Natural image and receptive field statistics predict saccade sizes

Samonds, Jason M.; Geisler, Wilson S.; Priebe, Nicholas J.

doi:10.1038/s41593-018-0255-5

Cited by 53 publications

(130 citation statements)

References 82 publications

(133 reference statements)

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“…Many studies have reported a limited range of infrequent eye movements in head restrained mice [6,25,28,29] , consistent with the idea that eye movements are generally driven by head movement.…”

Section: Coordinated Horizontal Eye Movements Are Primarily Compensatsupporting

confidence: 53%

Dynamics of gaze control during prey capture in freely moving mice

Michaiel

Abe

Niell

2020

Preprint

102

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Many studies of visual processing are conducted in unnatural conditions, such as head-and gaze-fixation.As this radically limits natural exploration of the visual environment, there is much less known about how animals actively use their sensory systems to acquire visual information in natural, goal-directed contexts.Recently, prey capture has emerged as an ethologically relevant behavior that mice perform without training, and that engages vision for accurate orienting and pursuit. However, it is unclear how mice target their gaze during such natural behaviors, particularly since, in contrast to many predatory species, mice have a narrow binocular field and lack foveate vision that would entail fixing their gaze on a specific point in the visual field. Here we measured head and bilateral eye movements in freely moving mice performing prey capture. We find that the majority of eye movements are compensatory for head movements, thereby acting to stabilize the visual scene. During head turns, however, these periods of stabilization are interspersed with non-compensatory saccades that abruptly shift gaze position. Analysis of eye movements relative to the cricket position shows that the saccades do not preferentially select a specific point in the visual scene. Rather, orienting movements are driven by the head, with the eyes following in coordination to sequentially stabilize and recenter the gaze. These findings help relate eye movements in the mouse to other species, and provide a foundation for studying active vision during ethological behaviors in the mouse.

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Section: Coordinated Horizontal Eye Movements Are Primarily Compensatsupporting

confidence: 53%

Dynamics of gaze control during prey capture in freely moving mice

Michaiel

Abe

Niell

2020

Preprint

102

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“…There is conicting evidence about the role of eye movements in mice. Mice have laterally facing eyes with a large eld of view of approximately 280 • extending in front, above, below, and behind the animal's head (Wagor et al, 1980, Dräger, 1978, Hübener, 2003, Seabrook et al, 2017, Samonds et al, 2018. There is only a narrow binocular eld of approximately 40 50 • overlap.…”

Section: Introductionmentioning

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%

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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“…In between saccades, periods of stable gaze, termed fixations, allow the integration of information about stimuli falling on the fovea. Successive saccade-fixation cycles incrementally build a detailed picture of the environment (Gottlieb, Hayhoe, Hikosaka, & Rangel, 2014;Liu, Shen, Olsen, & Ryan, 2017;Samonds, Geisler, & Priebe, 2018;Zimmermann & Lappe, 2016), enacting memory associations of foveated objects, their spatial arrangement, and context. Conversely, saccade target selection can be influenced by expectations derived from these associations (Buschman & Miller, 2007;Frank & Sabatinelli, 2017;Najemnik & Geisler, 2005;Peelen & Kastner, 2014).…”

Section: Introductionmentioning

confidence: 99%

Modulation of local field potentials and neuronal activity in primate hippocampus during saccades

et al. 2019

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Primates use saccades to gather information about objects and their relative spatial arrangement, a process essential for visual perception and memory. It has been proposed that signals linked to saccades reset the phase of local field potential (LFP) oscillations in the hippocampus, providing a temporal window for visual signals to activate neurons in this region and influence memory formation. We investigated this issue by measuring hippocampal LFPs and spikes in two macaques performing different tasks with unconstrained eye movements. We found that LFP phase clustering (PC) in the alpha/beta (8–16 Hz) frequencies followed foveation onsets, while PC in frequencies lower than 8 Hz followed spontaneous saccades, even on a homogeneous background. Saccades to a solid grey background were not followed by increases in local neuronal firing, whereas saccades toward appearing visual stimuli were. Finally, saccade parameters correlated with LFPs phase and amplitude: saccade direction correlated with delta (≤4 Hz) phase, and saccade amplitude with theta (4–8 Hz) power. Our results suggest that signals linked to saccades reach the hippocampus, producing synchronization of delta/theta LFPs without a general activation of local neurons. Moreover, some visual inputs co‐occurring with saccades produce LFP synchronization in the alpha/beta bands and elevated neuronal firing. Our findings support the hypothesis that saccade‐related signals enact sensory input‐dependent plasticity and therefore memory formation in the primate hippocampus.

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Natural image and receptive field statistics predict saccade sizes

Cited by 53 publications

References 82 publications

Dynamics of gaze control during prey capture in freely moving mice

Dynamics of gaze control during prey capture in freely moving mice

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

Modulation of local field potentials and neuronal activity in primate hippocampus during saccades

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