Saccadic head movements of the praying mantis, with particular reference to visual and proprioceptive information

ABSTRACT. Horizontal head movements of the praying mantis, Sphodromantis lineola Burm., were recorded continuously. They responded to the presence of a live blowfly prey in the antero-lateral visual field with a rapid saccadic head movement. The angular movement of a fixation saccade was correlated positively to the displacement of the prey from the prothoracic midline. Saccade magnitude and velocity are related. After the stimulus moved out of the visual field, the mantis made a second saccadic head movement, a return saccade towards the body midline. We observed return saccades in which the head overshot or undershot the body midline, as well as saccades which returned the head exactly to its initial position. In 92% of trials with intact mantids, the return movement succeeded eventually in rotating the head back to its initial position, whereas after removal of the neck hair plates this occurred in only 47% of trials. There is a consistent relation between saccade extent and velocity. Velocities of return saccades were slower than those of fixation saccades. It is suggested that sensory inputs from the neck hair plate proprioceptors modify both the magnitude and the angular velocity of fixation and return saccadic head movements.     

How Lovebirds Maneuver Rapidly Using Super-Fast Head Saccades and Image Feature Stabilization

Diurnal flying animals such as birds depend primarily on vision to coordinate their flight path during goal-directed flight tasks. To extract the spatial structure of the surrounding environment, birds are thought to use retinal image motion (optical flow) that is primarily induced by motion of their head. It is unclear what gaze behaviors birds perform to support visuomotor control during rapid maneuvering flight in which they continuously switch between flight modes. To analyze this, we measured the gaze behavior of rapidly turning lovebirds in a goal-directed task: take-off and fly away from a perch, turn on a dime, and fly back and land on the same perch. High-speed flight recordings revealed that rapidly turning lovebirds perform a remarkable stereotypical gaze behavior with peak saccadic head turns up to 2700 degrees per second, as fast as insects, enabled by fast neck muscles. In between saccades, gaze orientation is held constant. By comparing saccade and wingbeat phase, we find that these super-fast saccades are coordinated with the downstroke when the lateral visual field is occluded by the wings. Lovebirds thus maximize visual perception by overlying behaviors that impair vision, which helps coordinate maneuvers. Before the turn, lovebirds keep a high contrast edge in their visual midline. Similarly, before landing, the lovebirds stabilize the center of the perch in their visual midline. The perch on which the birds land swings, like a branch in the wind, and we find that retinal size of the perch is the most parsimonious visual cue to initiate landing. Our observations show that rapidly maneuvering birds use precisely timed stereotypic gaze behaviors consisting of rapid head turns and frontal feature stabilization, which facilitates optical flow based flight control. Similar gaze behaviors have been reported for visually navigating humans. This finding can inspire more effective vision-based autopilots for drones.     

Function of a fly motion-sensitive neuron matches eye movements during free flight

Sensing is often implicitly assumed to be the passive acquisition of information. However, part of the sensory information is generated actively when animals move. For instance, humans shift their gaze actively in a sequence of saccades towards interesting locations in a scene. Likewise, many insects shift their gaze by saccadic turns of body and head, keeping their gaze fixed between saccades. Here we employ a novel panoramic virtual reality stimulator and show that motion computation in a blowfly visual interneuron is tuned to make efficient use of the characteristic dynamics of retinal image flow. The neuron is able to extract information about the spatial layout of the environment by utilizing intervals of stable vision resulting from the saccadic viewing strategy. The extraction is possible because the retinal image flow evoked by translation, containing information about object distances, is confined to low frequencies. This flow component can be derived from the total optic flow between saccades because the residual intersaccadic head rotations are small and encoded at higher frequencies. Information about the spatial layout of the environment can thus be extracted by the neuron in a computationally parsimonious way. These results on neuronal function based on naturalistic, behaviourally generated optic flow are in stark contrast to conclusions based on conventional visual stimuli that the neuron primarily represents a detector for yaw rotations of the animal.     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

Oculomotor factors in the aetiology of occupational cervicobrachial diseases (OCD)

The traditional posture-ergonomic perspective on the aetiology of Occupational Cervicobrachial Disease (OCD) is discussed and criticized in the light of present knowledge of oculomotor strain during sustained visual work at short distances. Two experiments on ocularly induced neck muscular tension are reported. In both experiments EMG's were taken from six different muscles in the head, neck and shoulder region during a visual discrimination task. In Experiment 1, accommodation and fusion requirements were systematically varied by changing viewing distance in combination with the application of minus-lenses and base-out prisms. EMG was shown to increase as a function of accommodation and fusion load. In Experiment 2, a clinical population with severe and long lasting neck and shoulder problems and inappropriate optical corrections was studied with the same experimental design. EMG was shown to decrease when habitual corrections were replaced by more appropriate ones.     

Slow Cortical Potentials Preceeding Visually Guided Saccades in Schizophrenics

The parameters of saccades and presaccadic slow potentials were studied in right-handed men with a dominant right eye, including 19 schizophrenics and 12 healthy subjects. For visual stimulation, three light-emitting diodes were used, which were located in the center of the visual field (the central fixation stimulus) and 10° to the right and left of it (peripheral stimuli). Two stimulation protocols were used: with a simultaneous switching off of the central fixation stimulus and switching on of the peripheral stimuli (test 1) and with an interstimulus gap of 200 ms (test 2). According to the latency, saccades were divided into anticipatory, express, and regular. Slow EEG potentials preceding regular saccades were analyzed. It was found that the proportion of anticipatory saccades is considerably higher than the normal value in schizophrenia. The analysis of the presaccadic potentials demonstrated a significant decrease in the amplitude of negative potentials in the vertex region at early stages of presaccadic preparation and its increase in the occipital region at late stages. Test 2 in the patients demonstrated an increase in the positivity focus in the frontal region of the right hemisphere. It was assumed that the alterations found in schizophrenia result from the deficit of frontal cortical fields.     

Analysis of the middle latency evoked potentials to angular acceleration impulses in man

The middle latency vestibular evoked potential (ML-VsEP) recorded with scalp electrodes in man in response to impulses of angular acceleration is dominated by a forehead positive peak at about 15 ms and a negative peak at about 20 ms; the peak amplitude of this component is about 30 μV. This is followed by slower, smaller amplitude activity. The latency of this initial peak is similar to the latency of the vestibulo-ocular reflex (VOR) in monkeys. The present study was undertaken to elucidate the possible relation between the ML-VsEPs and VOR. This included recordings from forehead-mastoid electrodes (sites used to record VsEP) and other scalp electrodes and the recording of potentials due to eye movement: the electro-oculogram. Direct recording of eye movements was also conducted using an infra-red reflection device in those experiments in which the head was not moved. The recordings were conducted in man during vestibular stimulation eliciting VsEPs, during voluntary eye movements and during caloric and optokinetic stimulation. These experiments indicated that the 15–20 ms component of the ML-VsEP was not due to movements of the eye (corneoretinal dipole). The large amplitude 15–20 ms component of the ML-VsEP was similar in general magnitude, waveform, polarity, duration and rise time to the highly synchronous pre-saccadic spike (neural and/or myogenic) which precedes nystagnys and voluntary saccades. It therefore probably represents vestibular-initiated electrical activity in motor units of the extra-ocular muscles which then produce anti-compensatory saccades.     

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.     

Relationship between reaction time of eye movement and activity of the neck extensors

This study investigated the relationship between the reaction time of eye movement (RTEM) and activity of the superficial neck extensor muscles when the shoulder girdle elevator muscles contracted isometrically. The results were compared with those of a previous study in which the subjects's head was fixed and loaded with the neck flexed. When the shoulder girdle elevator muscles contracted isometrically, RTEM decreased significantly in comparison to RTEM at rest. This demonstrated that the reaction time significantly decreased not only as a result of the neck in flexion, which activated the deep and superficial neck extensor muscles, but also from contraction of the shoulder girdle elevator muscles which mainly activated the superficial extensor muscles. The relationship between RTEM and relative muscle load of the shoulder girdle elevator muscles showed that RTEM decreased up to 30% loading, and with loading above 40% the RTEM was longer than with 30%. The relative muscle load for the shortest RTEM demonstrated a subject-to-subject variance ranging from 24.7% to 49.6%. The difference between RTEM at rest and at their shortest reaction time was approximately 20 ms, which was consistent with the data for the neck in flexion. However, the relative muscle load for the shortest RTEM differed between the current and previous studies. The parameters obtained in this study were higher than for those in the previous study.     

Control of the superior colliculus by the lateral prefrontal cortex

Several decades of patient, functional imaging and neurophysiological studies have supported a model in which the lateral prefrontal cortex (PFC) acts to suppress unwanted saccades by inhibiting activity in the oculomotor system. However, recent results from combined PFC deactivation and neural recordings of the superior colliculus in monkeys demonstrate that the primary influence of the PFC on the oculomotor system is excitatory, and stands in direct contradiction to the inhibitory model of PFC function. Although erroneous saccades towards a visual stimulus are commonly labelled reflexive in patients with PFC damage or dysfunction, the latencies of most of these saccades are outside of the range of express saccades, which are triggered directly by the visual stimulus. Deactivation and pharmacological manipulation studies in monkeys suggest that response errors following PFC damage or dysfunction are not the result of a failure in response suppression but can best be understood in the context of a failure to maintain and implement the proper task set.     

Latent period of antisaccades in various conditions of visual stimulation in man

The latent periods (LP) of normal saccades and antisaccades were studied in 10 right-handed healthy subjects in two series of experiments. Peripheral visual stimuli were located at an angle of 10 degrees with respect to the central fixation stimulus in the left and right visual semifields. Two standard schemes of visual stimulation: 1) SS (single step), i.e., switching the peripheral stimulus on immediately after switching the central stimulus of; 2) GAP, i.e., the same with the interstimulus interval in 200 ms. It was shown that in the GAP stimulation condition, the LP of both saccades and antisaccades was 30-50 shorter than in the SS condition. The LP of antisaccades was longer than that of saccades by 145-300 ms. The LP of the leftward antisaccades was by 10-100 ms shorter than that of the rightward ones. Probably, this phenomenon reflects the dominance of the right hemisphere in spatial attention.     

Interaction between acoustic startle and habituated neck postural responses in seated subjects.

Postural and startle responses rapidly habituate with repeated exposures to the same stimulus, and the first exposure to a seated forward acceleration elicits a startle response in the neck muscles. Our goal was to examine how the acoustic startle response is integrated with the habituated neck postural response elicited by forward accelerations of seated subjects. In experiment 1, 14 subjects underwent 11 sequential forward accelerations followed by 5 additional sled accelerations combined with a startling tone (124-dB sound pressure level) initiated 18 ms after sled acceleration onset. During the acceleration-only trials, changes consistent with habituation occurred in the root-mean-square amplitude of the neck muscles and in the peak amplitude of five head and torso kinematic variables. The subsequent addition of the startling tone restored the amplitude of the neck muscles and four of the five kinematic variables but shortened onset of muscle activity by 9-12 ms. These shortened onset times were further explored in experiment 2, wherein 16 subjects underwent 11 acceleration-only trials followed by 15 combined acceleration-tone trials with interstimulus delays of 0, 13, 18, 23, and 28 ms. Onset times shortened further for the 0- and 13-ms delays but did not lengthen for the 23- and 28-ms delays. These temporal and spatial changes in EMG can be explained by a summation of the excitatory drive converging at or before the neck muscle motoneurons. The present observations suggest that habituation to repeated sled accelerations involves extinguishing the startle response and tuning the postural response to the whole body disturbance.     

Precisely timed oculomotor and parietal EEG activity in perceptual switching

Blinks and saccades cause transient interruptions of visual input. To investigate how such effects influence our perceptual state, we analyzed the time courses of blink and saccade rates in relation to perceptual switching in the Necker cube. Both time courses of blink and saccade rates showed peaks at different moments along the switching process. A peak in blinking rate appeared 1,000 ms prior to the switching responses. Blinks occurring around this peak were associated with subsequent switching to the preferred interpretation of the Necker cube. Saccade rates showed a peak 150 ms prior to the switching response. The direction of saccades around this peak was predictive of the perceived orientation of the Necker cube afterwards. Peak blinks were followed and peak saccades were preceded by transient parietal theta band activity indicating the changing of the perceptual interpretation. Precisely-timed blinks, therefore, can initiate perceptual switching, and precisely-timed saccades can facilitate an ongoing change of interpretation.     

Spatio-temporal evaluation of neck muscle activation during postural perturbations in healthy subjects.

The purpose of this study was to examine the spatio-temporal activation of the sternocleidomastoid (SCM) and cervical extensor (CE) muscles with respect to the deltoid muscle onset during rapid voluntary upper limb movement in healthy volunteers. The repeatability and reliability of the spatio-temporal aspects of the myoelectric signals were also examined. Ten subjects performed bilateral and unilateral rapid upper limb flexion, abduction and extension in response to a visual stimulus. EMG onsets and normalised root mean square (nRMS) values were calculated for the SCM and CE muscles. Subjects attended three testing sessions over non-consecutive days allowing the repeatability and reliability of these measures to be assessed. The SCM and CE muscles demonstrated feed-forward activation (activation within 50 ms of deltoid onset) during rapid arm movements in all directions. The sequence and magnitude of neck muscle activation displayed directional specificity, however, the neck flexor and extensor muscles displayed co-activation during all perturbations. EMG onsets demonstrated high repeatability in terms of repeated measure precision (nSEM in the range 1.9-5.7%). This was less evident for the repeatability of nRMS values. The results of this study provide a greater understanding of cervical neuromotor control strategies. During bilateral and unilateral upper limb perturbations, the SCM and CE muscles demonstrate feed-forward co-activation. It seems apparent that feed-forward activation of neck muscles is a mechanism necessary to achieve stability for the visual and vestibular systems, whilst ensuring stabilisation and protection of the cervical spine.     

Lateralization of saccadic latency during monocular presentation of stimuli to a leading and non-leading eye

Saccadic latencies were studied in ten healthy subjects. Peripheral targets were presented monocularly to a leading and nonleading eyes in the right and left hemifields. SS (single step) and OVERLAP (200 ms) schemes of visual stimulation were used. Under OVERLAP conditions, the saccadic latency was longer by 30-39 ms and the number of long-latency saccades was higher than under SS conditions, especially in subjects with mixed asymmetry profiles. In the majority of subjects with right asymmetry profile, the latencies of saccades during stimulation of the leading eye were by 12 ms shorter than during stimulation of the nonleading eye, and the latencies of right saccades were by 24 ms shorter than that of the left saccades independently of the stimulated eye. The obtained results explain some characteristic features of hemyspheric asymmetry in organization of saccadic movements.     

Saccadic head and thorax movements in freely walking blowflies

Visual information processing is adapted to the statistics of natural visual stimuli, and these statistics depend to a large extent on the movements of an animal itself. To investigate such movements in freely walking blowflies, we measured the orientation and position of their head and thorax, with high spatial and temporal accuracy. Experiments were performed on Calliphora vicina, Lucilia cuprina and L. caesar. We found that thorax and head orientation of walking flies is typically different from the direction of walking, with differences of 45° common. During walking, the head and the thorax turn abruptly, with a frequency of 5–10 Hz and angular velocities in the order of 1,000°/s. These saccades are stereotyped: head and thorax start simultaneously, with the head turning faster, and finishing its turn before the thorax. The changes in position during walking are saccade-like as well, occurring synchronously, but on average slightly after the orientation saccades. Between orientation saccades the angular velocities are low and the head is held more stable than the thorax. We argue that the strategy of turning by saccades improves the performance of the visual system of blowflies.     

Different programming modes of human saccadic eye movements as a function of stimulus eccentricity: Indications of a functional subdivision of the visual field

1. Voluntary saccadic eye movements were made toward flashes of light on the horizontal meridian, whose duration and distance from the point of fixation were varied; eye movements were measured using d.c.-electrooculography.—2. Targets within 10°–15° eccentricity are usually reached by one saccadic eye movement. When the eyes turn toward targets of more than 10°–15° eccentricity, the first saccadic eye movement falls short of the target by an angle usually not exceeding 10°. The presence of the image of the target off the fovea (visual error signal) subsequent to such an undershoot elicits, after a short interval, corrective saccades (usually one) which place the image of the target on the fovea. In the absence of a visual error signal, the probability of occurrence of corrective saccades is low, but it increases with greater target eccentricities. These observations suggest that there are different, eccentricity-dependent modes of programming saccadic eye movements.—3. Saccadic eye movements appear to be programmed in retinal coordinates. This conclusion is based on the observations that, irrespective of the initial position of the eyes in the orbit, a) there are different programming modes for eye movements to targets within and beyond 10°–15° from the fixation point, and b_ the maximum velocity of saccadic eye movements is always reached at 25° to 30° target eccentricity. —4. Distributions of latency and intersaccadic interval (ISI) are frequently multimodal, with a separation between modes of 30 to 40 msec. These observations suggest that saccadic eye movements are produced by mechanisms which, at a frequency of 30 Hz, process visual information. —5. Corrective saccades may occur after extremely short intervals (30 to 60 msec) regardless of whether or not a visual error signal is present; the eyes may not even come to a complete stop during these very short intersaccadic intervals. It is suggested that these corrective saccades are triggered by errors in the programming of the initial saccadic eye movements, and not by a visual error signal. —6. The exitence of different, eccentricity-dependent programming modes of saccadic eye movements, is further supported by anatomical, physiological, psychophysical, and neuropathological observations that suggest a dissociation of visual functions dependent on retinal eccentricity. Saccadic eye movements to targets more eccentric than 10°–15° appear to be executed by a mechanism involving the superior colliculus (perhaps independent of the visual cortex), whereas saccadic eye movements to less eccentric targets appear to depend on a mechanism involving the geniculo-cortical pathway (perhaps in collaboration with the superior colliculus).     

Spatiotopic transfer of visual-form adaptation across saccadic eye movements

Although conscious perception is smooth and continuous, the input to the visual system is a series of short, discrete fixations interleaved with rapid shifts of the eye. One possible explanation for visual stability is that internal maps of objects and their visual properties are remapped around the time of saccades, but numerous studies have demonstrated that visual patterns are not combined across saccades. Here, we report that visual-form aftereffects transfer across separate fixations when adaptor and test are presented in the same spatial position. The magnitude of the transsaccadic adaptation increased with stimulus complexity, suggesting a progressive construction of spatiotopic receptive fields along the visual-form pathway. These results demonstrate that basic shape information is combined across saccades, allowing for predictive and consistent information from the past to be incorporated into each new fixation.     

Resistance training and human cervical muscle recruitment plasticity

Conley, Michael S., Michael H. Stone, Michael Nimmons, andGary A. Dudley. Resistance training and human cervical muscle recruitment plasticity. J. Appl.Physiol. 83(6): 2105-2111, 1997.This studyexamined cervical neuromuscular adaptations to resistance training. TheResX group performed conventional resistance training plushead-extension exercise. Another group performed only conventional resistance training, and the control group performed no resistance exercise. Muscle use during head extension was determinedby quantifying shifts in T2 in serial-transaxial magnetic resonanceimages of the neck. ResX was the only group that showed a trainingeffect. Training decreased (P < 0.05) the cross-sectional area (CSA) of cervical muscle used to performsubmaximal head extension by 31%. This reflected a decrease(P < 0.05) in relative use of thesplenius capitis, semispinalis capitis, and semispinalis cervicis andmultifidus muscles by about one-third; their percentage of CSA showingcontrast shift was reduced from 60 to 40% on average. This sameexercise evoked no contrast shift in the levator scapulae, longissimus capitis and cervicis, and scalenus medius and anterior muscles posttraining, yet 20% or more of their CSA was engaged pretraining. The relative CSA of cervical musculature that was used to perform maximal head extension was increased(P < 0.05) 16% bytraining. The findings suggest functional redundancy ofneck musculature that can be modified by training; submaximal tasks canbe performed despite cessation of recruitment of individual muscles,yet recruitment can be increased for maximal efforts. These resultsalso suggest that neuromuscular adaptations to training require aspecific cervical exercise

     

Activation of Neck and Low-Back Muscles Is Reduced with the Use of a Neck Balance System Together with a Lumbar Support in Urban Drivers

Driving is associated with high activation of low-back and neck muscles due to the sitting position and perturbations imposed by the vehicle. The aim of this study was to investigate the use of a neck balance system together with a lumbar support on the activation of low-back and neck muscles during driving. Twelve healthy male subjects (age 32±6.71 years) were asked to drive in two conditions: 1) with devices; 2) without devices. During vehicle accelerations and decelerations root mean square (RMS) of surface electromyography (sEMG) was recorded from the erector spinae, semispinalis capitis and sternocleidomastoid muscles and expressed as a percentage of maximal voluntary contraction (MVC). The pitch of the head was obtained by means of an inertial sensor placed on the subjects’ head. A visual analog scale (VAS) was used to assess the level of perceived comfort. RMS of the low back muscles was lower with than without devices during both acceleration and deceleration of the vehicle (1.40±0.93% vs 29 2.32±1.90% and 1.88±1.45% vs 2.91±2.33%, respectively), while RMS of neck extensor muscles was reduced only during acceleration (5.18±1.96% vs 5.91±2.16%). There were no differences between the two conditions in RMS of neck flexor muscles, the pitch of the head and the VAS score. The use of these two ergonomic devices is therefore effective in reducing the activation of low-back and neck muscles during driving with no changes in the level of perceived comfort, which is likely due to rebalancing weight on the neck and giving a neutral position to lumbar segments.