Edward G. Freedman

Coordination of the eyes and head during visual orienting

Changing the direction of the line of sight is essential for the visual exploration of our environment. When the head does not move, re-orientation of the visual axis is accomplished with high velocity, conjugate movements of the eyes known as saccades. Our understanding of the neural mechanisms that control saccadic eye movements has advanced rapidly as specific hypotheses have been developed, evaluated and sometimes rejected on the basis of new observations. Constraints on new hypotheses and new tests of existing models have often arisen from the careful assessment of behavioral observations. The definition of the set of features (or rules) of saccadic eye movements was critical in the development of hypotheses of their neural control. When the head is free to move, changes in the direction of the line of sight can involve simultaneous saccadic eye movements and movements of the head. When the head moves in conjunction with the eyes to accomplish these shifts in gaze direction, the rules that helped define head-restrained saccadic eye movements are altered. For example, the slope relationship between duration and amplitude for saccadic eye movements is reversed (the slope is negative) during gaze shifts of similar amplitude initiated with the eyes in different orbital positions. Modifications to the hypotheses developed in head-restrained subjects may be needed to account for these new observations. This review briefly recounts features of head-restrained saccadic eye movements, and then describes some of the characteristics of coordinated eye–head movements that have led to development of new hypotheses describing the mechanisms of gaze shift control.

Coordination of the eyes and head: movement kinematics.

Abstract. When the head is restrained, saccades are characterized by lawful relationships between movement amplitude, peak velocity, and duration. In addition, the spatiotemporal progression of saccades (i.e., movement kinematics) is predictable if saccade amplitude and direction are known. However, when the head is free to move, changes in the direction of the line of sight (gaze shifts) often involve saccades associated with simultaneous head movements. The metrics (duration, amplitude, peak velocity) and kinematics of saccades occurring in conjunction with head movements cannot be predicted on the basis of saccade amplitude and direction alone. For example, when the head is unrestrained, velocity profiles of 35° eye movements can be symmetrical and might have peaks ~600°/s. But, 35° eye movements can also have peak velocities of ~300°/s and have velocity profiles with two pronounced peaks: an initial peak followed by a reduction and subsequent increase in velocity. Saccade amplitude and direction are insufficient to predict the shape of the velocity profile. However, as illustrated in this report, if the amplitude of the concurrent head movement is taken into account, saccade kinematics are predictable even during gaze shifts with large head components. The data presented here are indicative of an interaction between eye and head motor systems in which head movement commands alter the execution of concurrent saccades.

Interactions between eye and head control signals can account for movement kinematics.

Abstract. Advances in understanding the neural control of saccades (visual orienting movements made when the head is prevented from moving) stem largely from early modeling efforts which provided a framework for developing and testing hypotheses about the relationships between neural activity and observed behaviors. When the head is free to move, visual orienting is often accomplished with coordinated movements of the eyes and head. A recent description of the temporal progression (i.e., kinematics) of these movements led to the hypothesis that eye and head control signals interact. This hypothesis is now formalized as a control systems model which accounts for existing data and makes explicit predictions about the neural control of orienting gaze shifts.

Clutter interference and the integration time of echoes in the echolocating bat, Eptesicus fuscus

The ability of the echolocating bat, Eptesicus fuscus, to detect a sonar target is affected by the presence of other targets along the same axis at slightly different ranges. If echoes from one target arrive at about the same delay as echoes from another target, clutter interference occurs and one set of echoes masks the other. Although the bats sonar emissions and the echoes themselves are 2 to 5 ms long, echoes (of approximately equal sensation levels--around 15 dB SL) only interfere with each other if they arrive within 200 to 400 microseconds of the same arrival time. This figure is an estimate of the integration time of the bats sonar receiver for echoes. The fine structure of the clutter-interference data reflects the reinforcement and cancellation of echoes according to their time separation. When clutter interference first occurs, the waveforms of test and cluttering echoes already overlap for much of their duration. The masking effect underlying clutter interference appears specifically due to overlap, not between raw echo waveforms, but between the patterns of mechanical excitation created when echoes pass through bandpass filters equivalent to auditory-nerve tuning curves. While the time scale of clutter interference is substantially shorter than the duration of echo waveforms, it still is much longer than the eventual width of a targets range-axis image expressed in terms of echo delay.

Serotonin in the leech central nervous system: anatomical correlates and behavioral effects

Summary1.Serotonin is sequestered by a limited population of identified neurons in the 32 ganglia of the leech nervous system. A major fraction of the serotonin in each ganglion is contained in the paired Retzius cells, colossal effector neurons whose size varies longitudinally. The 5 other classes of identified serotonin-containing neurons, one effector cell and 4 interneurons, are approximately twice as numerous in anterior as in posterior ganglia.2.We dissected 6 longitudinal samples from the ventral nerve cords of hungry Hirudo medicinalis, and measured their serotonin content using high pressure liquid chromatography with electrochemical detection. A consistent neurochemical pattern emerged in which segmental ganglia 2–4 had the highest quantity of serotonin: 18.51 pmol per ganglion. The anterior cerebral ganglion contained 14.78 pmol, and the content of the 4 posterior samples, segmental ganglia 7–10, 12–15, 17–20 and the caudal ganglion, decreased continuously from 16.35, 15.08, 10.75 to 2.51 pmol per ganglion, respectively. Morphometric analyses indicated that this pattern of ganglionic serotonin correlated primarily with longitudinal variations in the number of serotonin neurons per ganglion and secondarily with volume of the Retzius cells. Retzius cell volume correlated highly with the mass of their innervated body segments both of which are largest in mid-body domains.3.Serotonin expresses leech feeding, and its ganglionic levels are a potentially useful index of behavioral state. We measured serotonin in the ganglionic samples from hungry and satiated leeches. The samples from recently fed animals contained 28% less serotonin than those from hungry ones. The amounts of serotonin in the cerebral and all the segmental samples from satiated leeches were significantly lower than equivalent samples of hungry animals. A similar pattern of depletion was seen in leeches which fed for a prolonged period (90 to 120 min) rather than the normal period of 30 min.4.The effects of ingestion on serotonin-containing neurons was examined with the glyoxylic acid-induced histochemical fluorescence. The levels of fluorescence in all serotonin neurons in fed leeches were consistently lower than those in equivalent neurons in hungry animals, corroborating the ganglionic decrease in serotonin in satiated leeches.5.To examine effects of body wall distension on serotonin levels, hungry leeches were fed to satiation, and half of them were relaxed by removing their distending blood meals. After 6 weeks, ganglionic serotonin in leeches with relaxed bodies was 21% higher than in those with distended bodies.6.Ingestive behavior depletes serotonin from leech neurons and body wall distension appears to interfere with its synthesis. The behavioral states of leech feeding are implicated in the turnover and the ganglionic levels of a behaviorally important monoamine.

Cortical and subcortical contributions to coordinated eye and head movements.

This paper summarizes recent experiments conducted by the authors - experiments that studied the behavioral characteristics of large gaze shifts and the neural bases of coordinated movements of the eyes and head.

Electrical stimulation of rhesus monkey nucleus reticularis gigantocellularis. I. Characteristics of evoked head movements.

The nucleus reticularis gigantocellularis (NRG) receives monosynaptic input from the superior colliculus (SC) and projects directly to neck motor neuron pools. Neurons in NRG are well situated to play a critical role in transforming SC signals into head movement commands. A previous study of movements evoked by NRG stimulation in the primate reported a variety of ipsilateral and contralateral head movements with horizontal, vertical and torsional components. In addition to head movements, it was reported that NRG stimulation could evoke movements of the pinnae, face, upper torso, and co-contraction of neck muscles. In this report, the role of the rhesus monkey NRG in head movement control was investigated using electrical stimulation of the rostral portion of the NRG. The goal was to characterize head movements evoked by NRG stimulation, describe the effects of altering stimulation parameters, and assess the relative movements of the eyes and head. Results indicate that electrical stimulation in the rostral portion of the NRG of the primate can consistently evoke ipsilateral head rotations in the horizontal plane. Head movement amplitude and peak velocity depend upon stimulation parameters (primarily frequency and duration of stimulation trains). During stimulation-induced head movements the eyes counter-rotate (presumably a result of the vestibulo-ocular reflex: VOR). At 46 stimulation sites from two subjects the average gain of this counter-rotation was −0.38 (±0.18). After the end of the stimulation train the head generally continued to move. During this epoch, after electrical stimulation ceased, VOR gain remained at this reduced level. In addition, VOR gain was similarly low when electrical stimulation was carried out during active fixation of a visual target. These data extend existing descriptions of head movements evoked by electrical stimulation of the NRG, and add to the understanding of the role of this structure in producing head movements.

Electrical stimulation of rhesus monkey nucleus reticularis gigantocellularis

Saccade kinematics are altered by ongoing head movements. The hypothesis that a head movement command signal, proportional to head velocity, transiently reduces the gain of the saccadic burst generator (Freedman 2001, Biol Cybern 84:453–462) can account for this observation. Using electrical stimulation of the rhesus monkey nucleus reticularis gigantocellularis (NRG) to alter the head contribution to ongoing gaze shifts, two critical predictions of this gaze control hypothesis were tested. First, this hypothesis predicts that activation of the head command pathway will cause a transient reduction in the gain of the saccadic burst generator. This should alter saccade kinematics by initially reducing velocity without altering saccade amplitude. Second, because this hypothesis does not assume that gaze amplitude is controlled via feedback, the added head contribution (produced by NRG stimulation on the side ipsilateral to the direction of an ongoing gaze shift) should lead to hypermetric gaze shifts. At every stimulation site tested, saccade kinematics were systematically altered in a way that was consistent with transient reduction of the gain of the saccadic burst generator. In addition, gaze shifts produced during NRG stimulation were hypermetric compared with control movements. For example, when targets were briefly flashed 30° from an initial fixation location, gaze shifts during NRG stimulation were on average 140% larger than control movements. These data are consistent with the predictions of the tested hypothesis, and may be problematic for gaze control models that rely on feedback control of gaze amplitude, as well as for models that do not posit an interaction between head commands and the saccade burst generator.

The Locus of Motor Activity in the Superior Colliculus of the Rhesus Monkey Is Unaltered during Saccadic Adaptation

The location of motor-related activity in the deeper layers of the superior colliculus (SC) is thought to generate a desired displacement command specifying the amplitude and direction of saccadic eye movements. However, the amplitude of saccadic eye movements made to visual targets can be systematically altered by surreptitiously moving the target location after the saccade has been initiated. Depending on whether the target is moved closer to or further from the fixation location, adaptation of saccade amplitude results in movements that are either smaller or larger than control movements. It remains an open question whether the SC specifies the desired movement to the original target location or whether SC activity specifies the vector of the amplitude-altered movement that is observed as adaptation progresses. We investigated this question by recording the activity of saccade-related burst neurons in the SC of head-restrained rhesus monkeys during both backward and forward saccadic adaptation. During adaptation in each direction, we find no evidence that is consistent with a change in the locus of SC activity despite changes in saccade amplitude; the location of SC motor-related activity does not appear to be remapped during either forward or backward saccadic adaptation. These data are inconsistent with hypotheses that propose a key role for the SC in mediating the changes in saccade amplitude observed during adaptation.

Amplitude changes in response to target displacements during human eye-head movements.

Sensorimotor adaptation, the ability to adjust motor output in response to persistent changes in sensory input, is a key function of the central nervous system. Although a great deal is known about vestibulo-ocular reflex and saccadic adaptation, relatively little is known about the behavior and neural mechanisms underlying gaze adaptation when the head is free to move. In an attempt to understand the mechanisms of gaze adaptation, and constrain hypotheses concerning the locus at which changes in gaze control may be implemented, we altered the size of large, head-unrestrained gaze shifts made to visual targets by surrepetitiously moving the visual target forward (30 degrees -->60 degrees ) or backwards (60 degrees -->30 degrees ) during gaze shifts. In our 10 human subjects, after a few hundred back-step trials, gaze amplitudes were reduced by between 6 degrees and 27 degrees. Similarly, after a few hundred forward adaptation trials, our subjects increased gaze amplitude by between 0 degrees and 26 degrees. Changes in the amplitude of primary gaze shifts occurred regardless of the particular combinations of eye and head movements that made up the amplitude-altered gaze shifts. When gaze shifts were initiated with the eyes in systematically different positions relative to the head, the resulting changes in gaze, eye and head movement amplitudes were consistent with the hypothesis that gaze adaptation occurs at the level of a gaze shift command and not by altering separately the signals that produce eye and head movements.