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.     

Visual fields, eye movements, and scanning behavior of a sit-and-wait predator, the black phoebe (Sayornis nigricans)

Foraging mode influences the dominant sensory modality used by a forager and likely the strategies of information gathering used in foraging and anti-predator contexts. We assessed three components of visual information gathering in a sit-and-wait avian predator, the black phoebe (Sayornis nigricans): configuration of the visual field, degree of eye movement, and scanning behavior through head-movement rates. We found that black phoebes have larger lateral visual fields than similarly sized ground-foraging passerines, as well as relatively narrower binocular and blind areas. Black phoebes moved their eyes, but eye movement amplitude was relatively smaller than in other passerines. Black phoebes may compensate for eye movement constraints with head movements. The rate of head movements increased before attacking prey in comparison to non-foraging contexts and before movements between perches. These findings suggest that black phoebes use their lateral visual fields, likely subtended by areas of high acuity in the retina, to track prey items in a three-dimensional space through active head movements. These head movements may increase depth perception, motion detection and tracking. Studying information gathering through head movement changes, rather than body posture changes (head-up, head-down) as generally presented in the literature, may allow us to better understand the mechanisms of information gathering from a comparative perspective.     

Head Movements Evoked in Alert Rhesus Monkey by Vestibular Prosthesis Stimulation: Implications for Postural and Gaze Stabilization

The vestibular system detects motion of the head in space and in turn generates reflexes that are vital for our daily activities. The eye movements produced by the vestibulo-ocular reflex (VOR) play an essential role in stabilizing the visual axis (gaze), while vestibulo-spinal reflexes ensure the maintenance of head and body posture. The neuronal pathways from the vestibular periphery to the cervical spinal cord potentially serve a dual role, since they function to stabilize the head relative to inertial space and could thus contribute to gaze (eye-in-head + head-in-space) and posture stabilization. To date, however, the functional significance of vestibular-neck pathways in alert primates remains a matter of debate. Here we used a vestibular prosthesis to 1) quantify vestibularly-driven head movements in primates, and 2) assess whether these evoked head movements make a significant contribution to gaze as well as postural stabilization. We stimulated electrodes implanted in the horizontal semicircular canal of alert rhesus monkeys, and measured the head and eye movements evoked during a 100ms time period for which the contribution of longer latency voluntary inputs to the neck would be minimal. Our results show that prosthetic stimulation evoked significant head movements with latencies consistent with known vestibulo-spinal pathways. Furthermore, while the evoked head movements were substantially smaller than the coincidently evoked eye movements, they made a significant contribution to gaze stabilization, complementing the VOR to ensure that the appropriate gaze response is achieved. We speculate that analogous compensatory head movements will be evoked when implanted prosthetic devices are transitioned to human patients.     

Tonic and modulatory subsystems of the complex gravity receptor system in crickets, Gryllus bimaculatus

The gravity receptor system of crickets Gryllus bimaculatus is composed of antennal, cercal and leg subsystems. The cercal gravity receptors are the club-shaped sensilla. Each of these subsystems elicits compensatory head movements during passive roll.The extent of compensatory head movements depends on the strength of the gravitational stimulus applied to the leg subsystem. Amputation of 2 legs never causes a decrease in reflex amplitude. Unilateral amputation of 1 to 3 legs always induces a roll movement of the head to the intact body side. Therefore, the leg gravity receptor system exerts a modulatory and tonic effect on the neck muscles.The gravity receptors of 1 cercus or 1 antenna only elicit compensatory head movements. They exert no tonic effect on the neck muscles.The results are discussed with respect to (i) the proposed connectivity of the cercus-neck muscle pathway, (ii) mutual inhibitory interactions between the sensory pathways originating in the leg gravity receptors, and (iii) the influence of non-gravitationally induced excitation on the occurrence of compensatory head movements during passive roll of the crickets.     

Function of otolith organ in goldfish revealed from analysis of eye movement induced by acceleration.

An otolith organ on ground behave as a detector of both gravity and linear acceleration, and play an important role in controlling posture and eye movement for tilt of the head or translational motion. On the other hand, a gravitational acceleration ingredient to an otolith organ disappears in microgravity environment. However, linear acceleration can be received by otolith organ and produce a sensation that is different from that on Earth. It is suggested that in microgravity signal from the otolith organ may cause abnormality of posture control and eye movement. Therefore, the central nervous system may re-interprets all output from the otolith organ to indicate linear motion. A study of eye movement has been done a lot as one of a reflection related to an otolith organ system. In this study, we examined function of otolith organ in goldfish revealed from analysis of eye movement induced by linear acceleration or the tilt of body. We analyzed both torsional and vertical eye movements from video images frame by frame. For tilting stimulation, torsional eye movements induced by head down was larger than that induced by head up for larger tilt angle than 30 degrees. In the case of linear acceleration below 0.4 G, however, no clear differences were observed in both torsional and vertical eye movement. These results suggest that body tilt and linear acceleration may not be with equivalent stimulation to cause eye movement on the ground.     

The equine neck and its function during movement and locomotion

During both locomotion and body movements at stance, the head and neck of the horse are a major craniocaudal and lateral balancing mechanism employing input from the visual, vestibular and proprioceptive systems. The function of the equine neck has recently become the focus of several research groups; this is probably also feeding on an increase of interest in the equine neck in equestrian sports, with a controversial discussion of specific neck positions such as maximum head and neck flexion. The aim of this review is to offer an overview of new findings on the structures and functions of the equine neck, illustrating their interplay. The movement of the neck is based on intervertebral motion, but it is also an integral part of locomotion; this is illustrated by the different neck conformations in the breeds of horses used for various types of work. The considerable effect of the neck movement and posture onto the whole trunk and even the limbs is transmitted via bony, ligamentous and muscular structures. Also, the fact that the neck position can easily be influenced by the rider and/or by the employment of training aids makes it an important avenue for training of new movements of the neck as well as the whole horse. Additionally, the neck position also affects the cervical spinal cord as well as the roots of the spinal nerves; besides the commonly encountered long-term neurological effects of cervical vertebral disorders, short-term changes of neural and muscular function have also been identified in the maximum flexion of the cranial neck and head position. During locomotion, the neck stores elastic energy within the passive tissues such as ligaments, joint capsules and fasciae. For adequate stabilisation, additional muscle activity is necessary; this is learned and requires constant muscle training as it is essential to prevent excessive wear and tear on the vertebral joints and also repetitive or single trauma to the spinal nerves and the spinal cord. The capability for this stabilisation decreases with age in the majority of horses due to changes in muscle tissue, muscle coordination and consequently muscle strength.     

Head bobbing and the body movement of little egrets (<Emphasis Type="Italic">Egretta garzetta</Emphasis>) during walking

Although previous studies have indicated that head bobbing of birds is an optokinetic movement, head bobbing can also be controlled by some biomechanical constraints when it occurs during walking. In the present study, the head bobbing, center of gravity, and body movements of little egrets (Egretta garzetta) during walking were examined by determination of the position of the center of gravity using carcasses and by motion analysis of video films of wild egrets during walking. The results showed that the hold phase occurs while the center of gravity is over the supporting foot during the single support phase. In addition, the peak speed of neck extension was coincident with the peak speed of the center of gravity. These movements are similar to those of pigeons, and suggest the presence of biomechanical constraints on the pattern of head bobbing and body movements during walking.     

Control and modulation of canal driven vestibulo-ocular reflex.

It has been well known that the canal driven vestibulo-ocular reflex (VOR) is controlled and modulated through the central nervous system by external sensory information (e.g. visual, otolithic and somatosensory inputs) and by mental conditions. Because the origin of retinal image motion exists both in the subjects (eye, head and body motions) and in the external world (object motion), the head motion should be canceled and/or the object should be followed by smooth eye movements. Human has developed a lot of central nervous mechanisms for smooth eye movements (e.g. VOR, optokinetic reflex and smooth pursuit eye movements). These mechanisms are thought to work for the purpose of better seeing. Distinct mechanism will work in appropriate self motion and/or object motion. As the results, whole mechanisms are controlled in a purpose-directed manner. This can be achieved by a self-organizing holistic system. Holistic system is very useful for understanding human oculomotor behavior.     

Numerical study of the effect of head and eye movement on progression of retinal detachment

Rhegmatogenous retinal detachment (RD) is a sight threatening condition. In this type of RD a break in the retina allows retrohyaloid fluid to enter the subretinal space. The prognosis concerning the patients’ visual acuity is better if the RD has not progressed to the macula. The patient is given a posturing advice of bed rest and semi-supine positioning (with the RD as low as possible) to allow the utilisation of gravity and immobilisation in preventing progression of the RD. It is, however, unknown what external loads on the eye contribute the most to the progression of a RD. The goal of this exploratory study is to elucidate the role of eye movements caused by head movements and saccades on the progression of an RD. A finite element model is produced and evaluated in this study. The model is based on geometric and material properties reported in the literature. The model shows that a mild head movement and a severe eye movement produce similar traction loads on the retina. This implies that head movements—and not eye movements—are able to cause loads that can trigger and progress an RD. These preliminary results suggest that head movements have a larger effect on the progression of an RD than saccadic eye movements. This study is the first to use numerical analysis to investigate the development and progression of RD and shows promise for future work.     

Three-dimensional head angular velocity detection from otolith afferent signals

Afferent signals from the otolith organs can produce compensatory eye position and velocity signals which has been described as linear vestibulo-ocular reflex (LVOR). The afferent otolith signals carry information about head orientation and changes of head orientation relative to gravity. A head orientation (tilt) related position signal can be obtained from population vector coding of tonic otolith afferent signals during static or dynamic head tilts, which in turn could produce compensatory eye position signals in the LVOR. On the other hand, eye angular velocity signals may be extracted, as proposed in this study, from the population response of tilt-velocity sensitive otolith afferents. Such afferents are shown to encode instantaneous head orientation relative to gravity at onset of a head movement and, as the movement continues, the projection of head angular velocity onto the earth-horizontal plane, indicating the instantaneous direction of movement relative to gravity. Angular velocity components along the earth-vertical direction which are not directly encoded by otolith afferents can be detected by central signal processing. Central reconstruction of 3D head angular velocity allows to obtain information about absolute head orientation in space even in the absence of semicircular canal related information. Such information is important for generating compensatory eye movements as well as for dynamic control of posture.     

Spatial constancy mechanisms in motor control

The success of the human species in interacting with the environment depends on the ability to maintain spatial stability despite the continuous changes in sensory and motor inputs owing to movements of eyes, head and body. In this paper, I will review recent advances in the understanding of how the brain deals with the dynamic flow of sensory and motor information in order to maintain spatial constancy of movement goals. The first part summarizes studies in the saccadic system, showing that spatial constancy is governed by a dynamic feed-forward process, by gaze-centred remapping of target representations in anticipation of and across eye movements. The subsequent sections relate to other oculomotor behaviour, such as eye-head gaze shifts, smooth pursuit and vergence eye movements, and their implications for feed-forward mechanisms for spatial constancy. Work that studied the geometric complexities in spatial constancy and saccadic guidance across head and body movements, distinguishing between self-generated and passively induced motion, indicates that both feed-forward and sensory feedback processing play a role in spatial updating of movement goals. The paper ends with a discussion of the behavioural mechanisms of spatial constancy for arm motor control and their physiological implications for the brain. Taken together, the emerging picture is that the brain computes an evolving representation of three-dimensional action space, whose internal metric is updated in a nonlinear way, by optimally integrating noisy and ambiguous afferent and efferent signals.     

Eye Movements Induced by Changes in the Internal Representation of Body Posture

Oculomotor responses to body rotation were investigated in subjects standing with the eyes closed. A rotatable platform was used to provide body rotation relative to the space-stationary head or upper part of the body (fixation of the head; the head and the shoulders; and the head, the shoulders, and the pelvis). A slow rotation of the body about the longitudinal axis by ±6.5° within 10–150 s evoked an illusion of the upper part of the body turning in space, while the moving footplate was perceived as stationary in space. This illusion was accompanied by marked eye movements in the direction of the illusory rotation. In subjects grasping a rigid ground-based handle, the perception of body movements corresponded to the actual rotation of body parts. In this case, the amplitude of eye movements was substantially lower. It was concluded that the eye movement pattern depends not only on the actual relative movement of the body segments but also on the perception of this movement relative to the extrapersonal space.     

Normal gait is differentially influenced by the otoliths

Postural control depends on the integration of vestibular, somatosensory and visual orientation signals. The otolith contribution to postural control is achieved by the integration of otolith inputs and peripheral afferent inputs involved in crossed reflex pathways. This study shows that a functional linkage between otolith signals and activity in lower limb muscles is detectable in normal human gait. The otolith input appears to dominate particularly the neck proprioceptive and gaze motor influences during normal gait. This is demonstrated by an increase of tibialis anterior muscle activity during retroflexion of the head/neck, leading to an increased stability and counteracting possible perturbations. It is also shown by decrease of coordination during the movement caused by larger displacement of the centre of gravity demonstrated in vector diagrams.     

Rotation of subjective vertical is an important factor of visually-induced motion sickness

Motion of visual scene (optokinetic stimulus) projected on a wide screen frequently induces motion sickness. Rotational movements of 3D visual images were analyzed to examine what factors are effective in visually-induced motion sickness and how the gravity contributes to its inducement. While an angle of a rotational axis of 3D visual image from the gravitational direction and its angle from the subjective vertical which was perceived by viewers through 3D visual image were varied, the severity of visually-induced motion sickness was measured.     

Visual attention and stability

In the present review, we address the relationship between attention and visual stability. Even though with each eye, head and body movement the retinal image changes dramatically, we perceive the world as stable and are able to perform visually guided actions. However, visual stability is not as complete as introspection would lead us to believe. We attend to only a few items at a time and stability is maintained only for those items. There appear to be two distinct mechanisms underlying visual stability. The first is a passive mechanism: the visual system assumes the world to be stable, unless there is a clear discrepancy between the pre- and post-saccadic image of the region surrounding the saccade target. This is related to the pre-saccadic shift of attention, which allows for an accurate preview of the saccade target. The second is an active mechanism: information about attended objects is remapped within retinotopic maps to compensate for eye movements. The locus of attention itself, which is also characterized by localized retinotopic activity, is remapped as well. We conclude that visual attention is crucial in our perception of a stable world.     

Tuning Properties of MT and MSTd and Divisive Interactions for Eye-Movement Compensation

The primate brain intelligently processes visual information from the world as the eyes move constantly. The brain must take into account visual motion induced by eye movements, so that visual information about the outside world can be recovered. Certain neurons in the dorsal part of monkey medial superior temporal area (MSTd) play an important role in integrating information about eye movements and visual motion. When a monkey tracks a moving target with its eyes, these neurons respond to visual motion as well as to smooth pursuit eye movements. Furthermore, the responses of some MSTd neurons to the motion of objects in the world are very similar during pursuit and during fixation, even though the visual information on the retina is altered by the pursuit eye movement. We call these neurons compensatory pursuit neurons. In this study we develop a computational model of MSTd compensatory pursuit neurons based on physiological data from single unit studies. Our model MSTd neurons can simulate the velocity tuning of monkey MSTd neurons. The model MSTd neurons also show the pursuit compensation property. We find that pursuit compensation can be achieved by divisive interaction between signals coding eye movements and signals coding visual motion. The model generates two implications that can be tested in future experiments: (1) compensatory pursuit neurons in MSTd should have the same direction preference for pursuit and retinal visual motion; (2) there should be non-compensatory pursuit neurons that show opposite preferred directions of pursuit and retinal visual motion.     

Visual response properties of neck motor neurons in the honeybee

Recent behavioural studies have demonstrated that honeybees use visual feedback to stabilize their gaze. However, little is known about the neural circuits that perform the visual motor computations that underlie this ability. We investigated the motor neurons that innervate two neck muscles (m44 and m51), which produce stabilizing yaw movements of the head. Intracellular recordings were made from five (out of eight) identified neuron types in the first cervical nerve (IK1) of honeybees. Two motor neurons that innervate muscle 51 were found to be direction-selective, with a preference for horizontal image motion from the contralateral to the ipsilateral side of the head. Three neurons that innervate muscle 44 were tuned to detect motion in the opposite direction (from ipsilateral to contralateral). These cells were binocularly sensitive and responded optimally to frontal stimulation. By combining the directional tuning of the motor neurons in an opponent manner, the neck motor system would be able to mediate reflexive optomotor head turns in the direction of image motion, thus stabilising the retinal image. When the dorsal ocelli were covered, the spontaneous activity of neck motor neurons increased and visual responses were modified, suggesting an ocellar input in addition to that from the compound eyes.     

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.     

Hawk Eyes II: Diurnal Raptors Differ in Head Movement Strategies When Scanning from Perches

Background

Relatively little is known about the degree of inter-specific variability in visual scanning strategies in species with laterally placed eyes (e.g., birds). This is relevant because many species detect prey while perching; therefore, head movement behavior may be an indicator of prey detection rate, a central parameter in foraging models. We studied head movement strategies in three diurnal raptors belonging to the Accipitridae and Falconidae families.

Methodology/Principal Findings

We used behavioral recording of individuals under field and captive conditions to calculate the rate of two types of head movements and the interval between consecutive head movements. Cooper''s Hawks had the highest rate of regular head movements, which can facilitate tracking prey items in the visually cluttered environment they inhabit (e.g., forested habitats). On the other hand, Red-tailed Hawks showed long intervals between consecutive head movements, which is consistent with prey searching in less visually obstructed environments (e.g., open habitats) and with detecting prey movement from a distance with their central foveae. Finally, American Kestrels have the highest rates of translational head movements (vertical or frontal displacements of the head keeping the bill in the same direction), which have been associated with depth perception through motion parallax. Higher translational head movement rates may be a strategy to compensate for the reduced degree of eye movement of this species.

Conclusions

Cooper''s Hawks, Red-tailed Hawks, and American Kestrels use both regular and translational head movements, but to different extents. We conclude that these diurnal raptors have species-specific strategies to gather visual information while perching. These strategies may optimize prey search and detection with different visual systems in habitat types with different degrees of visual obstruction.