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The Vertebrate Eye and Its Adaptive Radiation.

Head kinematics were studied in ten normal subjects while they executed various locomotor tasks The movement of the body was recorded with a video system which allowed a computer reconstruction of motion of joint articulations and other selected points on the body in three dimensions Analyses focus on head translation along the vertical axis and rotation in the sagittal plane This was done by recording the displacement of a line approximating the plane of horizontal semi-circular canals (the Frankfort plane: F-P) Four conditions were studied: free walking (W) walking in place (WIP) running in place (R) and hopping (H) In the 4 experimental conditions, amplitude and velocity of head translation along the vertical axis ranged from 1 cm to 25 cm and 015 m/s to 18 m/s In spite of the disparities in the tasks regarding the magnitude of dynamic components, we found a significant stabilization of the F-P around the earth horizontal Maximum amplitude of F-P rotation did not exceed 20° in the 4 situations Vertical angular velocities increased from locomotion tasks to the dynamic equilibrium task although the maximum values remained less than 140°/s Predominant frequencies of translations and rotations in all the tasks were within the range 04–35 Hz and harmonics were present up to 6–8 Hz During walking in darkness, mean head position is tilted downward, with the F-P always below the earth horizontal Darkness did not significantly influence the amplitude and velocity of head angular displacement during W, WIP and R, but during H the amplitude decreased by 37% Residual head angular displacement is found to compensate for head translation during the 4 conditions Our study emphasizes the importance of head stabilization as part of the postural control system and described as a basis for inertial guidance

Head stabilization during various locomotor tasks in humans. I. Normal subjects.

The optic tectum is the largest visual center in most vertebrates and the main target for retinal ganglion cells (RGCs) conveying visual information from the eye to the brain. The retinotectal projection has served as an important model in many areas of developmental neuroscience. However, knowledge of the function of the tectum is limited. We began to address this issue using laser ablations and subsequent behavioral testing in zebrafish. We used a transgenic zebrafish line that expresses green-fluorescent protein in RGCs projecting to the tectum. By aiming a laser beam at the labeled retinal fibers demarcating the tectal neuropil, the larval tectum could be selectively destroyed. We tested whether tectum-ablated zebrafish larvae, when presented with large-field movements in their surroundings, displayed optokinetic responses (OKR) or optomotor responses (OMR), two distinct visuomotor behaviors that compensate for self-motion. Neither OKR nor OMR were found to be dependent on intact retinotectal connections. Also, visual acuity remained unaffected. Tectum ablation, however, slowed down the OKR by reducing the frequency of saccades but left tracking velocity, gain, and saccade amplitude unaffected. Removal of the tectum had no effect on the processing of second-order motion, to which zebrafish show both OKR and OMR, suggesting that the tectum is not an integral part of the circuit that extracts higher-order cues in the motion pathway.

https://www.jneurosci.org/content/jneuro/23/9/3726.full.pdf

Visuomotor Behaviors in Larval Zebrafish after GFP-Guided Laser Ablation of the Optic Tectum

This article sets out to present a fairly comprehensive review of our knowledge about the functions of the receptors that have been found in the extraocular muscles--the six muscles that move each eye of vertebrates in its orbit--of all the animals in which they have been sought, including Man. Since their discovery at the beginning of the 20th century these receptors have, at various times, been credited with important roles in the control of eye movement and the construction of extrapersonal space and have also been denied any function whatsoever. Experiments intended to study the actions of eye muscle receptors and, even more so, opinions (and indeed polemic) derived from these observations have been influenced by the changing fashions and beliefs about the more general question of how limb position and movement is detected by the brain and which signals contribute to those aspects of this that are perceived (kinaesthesis). But the conclusions drawn from studies on the eye have also influenced beliefs about the mechanisms of kinaesthesis and, arguably, this influence has been even larger than that in the converse direction. Experimental evidence accumulated over rather more than a century is set out and discussed. It supports the view that, at the beginning of the 21st century, there are excellent grounds for believing that the receptors in the extraocular muscles are indeed proprioceptors, that is to say that the signals that they send into the brain are used to provide information about the position and movement of the eye in the orbit. It seems that this information is important in the control of eye movements of at least some types, and in the determination by the brain of the direction of gaze and the relationship of the organism to its environment. In addition, signals from these receptors in the eye muscles are seen to be necessary for the development of normal mechanisms of visual analysis in the mammalian visual cortex and for both the development and maintenance of normal visuomotor behaviour. Man is among those vertebrates to whose brains eye muscle proprioceptive signals provide information apparently used in normal sensorimotor functions; these include various aspects of perception, and of the control of eye movement. It is possible that abnormalities of the eye muscle proprioceptors and their signals may play a part in the genesis of some types of human squint (strabismus); conversely studies of patients with squint in the course of their surgical or pharmacological treatment have yielded much interesting evidence about the central actions of the proprioceptive signals from the extraocular muscles. The results of experiments on the eye have played a large part in the historical controversy, now in at least its third century, about the origin of signals that inform the brain about movement of parts of the body. Some of these results, and more of the interpretations of them, now need to be critically re-examined. The re-examination in the light of recent experiments that is presented here does not support many of the conclusions confidently drawn in the past and leads to both new insights and fresh questions about the roles of information from motor signals flowing out of the brain and that from signals from the peripheral receptors flowing into it. There remain many lacunae in our knowledge and filling some of these will, it is contended, be essential to advance our understanding further. It is argued that such understanding of eye muscle proprioception is a necessary part of the understanding of the physiology and pathophysiology of eye movement control and that it is also essential to an account of how organisms, including Man, build and maintain knowledge of their relationship to the external visual world. The eye would seem to provide a uniquely favourable system in which to study the way in which information derived within the brain about motor actions may interact with signals flowing in from peripheral receptors. The review is constructed in relatively independent sections that deal with particular topics. It ends with a fairly brief piece in which the author sets out some personal views about what has been achieved recently and what most immediately needs to be done. It also suggests some lines of study that appear to the author to be important for the future.

The functions of the proprioceptors of the eye muscles.

We quantitatively studied the ontogeny of oculomotor behavior in larval fish as a foundation for studies linking oculomotor structure and function with genetics. Horizontal optokinetic and vestibul...

https://www.physiology.org/doi/pdf/10.1152/jn.00311.2004

Quantifying the Ontogeny of Optokinetic and Vestibuloocular Behaviors in Zebrafish, Medaka, and Goldfish

A quantitative study of horizontal and vertical optokinetic nystagmus (OKN) and optocollic reflex (OCR) has been performed in the pigeon using the search-coil technique. The reflexes were analysed in response to either velocity steps or sinusoidal stimulation. Results show that: 1. In response to a velocity step stimulation, the slow phase velocity of both OKN and OCR increases gradually to reach a steady state level. When the stimulation stops in the dark, After Responses (OKAN-I, OKAR-I) occur. Time constants of the OKN charge (or OCR charge) and of the After Responses are lower for vertical than for horizontal responses. 2. In the free-head condition, both the head and the eye display a synchronized nystagmus which add their effects. However, the head reflex (OCR) accounts for about 80–90% of the entire linear gaze response (head + eye), except for the vertical steady state responses which are wholly accomplished by the head (OCR). 3. Both closed-loop and open-loop gains of steady state responses are higher for horizontal than for vertical reflexes. Vertical OCR, horizontal OKN and vertical OKN show properties of binocular integration, the response gain being higher for binocular than for monocular stimulations. By contrast, the horizontal OCR shows little binocular integration but displays a higher response gain for monocular stimulation, compared to horizontal OKN. 4. The horizontal OKN elicited by both monocular and binocular stimulation is asymmetrical, the gain being higher when the eye is driven by a temporo-nasal stimulation. In contrast, both vertical OKN and vertical OCR are practically symmetrical. 5. While both the gain of horizontal OKN and its linear range (up to 20°/s) are improved when the head is free (gaze gain close to 1 up to 40°/s), the vertical OKN and the vertical OCR have similar gain profiles and similar domains of linearity (up to 10°/s). 6. In response to increasing the frequency of a sinusoidal stimulation at constant peak velocity, all the reflexes display a drop in gain and a strong increase of phase lag. The phase increase is greater for horizontal than for vertical reflexes. On the other hand, both gain and phase are higher for OCR than for OKN, both in the horizontal plane as well as in the vertical plane. 7. For sinusoidal stimulations, when the peak velocity (PV) is increased at a constant frequency (0.03 Hz), nonlinearities appear (drop in gain, phase increase) both for OKN and OCR. While the most important parameter which determines the phase is the stimulation frequency, both peak velocity and peak acceleration are involved in the gain saturation.

Stabilizing gaze reflexes in the pigeon (Columba livia)

In birds, the accessory optic system (AOS) includes two nuclei: the nucleus ectomamillaris (nEM) and the pretectal nucleus superficialis synencephali (nSS) The role of the nSS in the production of a horizontal optokinetic nystagmus (OKN) was studied in the pigeon, by comparing the OKN before and after a unilateral lesion of this nucleus The lesions were performed either by electrolysis or by local application of kainic acid (KA); the KA lesions gave more stable modifications of the OKN than the electrolytic lesions A quantitative analysis of the slow-phase velocity (¯V) of the OKN was carried out on the animals receiving KA lesions

(1)

Lesion of the nSS provokes the almost total disappearance of the OKN for stimulation of the contralateral eye in the temporo-nasal direction, and a reduction of the OKN for stimulation in the nasotemporal direction Thus, the nSS is essential for the production of the OKN in the temporo-nasal direction, but it also participates in the production of the OKN in the naso-temporal direction (slow-phase direction)




(2)

The same lesion produces a large increase of the OKN (¯V) when the ipsilateral eye is stimulated in the temporo-nasal direction, and a smaller increase following stimulation in the naso-temporal direction These increases suggest some kind of inhibitory (or disfacilitatory) interactions between the nSS (or the associated system) on one side, and the contralateral optokinetic centers




(3)

The lesion of one nSS does not provoke a deficit when the stimulation is binocular This result probably reflects the combined effect of both monocular inputs




(4)

After a pretectal KA injection, a spontaneous nystagmus of the contralateral eye, in the nasotemporal direction, can be seen for several hours The mechanism is still unknown, but it might be rela2ted to a reverse optokinetic after nystagmus (ROKAN)

Optokinetic nystagmus in the pigeon (Columba livia): II. Role of the pretectal nucleus of the accessory optic system (AOS).

Extracellular recordings were performed in the nucleus of the basal optic root (nBOR) of alert pigeons during optokinetic nystagmus (OKN), vestibulo-ocular reflex (VOR) and combined visuo-vestibular stimulation. Cell identification was assessed either by histological control or by electrophysiological testing (antidromic response to vestibulo-cerebellar or oculomotor complex stimulation). 1) OKN was induced in 8 directions by a binocular stimulation. During the fast phase of OKN, optokinetic after nystagmus (OKAN) or reversed OKAN, most cells showed an inhibition which varied in magnitude independent of the direction of stimulation. A few cells however showed a phasic discharge for some OKN directions. 2) During the slow phase of OKN induced by a binocular stimulation, cells displayed either a tonic activation or a more or less strong inhibition according to the direction of the OKN. Cells were classified in 4 groups, according to their degree of directional specificity. The best OKN direction (slow phase) for maximal cell activation was upwards and naso-upwards, and next to best, nasotemporal and downwards. Maximal cell inhibition occurred during downward, and for some cells during upward, directions. 3) During OKN induced by stimulating the eye contralateral to the recorded nBOR, cell responses resembled those obtained during binocular stimulation, but, during ipsilaterally induced OKN, the cells lost their directional specificity. As a result of binocular integration, neuronal activation seems to originate from contralateral input whereas cell inhibition would mainly come from ipsilateral input. 4) During sinusoidal optokinetic stimulation induced in the temporo downward-naso upward axis, cells showed a more or less marked modulation (according to their directional selectivity) that was closely in phase with the stimulation velocity, and therefore probably with retinal slip. 5) nBOR cells appeared generally unaffected during both the slow phase and the fast phase of the VOR. However, some cells showed a slight but irregular modulation which might imply a weak vestibular input. During visuo-vestibular stimulation, the response resembled that obtained with sinusoidal optokinetic stimulation but the fast phase inhibition was often strengthened in the downwards direction (fast phase).

Single unit activity in the nucleus of the basal optic root (nBOR) during optokinetic, vestibular and visuo-vestibular stimulations in the alert pigeon (Columbia livia)

A study of optokinetic nystagmus (OKN) as produced by monocular or binocular stimulation was carried out in the pigeon. Nystagmus was provoked by constant speed rotation (13 or 36 °/s) of an optokinetic drum lined with alternate black and white vertical stripes. With the animal's head immobilized, the electro-oculogram of each eye was recorded for both directions of rotation.

I.

Depending on the response to monocular stimulation, the animals were put into three categories: (1) no nystagmus was detected in either eye, (2) nystagmus was found in the stimulated eye only, (3) both eyes displayed nystagmus. Moreover, the percentage of responses was greater for temporal to nasal (T-N) stimulation than for nasal to temporal (N-T) stimulation.




II.

Computer analysis performed in the last group of animals showed that: (1) In monocular stimulation: (a) OKN of the stimulated eye was asymmetrical, that is, the frequency, amplitude and average slow-phase velocity (¯V) of the nystagmus beats were higher in T-N (preferential direction) stimulation. (b) OKN of the masked eye was symmetrical. (c) OKN of the two eyes was conjugate, but the amplitude and velocity (¯V) were greater in the stimulated eye, this difference being more noticeable in the T-N direction than for the N-T one. (2) In binocular stimulation the monocular effects were partially summated and OKN remained asymmetrical, with a higher amplitude for the T-N stimulated eye.




III.

OKN was followed by optokinetic after-nystagmus (OKAN) for short durations of stimulation, and by reverse optokinetic after-nystagmus (R-OKAN) for longer durations of stimulation. In both monocular and binocular stimulation the nystagmus response (OKN, OKAN and R-OKAN) was conjugate, but always larger in the eye moving in the T-N direction (slow phase).

Optokinetic nystagmus in the pigeon (Columba livia). I. Study in monocular and binocular vision.

The accessory optic system (AOS) in birds is composed of two structures: the nucleus Superficialis Synencephali (nSS), essential for the production of an optokinetic nystagmus (OKN) in the temporo-nasal direction (slow phase) for the eye contralateral to the nucleus, and the nucleus Ectomamillaris (nEM), or nucleus of the basal optic root (nBOR). The objectives of the present work were: (1) to study the importance of the nEM for the horizontal OKN, (2) to study the interactions between the nSS and the nEM. Experiments were realized by combining different kinds of lesion.
 The role of the nuclei of the AOS in birds is discussed in terms of existing anatomical and physiological data.

H. Gioanni

Papers

Stabilizing gaze reflexes in the pigeon (Columba livia)

Optokinetic nystagmus in the pigeon (Columba livia): II. Role of the pretectal nucleus of the accessory optic system (AOS).

Single unit activity in the nucleus of the basal optic root (nBOR) during optokinetic, vestibular and visuo-vestibular stimulations in the alert pigeon (Columbia livia)

Optokinetic nystagmus in the pigeon (Columba livia). I. Study in monocular and binocular vision.

Optokinetic nystagmus in the pigeon (Columba livia) III. Role of the nucleus ectomamillaris (nEM): Interactions in the accessory optic system (AOS)