A model for optokinetic eye movements in turtles that incorporates properties of retinal-slip neurons

AbstractThe turtle's optokinetic response is described by a simple model that incorporates visual-response properties of neurons in the pretectum and accessory optic system. Using data from neuronal and eye-movement recordings that have been previously published, the model was realized using algebraic-block simulation software. It was found that the optokinetic response, modelled as a simple negative feedback system, was similar to that measured from a behaving animal. Because the responses of retinal-slip detecting neurons corresponded to the nonlinear, closed-loop optokinetic response, it was concluded that the visual signals encoded in these neurons could provide sufficient sensory information to drive the optokinetic reflex. Furthermore, it appears that the low gain of optokinetic eye movements in turtles, which have a negligible velocity storage time constant, may allow stable oculomotor output in spite of neuronal delays in the reflex pathway. This model illustrates how visual neurons in the pretectum and accessory optic system can contribute to visually guided eye movements.

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The interstitial nucleus of the superior fasciculus, posterior bundle (INSFp) in the guinea pig: Another nucleus of the accessory optic system processing the vertical retinal slip signal

Visual Neuroscience ◽

10.1017/s0952523800002182 ◽

1989 ◽

Vol 2 (4) ◽

pp. 377-382 ◽

Cited By ~ 10

Author(s):

C. Benassi ◽

G. P. Biral ◽

F. Lui ◽

C. A. Porro ◽

R. Corazza

Keyword(s):

Guinea Pig ◽

Optokinetic Nystagmus ◽

Vertical Direction ◽

Luminous Flux ◽

Visual Signals ◽

Optic System ◽

Accessory Optic System ◽

Retinal Slip ◽

Visual Patterns ◽

Medial Terminal Nucleus

AbstractAs in rabbit, gerbil, and rat, the guinea pig interstitial nucleus of the superior fasciculus, posterior bundle (INSFp) is a sparse assemblage of neurons scattered among the fibers forming the fasciculus bearing this name. Most of the INSFp neurons are small and are ovoid in shape. Interspersed among these, are a few larger, elongated neurons whose density becomes greater and whose shape becomes fusiform in correspondence to the zone of transition from the superior fasciculus to the ventral part of the medial terminal nucleus (MTN). Like the MTN, the INSFp is activated by retinal-slip signals evoked by whole-field visual patterns moving in the vertical direction, as shown by the increase of 14C-2-deoxyglucose (2DG) uptake into this nucleus. At the same level of luminous flux, neither pattern moving in the horizontal direction nor the same pattern held stationary can elicit increases in the INSFp 2DG assumption. The specificity of the observed increases in metabolic rates in INSFp following vertical whole-field motion suggests that this assemblage of neurons relays visual signals used in the control of vertical optokinetic nystagmus.

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Temporal Frequency and Velocity-Like Tuning in the Pigeon Accessory Optic System

Journal of Neurophysiology ◽

10.1152/jn.00654.2002 ◽

2003 ◽

Vol 90 (3) ◽

pp. 1829-1841 ◽

Cited By ~ 26

Author(s):

Nathan A. Crowder ◽

Michael R.W. Dawson ◽

Douglas R.W. Wylie

Keyword(s):

Motion Detection ◽

Temporal Frequency ◽

Sine Wave ◽

Direction Selectivity ◽

Large Field ◽

Apparent Velocity ◽

Correlation Model ◽

Optic System ◽

Accessory Optic System ◽

Optokinetic Response

Neurons in the accessory optic system (AOS) and pretectum are involved in the analysis of optic flow and the generation of the optokinetic response. Previous studies found that neurons in the pretectum and AOS exhibit direction selectivity in response to large-field motion and are tuned in the spatiotemporal domain. Furthermore, it has been emphasized that pretectal and AOS neurons are tuned to a particular temporal frequency, consistent with the “correlation” model of motion detection. We examined the responses of neurons in the nucleus of the basal optic root (nBOR) of the AOS in pigeons to large-field drifting sine wave gratings of varying spatial (SF) and temporal frequencies (TF). nBOR neurons clustered into two categories: “Fast” neurons preferred low SFs and high TFs, and “Slow” neurons preferred high SFs and low TFs. The fast neurons were tuned for TF, but the slow nBOR neurons had spatiotemporally oriented peaks that suggested velocity tuning (TF/SF). However, the peak response was not independent of SF; thus we refer to the tuning as “apparent velocity tuning” or “velocity-like tuning.” Some neurons showed peaks in both the fast and slow regions. These neurons were TF-tuned at low SFs, and showed velocity-like tuning at high SFs. We used computer simulations of the response of an elaborated Reichardt detector to show that both the TF-tuning and velocity-like tuning shown by the fast and slow neurons, respectively, may be explained by modified versions of the correlation model of motion detection.

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The accessory optic system of rabbit. I. Basic visual response properties

Journal of Neurophysiology ◽

10.1152/jn.1988.60.6.2037 ◽

1988 ◽

Vol 60 (6) ◽

pp. 2037-2054 ◽

Cited By ~ 122

Author(s):

R. E. Soodak ◽

J. I. Simpson

Keyword(s):

Ganglion Cells ◽

Receptive Fields ◽

Extracellular Recording ◽

Vestibular Stimulation ◽

Visual Response ◽

Optic System ◽

Accessory Optic System ◽

Response Properties ◽

Tuning Curves ◽

Sinusoidal Oscillations

1. The response properties of accessory optic system (AOS) neurons were assessed using single-unit extracellular recording from each of the three AOS terminal nuclei [medial, lateral, and dorsal terminal nuclei (MTN, LTN, and DTN)] in the anesthetized rabbit. 2. AOS neurons had large, monocular (contralateral) receptive fields (tens of degrees on a side) and exhibited a pronounced selectivity to the speed and direction of movement of large, textured patterns. The greatest responses occurred at slow speeds on the order of 0.5 degrees/s. 3. MTN and LTN neurons responded best to movement in near vertical directions. However, the stimulus directions corresponding to the greatest excitation and the greatest inhibition both had a posterior component and, thus, the preferred excitatory and inhibitory directions were not opposite each other. DTN neurons responded most strongly to horizontal movement and were excited by temporal to nasal movement. 4. AOS neurons were unresponsive to natural vestibular stimulation presented as sinusoidal oscillations of the rabbit about the yaw, pitch, and roll axes. 5. The response properties of AOS neurons are remarkably similar to those of the ON, direction-selective ganglion cells of the rabbit retina, and therefore this class of ganglion cell is most likely the predominant, if not the only, direct retinal input to the AOS. The local direction-selective properties of AOS neurons can be accounted for by combining the tuning curves of ON, direction-selective ganglion cells in a simple manner. 6. The low speed preference of AOS neurons, along with their large receptive fields suggests that they are suited to complement the vestibular system in detecting self-motion.

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Role of the pretectum and accessory optic system in pursuit eye movements of the monkey

Multisensory Control of Movement ◽

10.1093/acprof:oso/9780198547853.003.0049 ◽

1993 ◽

pp. 93-111

Author(s):

Klaus-Peter Hoffmann ◽

Uwe Ilg

Keyword(s):

Eye Movements ◽

Optic System ◽

Accessory Optic System ◽

Pursuit Eye Movements

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Independent eye movements in the turtle

Visual Neuroscience ◽

10.1017/s0952523800000055 ◽

1990 ◽

Vol 5 (1) ◽

pp. 29-41 ◽

Cited By ~ 12

Author(s):

M. Ariel

Keyword(s):

Eye Movements ◽

Optokinetic Nystagmus ◽

Contact Lenses ◽

The Other ◽

Slow Phase ◽

Accessory Optic System ◽

Retinal Slip ◽

The Mean ◽

The Difference ◽

Eye Velocity

AbstractIn order to evaluate the normal eye movements of the turtle, Pseudemys scripta elegans, the positions of each eye were recorded simultaneously using two search-coil contact lenses. Optokinetic nystagmus (OKN) was strikingly unyoked in this animal such that one eye's slow-phase velocity was substantially independent of that of the other eye. On the other hand, the fast-phase motions of both eyes occurred more or less in synchrony.An eye's slow-phase gain is primarily dependent on the direction and velocity of the stimulus to that eye. Using monocular stimuli, the highest mean gain (0.54 ± 0.047; mean ± standard error of mean) occurred using temporal-to-nasal movement at 2.5 deg/s. The mean OKN gain for nasal-to-temporal movement was only 0.13 ± 0.015 at that velocity. Additionally, using the optimal monocular stimulus (temporal-to-nasal stimulation at 2.5 deg/s) only drove the occluded eye to move nasal-to-temporally at 0.085 deg/s, equivalent to a “gain” of only 0.034 ± 0.011.The binocular OKN gain during rotational stimuli was higher than monocular gain, especially during nasal-to-temporal movement at high velocities. Also the difference in slow-phase eye velocity between the two eyes was smaller during binocular rotational stimuli. In contrast, when each eye simultaneously viewed its temporal-to-nasal stimulus at an equal velocity, two behaviors were observed. Often, OKN alternated between an animal's left eye and right eye. Occasionally, both eyes moved at equal but opposite velocities.These behavioral data provide a quantitative baseline to interpret the properties of the retinal slip information in the turtle's accessory optic system. Those properties are similar to the behavior of the turtle in that both are tuned to direction and velocity independently for each eye (Rosenberg & Ariel, 1990).

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Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate

Journal of Neurophysiology ◽

10.1152/jn.1989.61.6.1207 ◽

1989 ◽

Vol 61 (6) ◽

pp. 1207-1220 ◽

Cited By ~ 56

Author(s):

M. J. Mustari ◽

A. F. Fuchs

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Smooth Pursuit ◽

Large Field ◽

Smooth Pursuit Eye Movements ◽

Optic System ◽

Accessory Optic System ◽

Stimulus Velocity ◽

Firing Rates ◽

Pursuit Eye Movements

1. To determine the potential role of the primate accessory optic system (AOS) in optokinetic and smooth-pursuit eye movements, we recorded the activity of 110 single units in a subdivision of the AOS, the lateral terminal nucleus (LTN), in five alert rhesus macaques. All monkeys were trained to fixate a stationary target spot during visual testing and to track a small spot moving in a variety of visual environments. 2. LTN units formed a continuum of types ranging from purely visual to purely oculomotor. Visual units (50%) responded best for large-field (70 x 50 degrees), moving visual stimuli and had no response associated with smooth-pursuit eye movement; some responded during smooth pursuit in the dark, but the response disappeared if the target was briefly extinguished, indicating that their smooth-pursuit-related response reflected activation of a parafoveal receptive field. Eye movement and visual units (36%) responded both for large, moving visual stimuli and during smooth-pursuit eye movements made in the dark. Eye movement units (14%) discharged during smooth-pursuit or other eye movements but showed no evidence of visual sensitivity. 3. Essentially all (98%) LTN units were direction selective, responding preferentially during vertical background and/or smooth-pursuit movement. The vast majority (88%) preferred upward background and/or eye movement. During periodic movement of the large-field visual background while the animal fixated, their firing rates were modulated above and below rather high resting rates. Although LTN units typically responded best to movement of large-field stimuli, some also responded well to small moving stimuli (0.25 degrees diam). 4. LTN units could be separated into two populations according to their dependence on visual stimulus velocity. For periodic triangle wave stimuli, both types had velocity thresholds less than 3 degrees/s. As stimulus velocity increased above threshold, the activity of one type reached peak firing rates over a very narrow velocity range and remained nearly at peak firing for velocities from approximately 4-80 degrees/s. The firing rates of the other type exhibited velocity tuning in which the firing rate peaked at an average preferred velocity of 13 degrees/s and decreased for higher velocities. 5. A close examination of firing rates to sinusoidal background stimuli revealed that both unit types exhibited unusual behaviors at the extremes of stimulus velocity.(ABSTRACT TRUNCATED AT 400 WORDS)

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Response Properties of Optic Flow Neurons in the Accessory Optic System of Hummingbirds vs. Zebra Finches and Pigeons

Journal of Neurophysiology ◽

10.1152/jn.00437.2021 ◽

2021 ◽

Author(s):

Andrea H Gaede ◽

Vikram B Baliga ◽

Graham Smyth ◽

Cristian Gutiérrez-Ibáñez ◽

Douglas Leonard Altshuler ◽

...

Keyword(s):

Optic Flow ◽

Receptive Fields ◽

Bird Species ◽

Visual Response ◽

Zebra Finches ◽

Optic System ◽

Accessory Optic System ◽

Stimulus Velocity ◽

Response Properties ◽

Optokinetic Responses

Optokinetic responses function to maintain retinal image stabilization by minimizing optic flow that occurs during self-motion. The hovering ability of hummingbirds is an extreme example of this behaviour. Optokinetic responses are mediated by direction-selective neurons with large receptive fields in the accessory optic system (AOS) and pretectum. Recent studies in hummingbirds showed that, compared to other bird species, (i) the pretectal nucleus lentiformis mesencephali (LM) is hypertrophied, (ii) LM has a unique distribution of direction preferences, and (iii) LM neurons are more tightly tuned to stimulus velocity. In this study, we sought to determine if there are concomitant changes in the nucleus of the basal optic root (nBOR) of the AOS. We recorded the visual response properties of nBOR neurons to largefield drifting random dot patterns and sine wave gratings in Anna's hummingbirds and zebra finches and compared these with archival data from pigeons. We found no differences with respect to the distribution of direction preferences: Neurons responsive to upwards, downwards and nasal-to-temporal motion were equally represented in all three species, and neurons responsive to temporal-to-nasal motion were rare or absent (<5%). Compared to zebra finches and pigeons, however, hummingbird nBOR neurons were more tightly tuned to stimulus velocity of random dot stimuli. Moreover, in response to drifting gratings, hummingbird nBOR neurons are more tightly tuned in the spatio-temporal domain. These results, in combination with specialization in LM, supports a hypothesis that hummingbirds have evolved to be "optic flow specialist" to cope with the optomotor demands of sustained hovering flight.

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