Optokinetic response

Horizontal optokinetic nystagmus.

The optokinetic reflex (OKR), also referred to as the optokinetic response, or optokinetic nystagmus (OKN), is a compensatory reflex that supports visual image stabilization.[1] The purpose of OKR is to prevent motion blur on the retina that would otherwise occur when an animal moves its head or navigates through its environment. This is achieved by the reflexive movement of the eyes in the same direction as image motion, so as to minimize the relative motion of the visual scene on the eye. OKR is best evoked by slow, rotational motion, and operates in coordination with several complementary reflexes that also support image stabilization, including the vestibulo-ocular reflex (VOR).

Characteristics of OKR

Eliciting OKR

OKR is typically evoked by presenting full field visual motion to a subject. The optokinetic drum is a common clinic tool used for this purpose. The drum most commonly contains sinusoidal or square-wave stripes that move across the subject's field of view to elicit strong optokinetic eye movements. However, nearly any moving texture evokes OKR in mammals. Outside of laboratory settings, OKR is strongly evoked by natural image motion, including when looking out the side window of a moving vehicle.

Eye movement patterns

When viewing constant, unidirectional motion, OKR consists of a stereotyped "sawtooth" waveform that represents two types of eye movements. During slow nystagmus, the eyes smoothly follow the direction of the stimulus. Though slow nystagmus closely resembles smooth pursuit eye movements, it is distinct; several species that do not exhibit smooth pursuit nonetheless have slow nystagmus during OKR (though in humans, it is possible to substitute slow nystagmus for smooth pursuit during a version of OKR referred to as "look nystagmus", in which subjects are specifically instructed to track the moving stimuli[2]). Fast nystagmus is the second constituent eye movement in OKR. It consists of a rapid, resetting saccade in the opposite direction of the slow nystagmus (i.e., opposite to the stimulus motion). The purpose of the fast nystagmus is to keep the eye centered in the orbit, while the purpose of the slow nystagmus is to stabilize the moving visual scene on the retina.

Comparative biology

OKR is one of the best preserved behaviors in the animal kingdom. It has been identified in insects, invertebrates, reptiles, amphibians, birds, fish, and all mammals.[3] There are subtle differences in how OKR plays out across species. For instance, in fruit flies, individual segments of the compound eye move in response to image motion,[4] whereas in mammals and several other species the entire eye moves together. In addition, OKR patterns vary across species according to whether stimuli are presented monocularly or binocularly: in most species monocular presentation of stimuli results in asymmetric responses, with stimuli moving in the nasal-to-temporal direction resulting in larger responses than stimuli moving in the temporal-to-nasal direction. In humans, this asymmetry is seen only in infants, and monocular OKR becomes symmetric by six months of age because of cortical development.[3] In several species, OKR is also more reliably evoked by upward motion than by downward motion.[5][6][7] Both vertical and horizontal asymmetries are often attributed to functional adaptations that reflect common natural scene statistics associated with forward terrestrial locomotion.

Neural mechanisms

OKR is driven by a dedicated visual pathway called the accessory optic system (AOS).[8]

Retina

The AOS begins in the retina with a specialized class of retinal ganglion cell known as ON direction selective retinal ganglion cells (oDSGCs). These cells respond selectively to motion in one of three cardinal directions (upward, downward, or nasal motion),[9][10] and inherit their direction selectivity at least partially from asymmetric inhibition from starburst amacrine cells.[11] Glycinergic inhibition produces a speed tuning preference for slow stimulus motion in oDSGCs,[12][13] which has been used to explain the analogous slow tuning of OKR.[14] In some species, oDSGCs constitute the displaced ganglion cells, whose cell bodies reside in the inner nuclear layer of the retina. oDSGCs that respond to different directions of motion have slightly different response properties that are also reflected in OKR behavior, and it is thought that a linear subtraction of oDSGC spikes may predict the magnitude of the OKR slow phase.[7]

Midbrain

oDSGC axons do not target common visual structures. Instead, they are likely the only retinal ganglion cell type to innervate the three midbrain nuclei of the AOS:[8] the nucleus of the optic tract (NOT), the lateral terminal nucleus (LTN), and the medial terminal nucleus (MTN). These nuclei are targeted by oDSGCs that prefer nasal, downward, and upward image motion, respectively. Recurrent inhibitory connections exist between these AOS nuclei, further suggesting a subtraction of signals between different oDSGC types. There are only modest connections between these nuclei and the cortex. The activity of neurons in the AOS nuclei are well-correlated with the velocity of the OKR slow phase.

Oculomotor plant

The projection neurons of the NOT, LTN, and MTN converge on the oculomotor plant in the brainstem, where their activity is integrated to drive the eye movements. This occurs through Cranial Nerves III, IV, and VI, and their associated brainstem nuclei.

Plasticity

Potentiation of the OKR slow phase is known to occur after long periods of continuous stimulation. These mechanisms are cerebellar-dependent, and may be associated with corresponding changes to the VOR.

Scientific and medical interest

The reflexive nature of OKR has made it a popular method for objectively measuring vision in many contexts. OKR-based tests have been developed to objectively assess visual acuity, color vision, stereopsis and more.[15][16][17] Changes to the stereotypical OKR waveform can also be a biomarker of disease, including stroke, concussion, drug or alcohol intoxication, and parkinsonism.[18] OKR is also commonly used in basic science as an objective measure of acuity in animal disease models.

In neurobiology, the isolation of the AOS from other visual pathways, its clear connection to a behavioral readout in the form of OKR, and its conservation across species make it an attractive model system to study. The AOS has been used to understand molecular mechanisms of synapse formation, feature tuning and direction selectivity in the retina, neural circuit development, axon targeting, plasticity mechanisms, and computational strategies for integrating primary sensory information.[19][20][21][22]

See also

References

  1. ^ Simpson, J I (March 1984). "The Accessory Optic System". Annual Review of Neuroscience. 7 (1): 13–41. doi:10.1146/annurev.ne.07.030184.000305. ISSN 0147-006X. PMID 6370078.
  2. ^ Knapp, Christopher M.; Gottlob, Irene; McLean, Rebecca J.; Proudlock, Frank A. (2008-02-01). "Horizontal and Vertical Look and Stare Optokinetic Nystagmus Symmetry in Healthy Adult Volunteers". Investigative Ophthalmology & Visual Science. 49 (2): 581–588. doi:10.1167/iovs.07-0773. ISSN 1552-5783. PMID 18235002.
  3. ^ a b Masseck, Olivia Andrea; Hoffmann, Klaus-Peter (May 2009). "Comparative Neurobiology of the Optokinetic Reflex". Annals of the New York Academy of Sciences. 1164 (1): 430–439. Bibcode:2009NYASA1164..430M. doi:10.1111/j.1749-6632.2009.03854.x. ISSN 0077-8923. PMID 19645943. S2CID 34185107.
  4. ^ Fenk, Lisa M.; Avritzer, Sofia C.; Weisman, Jazz L.; Nair, Aditya; Randt, Lucas D.; Mohren, Thomas L.; Siwanowicz, Igor; Maimon, Gaby (2022-12-01). "Muscles that move the retina augment compound eye vision in Drosophila". Nature. 612 (7938): 116–122. Bibcode:2022Natur.612..116F. doi:10.1038/s41586-022-05317-5. ISSN 0028-0836. PMC 10103069. PMID 36289333.
  5. ^ Hoffmann, Klaus-Peter; Fischer, Wolfgang H (2001-11-01). "Directional effect of inactivation of the nucleus of the optic tract on optokinetic nystagmus in the cat". Vision Research. 41 (25): 3389–3398. doi:10.1016/S0042-6989(01)00184-5. ISSN 0042-6989. PMID 11718781.
  6. ^ Takahashi, Masahiro; Igarashi, Makoto (1977). "Comparison of Vertical and Horizontal Optokinetic Nystagmus in the Squirrel Monkey". ORL. 39 (6): 321–329. doi:10.1159/000275374. ISSN 1423-0275. PMID 97609.
  7. ^ a b Harris, Scott C; Dunn, Felice A (2023-03-17). Meister, Markus; Moore, Tirin; Meister, Markus; Yonehara, Keisuke (eds.). "Asymmetric retinal direction tuning predicts optokinetic eye movements across stimulus conditions". eLife. 12: e81780. doi:10.7554/eLife.81780. ISSN 2050-084X. PMC 10023158. PMID 36930180.
  8. ^ a b Giolli, Roland A.; Blanks, Robert H.I.; Lui, Fausta (2006), "The accessory optic system: Basic organization with an update on connectivity, neurochemistry, and function", Neuroanatomy of the Oculomotor System, Progress in Brain Research, vol. 151, Elsevier, pp. 407–440, doi:10.1016/s0079-6123(05)51013-6, ISBN 978-0-444-51696-1, PMID 16221596
  9. ^ Oyster, C. W. (December 1968). "The analysis of image motion by the rabbit retina". The Journal of Physiology. 199 (3): 613–635. doi:10.1113/jphysiol.1968.sp008671. ISSN 0022-3751. PMC 1365363. PMID 5710424.
  10. ^ Wang, Anna Y. M.; Kulkarni, Manoj M.; McLaughlin, Amanda J.; Gayet, Jacqueline; Smith, Benjamin E.; Hauptschein, Max; McHugh, Cyrus F.; Yao, Yvette Y.; Puthussery, Teresa (2023-10-25). "An ON-type direction-selective ganglion cell in primate retina". Nature. 623 (7986): 381–386. Bibcode:2023Natur.623..381W. doi:10.1038/s41586-023-06659-4. ISSN 0028-0836. PMC 10632142. PMID 37880369.
  11. ^ Wei, Wei (2018-09-15). "Neural Mechanisms of Motion Processing in the Mammalian Retina". Annual Review of Vision Science. 4 (1): 165–192. doi:10.1146/annurev-vision-091517-034048. ISSN 2374-4642. PMID 30095374.
  12. ^ Sivyer, Benjamin; Tomlinson, Alexander; Taylor, W. Rowland (2019-05-29). "Simulated Saccadic Stimuli Suppress ON-Type Direction-Selective Retinal Ganglion Cells via Glycinergic Inhibition". Journal of Neuroscience. 39 (22): 4312–4322. doi:10.1523/JNEUROSCI.3066-18.2019. ISSN 0270-6474. PMC 6538852. PMID 30926751.
  13. ^ Summers, Mathew T.; Feller, Marla B. (May 2022). "Distinct inhibitory pathways control velocity and directional tuning in the mouse retina". Current Biology. 32 (10): 2130–2143.e3. Bibcode:2022CBio...32E2130S. doi:10.1016/j.cub.2022.03.054. ISSN 0960-9822. PMC 9133153. PMID 35395192.
  14. ^ Oyster, Clyde W.; Takahashi, Ellen; Collewijn, Han (February 1972). "Direction-selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit". Vision Research. 12 (2): 183–193. doi:10.1016/0042-6989(72)90110-1. PMID 5033683.
  15. ^ Doustkouhi, Soheil M.; Turnbull, Philip R. K.; Dakin, Steven C. (2020-11-18). "The effect of refractive error on optokinetic nystagmus". Scientific Reports. 10 (1): 20062. Bibcode:2020NatSR..1020062D. doi:10.1038/s41598-020-76865-x. ISSN 2045-2322. PMC 7676235. PMID 33208790.
  16. ^ Doustkouhi, Soheil M.; Turnbull, Philip R. K.; Dakin, Steven C. (2020-02-21). "The Effect of Simulated Visual Field Loss on Optokinetic Nystagmus". Translational Vision Science & Technology. 9 (3): 25. doi:10.1167/tvst.9.3.25. ISSN 2164-2591. PMC 7354858. PMID 32742755.
  17. ^ Taore, Aryaman; Lobo, Gabriel; Turnbull, Philip R.; Dakin, Steven C. (2022-05-11). "Diagnosis of colour vision deficits using eye movements". Scientific Reports. 12 (1): 7734. Bibcode:2022NatSR..12.7734T. doi:10.1038/s41598-022-11152-5. ISSN 2045-2322. PMC 9095692. PMID 35562176.
  18. ^ Leigh, R. John; Zee, David S. (2015). The neurology of eye movements. Contemporary neurology series (5th ed.). Oxford: Oxford university press. ISBN 978-0-19-996928-9.
  19. ^ Yonehara, Keisuke; Shintani, Takafumi; Suzuki, Ryoko; Sakuta, Hiraki; Takeuchi, Yasushi; Nakamura-Yonehara, Kayo; Noda, Masaharu (2008-02-06). "Expression of SPIG1 Reveals Development of a Retinal Ganglion Cell Subtype Projecting to the Medial Terminal Nucleus in the Mouse". PLOS ONE. 3 (2): e1533. Bibcode:2008PLoSO...3.1533Y. doi:10.1371/journal.pone.0001533. ISSN 1932-6203. PMC 2217595. PMID 18253481.
  20. ^ Lilley, Brendan N.; Sabbah, Shai; Hunyara, John L.; Gribble, Katherine D.; Al-Khindi, Timour; Xiong, Jiali; Wu, Zhuhao; Berson, David M.; Kolodkin, Alex L. (January 2019). "Genetic access to neurons in the accessory optic system reveals a role for Sema6A in midbrain circuitry mediating motion perception". Journal of Comparative Neurology. 527 (1): 282–296. doi:10.1002/cne.24507. ISSN 0021-9967. PMC 6312510. PMID 30076594.
  21. ^ Al-Khindi, Timour; Sherman, Michael B.; Kodama, Takashi; Gopal, Preethi; Pan, Zhiwei; Kiraly, James K.; Zhang, Hao; Goff, Loyal A.; du Lac, Sascha; Kolodkin, Alex L. (October 2022). "The transcription factor Tbx5 regulates direction-selective retinal ganglion cell development and image stabilization". Current Biology. 32 (19): 4286–4298.e5. Bibcode:2022CBio...32E4286A. doi:10.1016/j.cub.2022.07.064. PMC 9560999. PMID 35998637.
  22. ^ Summers, Mathew T.; Feller, Marla B. (May 2022). "Distinct inhibitory pathways control velocity and directional tuning in the mouse retina". Current Biology. 32 (10): 2130–2143.e3. Bibcode:2022CBio...32E2130S. doi:10.1016/j.cub.2022.03.054. ISSN 0960-9822. PMC 9133153. PMID 35395192.

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