Streamlined sensory motor communication through cortical reciprocal connectivity in a visually guided eye movement task

Itokazu, Takahide; Hasegawa, Masashi; Kimura, Rui; Osaki, Hirokazu; Albrecht, Urban Raphael; Sohya, Kazuhiro; Chakrabarti, Shubhodeep; Itoh, Hidenori; Ito, Takatoshi; Sato, Tatsuo K.; Satō, Takashi

doi:10.1038/s41467-017-02501-4

Cited by 78 publications

(114 citation statements)

References 74 publications

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“…The result would be conjugate eye movements through coactivation of the ipsilateral abducens motoneurons and contralateral medial rectus motoneurons. The two eyes can move independently during free movement in the rat, suggesting that eye movements are not nearly as yoked as in frontally eyed species (Wallace et al, ; Itokazu et al, ). On the other hand, it should be noted that conjugate compensatory horizontal movements are present in rodents (Stahl, ), and some apparently disjunctive movements may be accounted for by the position of the eyes in the head (Maruta et al, ; Oommen and Stahl, ).…”

Section: Discussionmentioning

confidence: 99%

Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

Bohlen

Bui

Stahl

et al. 2019

The Anatomical Record

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The organization of extraocular muscles (EOMs) and their motor nuclei was investigated in the mouse due to the increased importance of this model for oculomotor research. Mice showed a standard EOM organization pattern, although their eyes are set at the side of the head. They do have more prominent oblique muscles, whose insertion points differ from those of frontal‐eyed species. Retrograde tracers revealed that the motoneuron layout aligns with the general vertebrate plan with respect to nuclei and laterality. The mouse departed in some significant respects from previously studied species. First, more overlap between the distributions of muscle‐specific motoneuronal pools was present in the oculomotor nucleus (III). Furthermore, motoneuron dendrites for each pool filled the entire III and extended beyond the edge of the abducens nucleus (VI). This suggests mouse extraocular motoneuron afferents must target specific pools based on features other than dendritic distribution and nuclear borders. Second, abducens internuclear neurons are located outside the VI. We concluded this because no unlabeled abducens internuclear neurons were observed following lateral rectus muscle injections and because retrograde tracer injections into the III labeled cells immediately ventral and ventrolateral to the VI, not within it. This may provide an anatomical substrate for differential input to motoneurons and internuclear neurons that allows rodents to move their eyes more independently. Finally, while soma size measurements suggested motoneuron subpopulations supplying multiply and singly innervated muscle fibers are present, markers for neurofilaments and perineuronal nets indicated overlap in the size distributions of the two populations. Anat Rec, 302:1865–1885, 2019. © 2019 American Association for Anatomy

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Section: Discussionmentioning

confidence: 99%

Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

Bohlen

Bui

Stahl

et al. 2019

The Anatomical Record

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“…In visual degrees, this corresponds to a velocity range of 100-300 deg s -1 and displacement range of 10-30 deg in mice, well in the range of observed mouse saccade amplitudes 70 . In fact, similar to primates, mice also have oculomotor behavior, even under cortical control 71 . For example, they make, on average, 7.5 saccade-like rapid eye movements per minute when their head is fixed 70 (humans make several saccades per second).…”

Section: Methodsmentioning

confidence: 99%

Perceptual saccadic suppression starts in the retina

Idrees

Baumann

Franke³

et al. 2019

Preprint

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AbstractVisual sensitivity, probed through perceptual detectability of very brief visual stimuli, is strongly impaired around the time of rapid eye movements. This robust perceptual phenomenon, called saccadic suppression, is frequently attributed to active suppressive signals that are directly derived from eye movement commands. Here we show instead that visual-only mechanisms, activated by saccade-induced image shifts, can account for all perceptual properties of saccadic suppression that we have investigated. Such mechanisms start at, but are not necessarily exclusive to, the very first stage of visual processing in the brain, the retina. Critically, neural suppression originating in the retina outlasts perceptual suppression around the time of saccades, suggesting that extra-retinal movement-related signals, rather than causing suppression, may instead act to shorten it. Our results demonstrate a far-reaching contribution of visual processing mechanisms to perceptual saccadic suppression, starting in the retina, without the need to invoke explicit motor-based suppression commands.

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“…We discovered a substantial asymmetry in horizontal nasaltemporal and temporalnasal eye movements in freely moving mice. Thus, similar to head-restrained mice, saccades or stabilizing eye movements along the horizontal eye axis occur simultaneously, but with unequal amplitude in the two eyes (Stahl et al, 2006, Sakatani and Isa, 2007, Itokazu et al, 2018. Since conjugate binocular eye movements typically co-occur with head rotation, the asymmetry might be related to a selective bias for processing visual information in the eye that is on the side of the animal's heading direction (for example causing improved compensation for head rotation in the left eye compared to the right eye during leftward turns) (Maruta et al, 2006).…”

Section: Asymmetry In Horizontal Gaze Movements Between the Two Eyesmentioning

confidence: 99%

“…Studying the neural signals during natural visual orienting behavior will require carefully designed experiments to disentangle eye- (Wang et al, 2015, Itokazu et al, 2018 and head motion-related (Wilson et al, 2018) components, and to understand the integration with visual, motor, vestibular, and proprioceptive signals (Chaplin and Margrie, 2019). For example, head tilt stabilization has been reported in the absence of visual input (darkness) (Andreescu et al, 2005, Oommen and Stahl, 2008, Meyer et al, 2018 suggesting that concomitant changes in eye position are driven by vestibular rather than visual input (Andreescu et al, 2005, Oommen andStahl, 2008).…”

Section: Brain Mechanismsmentioning

confidence: 99%

“…In contrast to humans, mice have no fovea and appear to lack other pronounced retinal specializations for high resolution vision (Dräger andOlsen, 1981, Jeon et al, 1998). Despite this, multiple studies have found that head-restrained mice move their eyes (Sakatani and Isa, 2007, Wang et al, 2015, Samonds et al, 2018, Itokazu et al, 2018, Meyer et al, 2018; these eye movements are rapid and conjugate, i.e. both eyes moving together in the same direction, with an average magnitude of 10 20 • and peak velocities that can reach more than 1000 • /s.…”

Section: Introductionmentioning

confidence: 99%

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Two distinct types of eye-head coupling in freely moving mice

Meyer

O’Keefe

Poort

2020

Preprint

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SummaryAnimals actively interact with their environment to gather sensory information. There is conflicting evidence about how mice use vision to sample their environment. During head restraint, mice make rapid eye movements strongly coupled between the eyes, similar to conjugate saccadic eye movements in humans. However, when mice are free to move their heads, eye movement patterns are more complex and often non-conjugate, with the eyes moving in opposite directions. Here, we combined eye tracking with head motion measurements in freely moving mice and found that both observations can be explained by the existence of two distinct types of coupling between eye and head movements. The first type comprised non-conjugate eye movements which systematically compensated for changes in head tilt to maintain approximately the same visual field relative to the horizontal ground plane. The second type of eye movements were conjugate and coupled to head yaw rotation to produce a “saccade and fixate” gaze pattern. During head initiated saccades, the eyes moved together in the same direction as the head, but during subsequent fixation moved in the opposite direction to the head to compensate for head rotation. This “saccade and fixate” pattern is similar to that seen in humans who use eye movements (with or without head movement) to rapidly shift gaze but in mice relies on combined eye and head movements. Indeed, the two types of eye movements very rarely occurred in the absence of head movements. Even in head-restrained mice, eye movements were invariably associated with attempted head motion. Both types of eye-head coupling were seen in freely moving mice during social interactions and a visually-guided object tracking task. Our results reveal that mice use a combination of head and eye movements to sample their environment and highlight the similarities and differences between eye movements in mice and humans.HighlightsTracking of eyes and head in freely moving mice reveals two types of eye-head couplingEye/head tilt coupling aligns gaze to horizontal planeRotational eye and head coupling produces a “saccade and fixate” gaze pattern with head leading the eyeBoth types of eye-head coupling are maintained during visually-guided behaviorsEye movements in head-restrained mice are related to attempted head movements

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Streamlined sensory motor communication through cortical reciprocal connectivity in a visually guided eye movement task

Cited by 78 publications

References 74 publications

Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

Mouse Extraocular Muscles and the Musculotopic Organization of Their Innervation

Perceptual saccadic suppression starts in the retina

Two distinct types of eye-head coupling in freely moving mice

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