present the results of simulation experiments that were performed to study the influence of various ocular motor disorders. The parameters of the model proved a useful diagnostic aid.     

Stability of the saccadic oculomotor system

A variety of different types of instability has been found in the saccadic system of humans. Some of the instabilities correspond to clinical conditions, whereas others are inherent in the normal saccadic system. How can these instabilities arise within the mechanism of normal saccadic eye movements? A physiologically-based model of the saccadic system predicts that horizontal saccadic oscillations will occur with excessive mutual inhibition between the left and right burst cells and with underaction of the pause cells. The amplitudes and frequencies of the oscillations had ranges of 0–6° and 6–20 cycles per second, respectively. Application of stability analysis techniques to the model reveals that development of the oscillations can be explained by the Hopf bifurcation mechanism. Future development of this approach will involve classifying pathological instabilities of the saccadic system according to the bifurcation involved in their generation.     

Neuronal response to sensory stimulation in the cat caudate nucleus

Neuronal response in the caudate nucleus to presentation of a wide variety of visual and other sensory stimuli was investigated in waking cats. Pronounced discrepancies in background activity of unknown origin as well as differing neuronal activity level were noted in adjacent sections of the nucleus. Of the neurons from which readings of response to sensory stimulation could be made, some reacted to presentation of exclusively visual and others to tactile stimuli; a third group responded to a combination of visual and somatic stimulation only. Response could only be produced in cells of all types by a high level of activity in the animal. Visual stimuli attracting the animal's interest proved to be the most effective form of stimulation. Ipsi- and contralateral sides of the animal's body were both represented in the caudate nucleus of each hemisphere. Neuronal response in the caudate nucleus may be compared with that produced by application of similar stimuli in cells belonging to different cortical areas.Institute for Research on Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 22, No. 1, pp. 3–10, January–February, 1990.     

Unit activity of neurons of the posterior ventral nucleus of the thalamus for various waking stages in the normal cat

Using the electrocortical activity in the sensorimotor cortex as an index, three distinct levels of motionless waking can be identified in the cat, all three different from active waking and from slow sleep (attentive waking, quiet waking and drowsiness). It has now been shown that spontaneous and evoked single unit activities in n. ventralis posterior of the thalamus undergo significant changes when passing from one level of waking into another one.     

Vision as oculomotor reward: cognitive contributions to the dynamic control of saccadic eye movements

Humans and other primates are equipped with a foveated visual system. As a consequence, we reorient our fovea to objects and targets in the visual field that are conspicuous or that we consider relevant or worth looking at. These reorientations are achieved by means of saccadic eye movements. Where we saccade to depends on various low-level factors such as a targets’ luminance but also crucially on high-level factors like the expected reward or a targets’ relevance for perception and subsequent behavior. Here, we review recent findings how the control of saccadic eye movements is influenced by higher-level cognitive processes. We first describe the pathways by which cognitive contributions can influence the neural oculomotor circuit. Second, we summarize what saccade parameters reveal about cognitive mechanisms, particularly saccade latencies, saccade kinematics and changes in saccade gain. Finally, we review findings on what renders a saccade target valuable, as reflected in oculomotor behavior. We emphasize that foveal vision of the target after the saccade can constitute an internal reward for the visual system and that this is reflected in oculomotor dynamics that serve to quickly and accurately provide detailed foveal vision of relevant targets in the visual field.     

Investigation of saccadic eye movement effects on the fluid dynamic in the anterior chamber

The aqueous humor (AH) flow in the anterior chamber (AC) due to saccadic movements is investigated in this research. The continuity, Navier-Stokes and energy equations in 3D and unsteady forms are solved numerically and the saccadic motion was modeled by the dynamic mesh technique. Firstly, the numerical model was validated for the saccadic movement of a spherical cavity with analytic solutions and experimental data where excellent agreement was observed. Then, two types of periodic and realistic saccadic motions of the AC are simulated, whereby the flow field is computed for various saccade amplitudes and the results are reported for different times. The results show that the acting shear stress on the corneal endothelial cells from AH due to saccadic movements is much higher than that due to normal AH flow by buoyancy induced due to temperature gradient. This shear stress is higher on the central region of the cornea. The results also depict that eye saccade imposes a 3D complicated flow field in the AC consist of various vortex structures. Finally, the enchantment of heat transfer in the AC by AH mixing as a result of saccadic motion is investigated.     

Neuronal activity in the nucleus basalis magnocellularis during performance of an instrumental task

Spike activity of 95 neurons in the rabbit basal forebrain forebrain magnocellular nucleus was recorded during spontaneous behavior and instrumental conditioned performance. Almost half of the neurons (48.4%) displayed a significant (p > 0.05) negative correlation between their spontaneous discharge rate and the power of the delta rhythm in the EEG of the frontal cortex; most of these cells can be classified as projection cholinergic neurons. During instrumental conditioned performance, neurons of this subgroup responded with excitation to the conditioned stimulus, whereas presumably noncholinergic nonprojection neurons responded to the conditioned stimulus with inhibition. Excitatory response of cells in the basal forebrain magnocellular nucleus was significantly more intense as compared to trials without the conditioned reaction. On the whole, our data testify that the basal forebrain magnocellular nucleus maintains the level of arousal and attention required for the instrumental conditioned performance.     

Neuronal plasticity in thalamocortical networks during sleep and waking oscillations

Spontaneous brain oscillations during states of vigilance are associated with neuronal plasticity due to rhythmic spike bursts and spike trains fired by thalamic and neocortical neurons during low-frequency rhythms that characterize slow-wave sleep and fast rhythms occurring during waking and REM sleep. Intracellular recordings from thalamic and related cortical neurons in vivo demonstrate that, during natural slow-wave sleep oscillations or their experimental models, both thalamic and cortical neurons progressively enhance their responsiveness. This potentiation lasts for several minutes after the end of oscillatory periods. Cortical neurons display self-sustained activity, similar to responses evoked during previous epochs of stimulation, despite the fact that thalamic neurons remain under a powerful hyperpolarizing pressure. These data suggest that, far from being a quiescent state during which the cortex and subcortical structures are globally inhibited, slow-wave sleep may consolidate memory traces acquired during wakefulness in corticothalamic networks. Similar phenomena occur as a consequence of fast oscillations during brain-activated states.     

Neuronal firing activity in the lateral vestibular nucleus during locomotion in the guinea pig

The effects of spontaneous locomotor activity on neuronal background firing in the lateral vestibular nucleus was investigated during experiments on decerebrate guinea pigs. The onset of rhythmic muscular activity in the extramities was found to produce a rise in the rate of such discharges, which increased from 10–15 to 100 spikes/sec in most neurons. A higher rate occurred as activity began in the ipsilateral forelimb extensor muscles (the stage corresponding to the end of the swing phase and start of the stance phase in the locomotor cycle). The alterations noted in vestibular neuronal activity during locomotion are thought to ensure the background of high anti-graveity muscle tonus against which rhythmic limb movements take place.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 23, No. 5, pp. 536–541, September–October, 1991.     

Neuronal activity of the pulvinar of the thalamus in the cat

Spontaneous and induced activity in the neurons in the pulvinar of the thalamus (PT) was studied extracellularly in unnarcotized cats immobilized with Remiolan. The PT neurons had a relatively low level of spontaneous activity, and either responded only to light flashes (61%) or did not respond to any of the stimuli applied. The latent periods of the responses varied within wide limits (from 15 to 60 msec), which indicates the possibility of direct peripheral activation of the PT neurons and also of the existence of multisynaptic afferent connections. Acoustic and electrical cutaneous stimuli, although they did not themselves evoke response-discharges, modulated both spontaneous activity and activity evoked by light flashes in the PT neurons. The same effect on the activity of the PT neurons was produced by electrical excitation of the mesencephalic reticular formation. That gives us grounds for surmising that the modulating effects of acoustic and electrical stimuli are produced through activation of reticular structures in the midbrain.Institute of Physiology, Academy of Sciences of the Georgian SSR, Tbilisi. Translated from Neirofiziologiya, Vol. 3, No. 5, pp. 491–499, September–October, 1971.     

Unit responses of the somatosensory cortex of the waking cat to stimulation of the ventro-posterolateral thalamic nucleus

Unit responses in the primary somatosensory projection cortex to stimulation of the ventro-posterolateral thalamic nucleus were investigated by extra- and intracellular recording in chronic experiments on cats. Short-latency spike responses of 71.3% of recorded neurons appeared after not more than 4 msec. It is concluded that activation of neurons in this area of the cortex is chiefly monosynaptic and disynaptic. Besides participating in the initial response to the stimulus, one-quarter of the neurons generated after-discharges 120–314 msec later. These after-discharges are based on rebound after IPSPs and additional synaptic activation. Initial inhibition may appear 1.5 msec after stimulation of the ventro-posterolateral nucleus, evidence against the participation of recurrent collaterals in the formation of these IPSPs.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 5, No. 4, pp. 348–354, July–August, 1973.     

Electrical stimulation of the primate lateral habenula suppresses saccadic eye movement through a learning mechanism

The lateral habenula (LHb) is a brain structure which represents negative motivational value. Neurons in the LHb are excited by unpleasant events such as reward omission and aversive stimuli, and transmit these signals to midbrain dopamine neurons which are involved in learning and motivation. However, it remains unclear whether these phasic changes in LHb neuronal activity actually influence animal behavior. To answer this question, we artificially activated the LHb by electrical stimulation while monkeys were performing a visually guided saccade task. In one block of trials, saccades to one fixed direction (e.g., right direction) were followed by electrical stimulation of the LHb while saccades to the other direction (e.g., left direction) were not. The direction-stimulation contingency was reversed in the next block. We found that the post-saccadic stimulation of the LHb increased the latencies of saccades in subsequent trials. Notably, the increase of the latency occurred gradually as the saccade was repeatedly followed by the stimulation, suggesting that the effect of the post-saccadic stimulation was accumulated across trials. LHb stimulation starting before saccades, on the other hand, had no effect on saccade latency. Together with previous studies showing LHb activation by reward omission and aversive stimuli, the present stimulation experiment suggests that LHb activity contributes to learning to suppress actions which lead to unpleasant events.