A model of the smooth pursuit eye movement system

Human, horizontal, smooth-pursuit eye movements were recorded by the search coil method in response to Rashbass step-ramp stimuli of 5 to 30 deg/s. Eye velocity records were analyzed by measuring features such as the time, velocity and acceleration of the point of peak acceleration, the time and velocity of the peaks and troughs of ringing and steady-state velocity. These values were averaged and mean responses reconstructed. Three normal subjects were studied and their responses averaged. All showed a peak acceleration-velocity saturation. All had ringing frequencies near 3.8 Hz and the mean steady-state gain was 0.95.It is argued that a single, linear forward path with any transfer function G(s) and a 100 ms delay (latency) cannot simultaneously simulate the initial rise of acceleration and ring at 3.8 Hz based on a Bode analysis. Also such a simple negative feedback model cannot have a steady-state gain greater than 1.0; a situation that occurs frequently experimentally. L.R. Young's model, which employs internal positive feedback to eliminate the built-in unity negative feedback, was felt necessary to resolve this problem and a modification of that model is proposed which simulates the data base. Acceleration saturation is achieved by borrowing the idea of the local feedback model for saccades so that one nonlinearity can account for the acceleration-velocity saturation: the main sequence for pursuit. Motor plasticity or motor learning, recently demonstrated for pursuit, is also incorporated and simulated.It was noticed that the offset of pursuit did not show the ringing seen in the onset so this was quantified in one subject. Offset velocity could be characterized by a single exponential with a time constant of about 90 ms. This observation suggests that fixation is not pursuit at zero velocity and that the pursuit system is turned on when needed and off during fixation.     

New methods for removing saccades in analysis of smooth pursuit eye movement

New computation methods for removing saccades in analysis of smooth pursuit eye movement characteristics were developed. They have removed saccades more completely than previous methods, and were very effective especially for noisy data recorded by the EOG method. The fully developed method was applicable to eye movement data in tracking of pseudo-random target movement as well as deterministic target movement. Furthermore, the methods were also useful for extracting the number and magnitudes of saccades more precisely.     

A step towards non-invasive characterization of the human frontal eye fields of individual subjects

Background

Identifying eye movement related areas in the frontal lobe has a long history, with microstimulation in monkeys producing the most clear-cut results. For humans, however, there is still no consensus about the location and the extent of the frontal eye field (FEF). There is also no simple non-invasive method for unambiguously defining the FEF in individual subjects, a prerequisite for clinical applications. Here we explore the use of magnetoencephalography (MEG) for the non-invasive identification and characterization of FEF activity in an individual subject.

Methods

We mapped human brain activity before, during and after saccades by applying tomographic analysis to MEG data. Statistical parametric maps and circular statistics produced plausible FEF loci, but no unambiguous definition for individual subjects. Here we first computed the spectral decomposition and correlation with electrooculogram (EOG) of the tomographic brain activations. For each of these two measures statistical comparisons were made between different saccades.

Results

In this paper, we first review the frontal cortex activations identified in earlier animal and human studies and place the putative human FEFs in a well-defined anatomical framework. This framework is then used as reference for describing the results of new Fourier analysis of the tomographic solutions comparing active saccade tasks and their controls. The most consistent change in the dorsal frontal cortex was at the putative left FEF, for both saccades to the left and right. The asymmetric result is consistent with the 1-way callosal traffic theory. We also showed that the new correlation analysis had its most consistent change in the contralateral putative FEF. This result was obtained for EOG latencies before saccade onset with delays of a few hundreds of milliseconds (FEF activity leading the EOG) and only for visual cues signaling the execution of a saccade in a previously defined saccade direction.

Conclusions

The FEF definition derived from microstimulation describes only one of the areas in the dorsal lateral frontal lobe that act together to plan, prepare and execute a saccade. The definition and characterization of these areas in an individual subject can be obtained from non-invasive MEG measurements.

     

Phencyclidine produces aggressive behavior in rapid eye movement sleep-deprived rats

This study examined effects of acute doses of phencyclidine (PCP; 0.025, 0.05, 0.10, and 0.20 mg/kg intraperitoneally) on intra-specific aggressive behavior and muricide in normal rats and rats deprived of rapid eye movement (REM) sleep. Dose-related changes in intra-specific aggression and muricide occurred in REM sleep-deprived rats only. Dose-response curves are inverted-U shaped with the .05 mg/kg dose producing increases in aggression. Intra-specific and muricide may serve as models of PCP-induced aggression in humans.     

Contribution of the frontal lobe secondary motor area to organization of postural components in human voluntary movement

A total of 225 patients with local verified brain lesions were investigated with a view to identifying the brain regions contributing to organizing postural aspects of voluntary movement. Impaired postural adjustment movements associated with voluntary deep breathing were found in patients with damage primarily to the posterior section of the frontal lobe inferior convolution. Impaired activation of leg and trunk muscles accompanying arm movements were revealed in patients with damage chiefly to the posterior section of the superior convolution of the lobe, including the accessory motor area. It was deduced that postural movements differing in their functional purpose are controlled, like other learned tasks, by different sections of the secondary motor zone of the frontal lobe of the brain.Institute for Information Transmission Studies, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 20, No. 1, pp. 7–15, January–February, 1988.     

Echinostoma caproni: mating behavior and the timing of development and movement of reproductive cells

The development and movement of reproductive cells were determined in Echinsostoma caproni on autoradiograms by labeling nuclei of stem cells during exposure to [3H]thymidine and then transplanting the worms to mice for various times. The development and movement of sperm, primary oocytes, and vitelline cells were much more rapid in E. caproni than other digenetic trematodes investigated previously. Mating behavior was determined by labeling the sperm of 1 adult by in vitro exposure to [3H]tyrosine and transplanting alone or with unlabeled worms to mice for 4 and 6 days. Echinostoma caproni adults self-inseminated when isolated and self- and cross-inseminated when in groups. This behavior is similar to that found for the frog rectal fluke Megalodiscus temperatus but unlike that determined for eyeflukes in the genus Philophthalmus. Worm size was not a barrier to insemination in E. caproni. Cross-insemination could not be detected in 6-day transplants probably because of dilution or elimination of radioactive sperm due to rapid turnover or frequent sperm transfer. An increased number of structural anomalies was noted in the transplanted worms. The most common anomaly was an accumulation of vitelline cells in the vitelline reservoir and ducts.     

Corticotectal and corticostriatal projections from the frontal eye fields of the cat: an anatomical examination using WGA-HRP

Corticofugal projections from the frontal eye fields (FEF) are believed to access the superior colliculus (SC) directly (i.e., monosynaptically) and indirectly (i.e., multisynaptically) through the basal ganglia. The present results suggest that these two pathways are derived from largely segregated populations of corticofugal neurons. Furthermore, while the different subregions of the FEF from which these pathways originate have different termination patterns in the basal ganglia (i.e., striatum, ST), they share a common termination pattern in the SC. Injections of wheat germ agglutinin-horseradish peroxidase (WGA-HRP) into the two major subdivisions of the FEF (presylvian and cruciate sulci) resulted in dense label in both the ST (bilaterally) and the SC (ipsilaterally). Corticostriatal labeling was found in the caudal part of the head of the caudate nucleus (heaviest ipsilaterally), with labeling from cruciate injections located ventromedial to that produced by presylvian injections. Only presylvian injections resulted in labeling in the putamen. Retrograde tracing experiments demonstrated that both presylvian and cruciate corticostriatal projections originated from neurons in lamina III and the upper aspects of lamina V. An additional but small group of presylvian corticostriatal projections was found in lamina VI. Corticotectal terminal labeling was restricted to the deep laminae of the SC and was derived exclusively from lamina V neurons in cortex. They differed from their corticostriatal counterparts in laminar/sub-laminar location and in soma sizes.     

Saccade generation by the frontal eye fields in rhesus monkeys is separable from visual detection and bottom-up attention shift

The frontal eye fields (FEF), originally identified as an oculomotor cortex, have also been implicated in perceptual functions, such as constructing a visual saliency map and shifting visual attention. Further dissecting the area's role in the transformation from visual input to oculomotor command has been difficult because of spatial confounding between stimuli and responses and consequently between intermediate cognitive processes, such as attention shift and saccade preparation. Here we developed two tasks in which the visual stimulus and the saccade response were dissociated in space (the extended memory-guided saccade task), and bottom-up attention shift and saccade target selection were independent (the four-alternative delayed saccade task). Reversible inactivation of the FEF in rhesus monkeys disrupted, as expected, contralateral memory-guided saccades, but visual detection was demonstrated to be intact at the same field. Moreover, saccade behavior was impaired when a bottom-up shift of attention was not a prerequisite for saccade target selection, indicating that the inactivation effect was independent of the previously reported dysfunctions in bottom-up attention control. These findings underscore the motor aspect of the area's functions, especially in situations where saccades are generated by internal cognitive processes, including visual short-term memory and long-term associative memory.     

Attention governs action in the primate frontal eye field

While the motor and attentional roles of the frontal eye field (FEF) are well documented, the relationship between them is unknown. We exploited the known influence of visual motion on the apparent positions of targets, and measured how this illusion affects saccadic eye movements during FEF microstimulation. Without microstimulation, saccades to a moving grating are biased in the direction of motion, consistent with the apparent position illusion. Here we show that microstimulation of spatially aligned FEF representations increases the influence of this illusion on saccades. Rather than simply impose a fixed-vector signal, subthreshold stimulation directed saccades away from the FEF movement field, and instead more strongly in the direction of visual motion. These results demonstrate that the attentional effects of FEF stimulation govern visually guided saccades, and suggest that the two roles of the FEF work together to select both the features of a target and the appropriate movement to foveate it.     

Differentiation between vergence and saccadic functional activity within the human frontal eye fields and midbrain revealed through fMRI

Purpose

Eye movement research has traditionally studied solely saccade and/or vergence eye movements by isolating these systems within a laboratory setting. While the neural correlates of saccadic eye movements are established, few studies have quantified the functional activity of vergence eye movements using fMRI. This study mapped the neural substrates of vergence eye movements and compared them to saccades to elucidate the spatial commonality and differentiation between these systems.

Methodology

The stimulus was presented in a block design where the ‘off’ stimulus was a sustained fixation and the ‘on’ stimulus was random vergence or saccadic eye movements. Data were collected with a 3T scanner. A general linear model (GLM) was used in conjunction with cluster size to determine significantly active regions. A paired t-test of the GLM beta weight coefficients was computed between the saccade and vergence functional activities to test the hypothesis that vergence and saccadic stimulation would have spatial differentiation in addition to shared neural substrates.

Results

Segregated functional activation was observed within the frontal eye fields where a portion of the functional activity from the vergence task was located anterior to the saccadic functional activity (z>2.3; p<0.03). An area within the midbrain was significantly correlated with the experimental design for the vergence but not the saccade data set. Similar functional activation was observed within the following regions of interest: the supplementary eye field, dorsolateral prefrontal cortex, ventral lateral prefrontal cortex, lateral intraparietal area, cuneus, precuneus, anterior and posterior cingulates, and cerebellar vermis. The functional activity from these regions was not different between the vergence and saccade data sets assessed by analyzing the beta weights of the paired t-test (p>0.2).

Conclusion

Functional MRI can elucidate the differences between the vergence and saccade neural substrates within the frontal eye fields and midbrain.     

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.     

Animal behavior: timing in the wild

A recent study has found that Rufous hummingbirds time the interval between successive visits to flowers that replenish at different rates. The hummingbirds have been shown to store information about both where and when they ate throughout the day, evidence that this species has two components of episodic memory.     

Learned changes in the complexity of movement organization during multijoint, standing pulls

 This paper tests the hypothesis that the central nervous system (CNS) learns to organize multijoint movements during a multijoint ‘bouncing pull’ task such that, after practice, motion of the anterior-posterior center of mass (CM_AP) more closely resembles that of a conservative, one degree of freedom (DF), inverted pendulum model. The task requires standing human subjects to produce precise peak pulling forces on a handle while maintaining balance – goals that can be easily accomplished if movement is organized as in the model. Ten freely standing subjects practiced making brief, bouncing pulls in the horizontal direction to target forces (20–80% of maximum) for 5 days. Pulling force, body kinematic and force plate data were recorded. An eight-segment analysis determined sagittal-plane CM motion. We compared the effects of practice on the regression-based fit between actual and model-simulated CM_AP trajectories, and on measures of CM_AP phase plane symmetry and parameter constancy that the model predicts. If the CNS learns to organize movements like the inverted pendulum model, then model fit should improve and all other measures should approach zero after practice. The fit between modeled and actual CM_AP motion did not improve significantly with practice, except for moderate force pulls. Nor did practice increase phase plane symmetry or parameter constancy. Specifically, practice did not decrease the differences between the pre-impact and rebound positions or speeds of the CM_AP, although speed difference increased with pulling force. CM_AP at the end of the movement was anterior to its initial position; the anterior shift increased after practice. Differences between the pre-pull and balance-recovery ankle torque (T _A) impulses were greater on day 5 and correlated with the anterior shift in CM_AP. These results suggest that practice separately influenced the force production and balance recovery phases. A modified model with damping could not explain the observed behaviors. A modified model using the actual time-varying T_A profiles improved fit at lower force levels, but did not explain the increased postural shift after practice. We conclude that the CNS does not learn to organize movements like the conservative, inverted pendulum model, but rather learned a more complex form of organization that capitalized on more time-varying controls and more intersegmental dynamics. We hypothesize that at least one additional DF and at least one time-varying parameter will be needed to explain fully how the CNS learns to organize multijoint, bouncing pulls made while standing. Received: 9 January 1997 / Accepted in revised form: 27 May 1997     

Neuromodulation for behavior in the locust frontal ganglion

Neuromodulators orchestrate complex behavioral routines by their multiple and combined effects on the nervous system. In the desert locust, Schistocerca gregaria, frontal ganglion neurons innervate foregut dilator muscles and play a key role in the control of foregut motor patterns. To further investigate the role of the frontal ganglion in locust behavior, we currently focus on the frontal ganglion central pattern generator as a target for neuromodulation. Application of octopamine, a well-studied insect neuromodulator, generated reversible disruption of frontal ganglion rhythmic activity. The threshold for the modulatory effects of octopamine was 10^–6 mol l^–1, and 10^–4 mol l^–1 always abolished the ongoing rhythm. In contrast to this straightforward modulation, allatostatin, previously reported to be a myoinhibitor of insect gut muscles, showed complex, tri-modal, dose-dependent effects on frontal ganglion rhythmic pattern. Using a novel cross-correlation analysis technique, we show that different allatostatin concentrations have very different effects not only on cycle period but also on temporal characteristics of the rhythmic bursts of action potentials. Allatostatin also altered the frontal ganglion rhythm in vivo. The analysis technique we introduce may be instrumental in the study of not fully characterized neural circuits and their modulation. The physiological significance of our results and the role of the modulators in locust behavior are discussed.Abbreviation CPG central pattern generator - FG frontal ganglion - JH juvenile hormone - STNS stomatogastric nervous system     

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.

     

Relative spike timing in stochastic oscillator networks of the Hermissenda eye

The role of relative spike timing on sensory coding and stochastic dynamics of small pulse-coupled oscillator networks is investigated physiologically and mathematically, based on the small biological eye network of the marine invertebrate Hermissenda. Without network interactions, the five inhibitory photoreceptors of the eye network exhibit quasi-regular rhythmic spiking; in contrast, within the active network, they display more irregular spiking but collective network rhythmicity. We investigate the source of this emergent network behavior first analyzing the role of relative input to spike–timing relationships in individual cells. We use a stochastic phase oscillator equation to model photoreceptor spike sequences in response to sequences of inhibitory current pulses. Although spike sequences can be complex and irregular in response to inputs, we show that spike timing is better predicted if relative timing of spikes to inputs is accounted for in the model. Further, we establish that greater noise levels in the model serve to destroy network phase-locked states that induce non-monotonic stimulus rate-coding, as predicted in Butson and Clark (J Neurophysiol 99:146–154, 2008a; J Neurophysiol 99:155–165, 2008b). Hence, rate-coding can function better in noisy spiking cells relative to non-noisy cells. We then study how relative input to spike–timing dynamics of single oscillators contribute to network-level dynamics. Relative timing interactions in the network sharpen the stimulus window that can trigger a spike, affecting stimulus encoding. Also, we derive analytical inter-spike interval distributions of cells in the model network, revealing that irregular Poisson-like spike emission and collective network rhythmicity are emergent properties of network dynamics, consistent with experimental observations. Our theoretical results generate experimental predictions about the nature of spike patterns in the Hermissenda eye.