Introduction
All animals need to react to changes in their environment. Many changes involve relative motion between the animal and its surroundings [
1
Biological image motion processing: a review.
], making visual motion detection a crucial sensory task [
2
- Clifford C.W.
- Ibbotson M.R.
Fundamental mechanisms of visual motion detection: models, cells and functions.
]. Spatially localized motion signals could indicate a salient object in the visual environment, such as a predator or prey [
3
- Semmelhack J.L.
- Donovan J.C.
- Thiele T.R.
- Kuehn E.
- Laurell E.
- Baier H.
A dedicated visual pathway for prey detection in larval zebrafish.
,
4
- Hoy J.L.
- Yavorska I.
- Wehr M.
- Niell C.M.
Vision Drives Accurate Approach Behavior during Prey Capture in Laboratory Mice.
,
5
Visuomotor transformations underlying hunting behavior in zebrafish.
,
6
- Hatsopoulos N.
- Gabbiani F.
- Laurent G.
Elementary computation of object approach by wide-field visual neuron.
,
7
- Temizer I.
- Donovan J.C.
- Baier H.
- Semmelhack J.L.
A Visual Pathway for Looming-Evoked Escape in Larval Zebrafish.
,
8
Looming responses of telencephalic neurons in the pigeon are modulated by optic flow.
], which might engage dedicated escape or hunting maneuvers [
9
- Bianco I.H.
- Kampff A.R.
- Engert F.
Prey capture behavior evoked by simple visual stimuli in larval zebrafish.
,
10
- Eaton R.C.
- Lavender W.A.
- Wieland C.M.
Identification of Mauthner-initiated response patterns in goldfish: Evidence from simultaneous cinematography and electrophysiology.
,
11
- von Reyn C.R.
- Breads P.
- Peek M.Y.
- Zheng G.Z.
- Williamson W.R.
- Yee A.L.
- Leonardo A.
- Card G.M.
A spike-timing mechanism for action selection.
,
12
- Evans D.A.
- Stempel A.V.
- Vale R.
- Ruehle S.
- Lefler Y.
- Branco T.
A synaptic threshold mechanism for computing escape decisions.
]. Spatially coherent global motion typically indicates that the animal is moving within its environment, and animals thereby exhibit a variety of stabilization responses to whole-field motion [
13
- Neuhauss S.C.
- Biehlmaier O.
- Seeliger M.W.
- Das T.
- Kohler K.
- Harris W.A.
- Baier H.
Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish.
,
14
- Kretschmer F.
- Tariq M.
- Chatila W.
- Wu B.
- Badea T.C.
Comparison of optomotor and optokinetic reflexes in mice.
,
15
The neural processing of 3-D visual information: evidence from eye movements.
]. To generate appropriate actions to visual motion stimuli, the animal must accurately estimate motion cues from light signals and route these motion signals through the central brain to the motor circuits that are required to generate the matched elements of behavior [
16
- Ewert J.-P.
- Buxbaum-Conradi H.
- Dreisvogt F.
- Glagow M.
- Merkel-Harff C.
- Röttgen A.
- Schürg-Pfeiffer E.
- Schwippert W.W.
Neural modulation of visuomotor functions underlying prey-catching behaviour in anurans: perception, attention, motor performance, learning.
,
17
- Dunn T.W.
- Gebhardt C.
- Naumann E.A.
- Riegler C.
- Ahrens M.B.
- Engert F.
- Del Bene F.
Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish.
,
18
- Borst A.
- Haag J.
- Reiff D.F.
,
19
- Gahtan E.
- Tanger P.
- Baier H.
Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum.
]. However, the circuits and computations that link sensation to action remain largely unknown. For example, although studies in humans and non-human primates have uncovered a variety of computational cues that brains use to infer whole-field motion from noisy sensory inputs [
20
A set of high-order spatiotemporal stimuli that elicit motion and reverse-phi percepts.
,
21
Three-systems theory of human visual motion perception: review and update.
,
22
Spatiotemporal energy models for the perception of motion.
], the extent to which these motion percepts rely on distinct versus common neural circuits is still debated [
23
Central neural mechanisms for detecting second-order motion.
,
24
- Nishida S.
- Kawabe T.
- Sawayama M.
- Fukiage T.
Motion Perception: From Detection to Interpretation.
].
Interestingly, what we do know about the principles, algorithms, and circuits of visual motion processing is remarkably conserved across both vertebrate and invertebrate brains [
25
Common circuit design in fly and mammalian motion vision.
,
26
Parallel Computations in Insect and Mammalian Visual Motion Processing.
,
27
Design principles of insect and vertebrate visual systems.
]. An appealing hypothesis to explain these observations is that each animal species has individually adapted its motion-processing strategy to reflect the commonly shared statistics of behaviorally relevant natural sensory environments [
28
- Dror R.O.
- O’Carroll D.C.
- Laughlin S.B.
Accuracy of velocity estimation by Reichardt correlators.
,
29
Statistical mechanics and visual signal processing.
,
30
A theory of the visual motion coding in the primary visual cortex.
]. The fundamental idea that visual information processing is adapted to natural scene statistics has provided quantitative and conceptual insights into diverse visual phenomena [
31
Could information theory provide an ecological theory of sensory processing?.
,
32
What Does the Retina Know about Natural Scenes?.
,
33
Theoretical understanding of the early visual processes by data compression and data selection.
,
34
Possible Principles Underlying the Transformations of Sensory Messages.
,
35
- van Hateren J.H.
- van der Schaaf A.
Independent component filters of natural images compared with simple cells in primary visual cortex.
,
36
- Simoncelli E.P.
- Olshausen B.A.
Natural image statistics and neural representation.
,
37
- Zimmermann M.J.Y.
- Nevala N.E.
- Yoshimatsu T.
- Osorio D.
- Nilsson D.E.
- Berens P.
- Baden T.
Zebrafish Differentially Process Color across Visual Space to Match Natural Scenes.
]. In the context of motion processing, this hypothesis has been most thoroughly developed for a class of complex motion stimuli called gliders [
20
A set of high-order spatiotemporal stimuli that elicit motion and reverse-phi percepts.
,
38
- Nitzany E.I.
- Menda G.
- Shamble P.S.
- Golden J.R.
- Hu Q.Q.
- Hoy R.R.
- et al.
Neural computations combine low-and high-order motion cues similarly, in dragonfly and monkey.
,
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
]. It’s worth noting several key results about gliders before addressing their computational logic. First, gliders are perceptually relevant for at least primates and insects [
20
A set of high-order spatiotemporal stimuli that elicit motion and reverse-phi percepts.
,
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
]. Second, the fly’s directional pattern of glider selectivity emerges in performance-optimized models of whole-field velocity estimation in natural environments [
40
- Leonhardt A.
- Ammer G.
- Meier M.
- Serbe E.
- Bahl A.
- Borst A.
Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation.
,
41
- Fitzgerald J.E.
- Clark D.A.
Nonlinear circuits for naturalistic visual motion estimation.
]. Finally, flies extract glider signals early in their visual system, whereas primate glider processing involves the visual cortex [
38
- Nitzany E.I.
- Menda G.
- Shamble P.S.
- Golden J.R.
- Hu Q.Q.
- Hoy R.R.
- et al.
Neural computations combine low-and high-order motion cues similarly, in dragonfly and monkey.
,
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
,
40
- Leonhardt A.
- Ammer G.
- Meier M.
- Serbe E.
- Bahl A.
- Borst A.
Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation.
]. This raises the interesting possibility that diverse animal brains have converged on useful algorithmic solutions to shared computational goals, despite differences in the implementation at the level of neural circuits.
An algorithmic description of visual motion estimation must discern when and how the brain interprets spatiotemporal patterns of light as motion. This is challenging to achieve because the space of possible stimuli is too large to sample exhaustively, and only a small fraction of stimuli will induce motion percepts. Furthermore, natural images and movies are notoriously difficult to parametrize because of their intricate statistical content [
42
Statistics of natural images: Scaling in the woods.
,
43
- Leon P.S.
- Vanzetta I.
- Masson G.S.
- Perrinet L.U.
Motion clouds: model-based stimulus synthesis of natural-like random textures for the study of motion perception.
,
44
The statistics of local motion signals in naturalistic movies.
,
45
- Salisbury J.M.
- Palmer S.E.
Optimal Prediction in the Retina and Natural Motion Statistics.
]. Glider stimuli approach this problem by characterizing motion estimation algorithms in the mathematically complete basis of spatiotemporal correlations [
20
A set of high-order spatiotemporal stimuli that elicit motion and reverse-phi percepts.
,
26
Parallel Computations in Insect and Mammalian Visual Motion Processing.
,
46
- Fitzgerald J.E.
- Katsov A.Y.
- Clandinin T.R.
- Schnitzer M.J.
Symmetries in stimulus statistics shape the form of visual motion estimators.
,
47
- Chen J.
- Mandel H.B.
- Fitzgerald J.E.
- Clark D.A.
Asymmetric ON-OFF processing of visual motion cancels variability induced by the structure of natural scenes.
,
48
Considerations on models of movement detection.
]. Each glider stimulus is designed to account for the fact that motion induces many different spatiotemporal correlations across the visual field [
46
- Fitzgerald J.E.
- Katsov A.Y.
- Clandinin T.R.
- Schnitzer M.J.
Symmetries in stimulus statistics shape the form of visual motion estimators.
,
49
- Hassenstein B.
- Reichardt W.
Systemtheoretische Analyse der Zeit-, Reihenfolgen-und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus.
,
50
- Salazar-Gatzimas E.
- Chen J.
- Creamer M.S.S.
- Mano O.
- Mandel H.B.B.
- Matulis C.A.A.
- Pottackal J.
- Clark D.A.A.
Direct Measurement of Correlation Responses in Drosophila Elementary Motion Detectors Reveals Fast Timescale Tuning.
]. By artificially isolating correlations that co-occur during real-world motion [
44
The statistics of local motion signals in naturalistic movies.
], gliders can flexibly reveal the contributions of various computational cues to motion perception. For example, odd-ordered glider stimuli measure basis elements that are explicitly asymmetric with respect to ON/OFF stimuli, and this property has been used to show that ON/OFF asymmetric neural processing is highly relevant to fly behavior [
40
- Leonhardt A.
- Ammer G.
- Meier M.
- Serbe E.
- Bahl A.
- Borst A.
Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation.
,
41
- Fitzgerald J.E.
- Clark D.A.
Nonlinear circuits for naturalistic visual motion estimation.
,
47
- Chen J.
- Mandel H.B.
- Fitzgerald J.E.
- Clark D.A.
Asymmetric ON-OFF processing of visual motion cancels variability induced by the structure of natural scenes.
]. Similar stimuli and correlation computations are also relevant for depth perception and texture perception [
51
Reversed Depth in Anticorrelated Random-Dot Stereograms and the Central-Peripheral Difference in Visual Inference.
,
52
Spatial organization of nonlinear interactions in form perception.
].
Here we introduce the larval zebrafish as a teleost model for unraveling the neural mechanisms of glider-induced behavior in a vertebrate brain. It is known that larval zebrafish respond behaviorally to phi, reverse-phi, and non-Fourier motion stimuli [
53
- Orger M.B.
- Smear M.C.
- Anstis S.M.
- Baier H.
Perception of Fourier and non-Fourier motion by larval zebrafish.
], which are well known precursors to glider stimuli [
20
A set of high-order spatiotemporal stimuli that elicit motion and reverse-phi percepts.
]. We begin by showing that zebrafish also exhibit directional-responses to third-order glider stimuli, thereby implicating light-dark asymmetric visual motion processing in zebrafish behavior [
40
- Leonhardt A.
- Ammer G.
- Meier M.
- Serbe E.
- Bahl A.
- Borst A.
Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation.
,
41
- Fitzgerald J.E.
- Clark D.A.
Nonlinear circuits for naturalistic visual motion estimation.
,
46
- Fitzgerald J.E.
- Katsov A.Y.
- Clandinin T.R.
- Schnitzer M.J.
Symmetries in stimulus statistics shape the form of visual motion estimators.
]. Importantly, larval zebrafish are small and optically translucent, which permits brain-wide functional imaging at cellular resolution [
54
- Ahrens M.B.
- Li J.M.
- Orger M.B.
- Robson D.N.
- Schier A.F.
- Engert F.
- Portugues R.
Brain-wide neuronal dynamics during motor adaptation in zebrafish.
,
55
- Friedrich R.W.
- Jacobson G.A.
- Zhu P.
Circuit neuroscience in zebrafish.
]. Recent work shows that several motion-guided stabilization behaviors recruit a central brain area called the pretectum [
56
- Kubo F.
- Hablitzel B.
- Dal Maschio M.
- Driever W.
- Baier H.
- Arrenberg A.B.
Functional architecture of an optic flow-responsive area that drives horizontal eye movements in zebrafish.
,
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
,
58
- Portugues R.
- Feierstein C.E.
- Engert F.
- Orger M.B.
Whole-brain activity maps reveal stereotyped, distributed networks for visuomotor behavior.
]. The pretectum spatially integrates visual signals from several classes of retinal ganglion cells [
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
,
59
- Robles E.
- Laurell E.
- Baier H.
The retinal projectome reveals brain-area-specific visual representations generated by ganglion cell diversity.
,
60
- Wang K.
- Hinz J.
- Haikala V.
- Reiff D.F.
- Arrenberg A.B.
Selective processing of all rotational and translational optic flow directions in the zebrafish pretectum and tectum.
,
61
- Kramer A.
- Wu Y.
- Baier H.
- Kubo F.
Neuronal Architecture of a Visual Center that Processes Optic Flow.
] and interconnects with multiple visual and motor pathways [
61
- Kramer A.
- Wu Y.
- Baier H.
- Kubo F.
Neuronal Architecture of a Visual Center that Processes Optic Flow.
,
62
- Yáñez J.
- Suárez T.
- Quelle A.
- Folgueira M.
- Anadón R.
Neural connections of the pretectum in zebrafish (Danio rerio).
]. This functional multiplexing is reflected in substantial response heterogeneity [
56
- Kubo F.
- Hablitzel B.
- Dal Maschio M.
- Driever W.
- Baier H.
- Arrenberg A.B.
Functional architecture of an optic flow-responsive area that drives horizontal eye movements in zebrafish.
,
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
,
60
- Wang K.
- Hinz J.
- Haikala V.
- Reiff D.F.
- Arrenberg A.B.
Selective processing of all rotational and translational optic flow directions in the zebrafish pretectum and tectum.
], although the relative contributions of inputs to the pretectum and within-pretectum computations in shaping the responses of individual pretectal neurons is unclear [
61
- Kramer A.
- Wu Y.
- Baier H.
- Kubo F.
Neuronal Architecture of a Visual Center that Processes Optic Flow.
]. By combining retinal and pretectal imaging, here we show that there are retinal ganglion cells that are direction selective across glider stimuli and that pretectal neurons refine this representation to precisely match the patterns that we observed behaviorally. These data suggest that retinal motion processing is tailored to the demands of naturalistic stimuli, whereas the pretectum provides a flexible code for those visual motion stimuli that drive stabilization behaviors.
Discussion
Visual motion influences a wide variety of ethological behaviors, so evolution demands that visual systems accurately estimate motion from naturalistic patterns of input. Canonical models of visual motion estimation in both flies and primates suppose that pairwise correlations between light signals provide the fundamental cues of elementary motion detection [
22
Spatiotemporal energy models for the perception of motion.
,
49
- Hassenstein B.
- Reichardt W.
Systemtheoretische Analyse der Zeit-, Reihenfolgen-und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus.
], and here we found temporal frequency tuning in zebrafish behavior that mimicked model predictions and fly behavior [
64
Transient and steady-state response properties of movement detectors.
,
65
- Creamer M.S.
- Mano O.
- Clark D.A.
Visual Control of Walking Speed in Drosophila.
]. Nevertheless, pairwise motion estimates have limited accuracy for complex naturalistic stimuli [
28
- Dror R.O.
- O’Carroll D.C.
- Laughlin S.B.
Accuracy of velocity estimation by Reichardt correlators.
,
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
]. Fortunately, the rich statistics of natural motion [
44
The statistics of local motion signals in naturalistic movies.
,
45
- Salisbury J.M.
- Palmer S.E.
Optimal Prediction in the Retina and Natural Motion Statistics.
] imply that a variety of higher-order spatiotemporal cues can help [
29
Statistical mechanics and visual signal processing.
,
41
- Fitzgerald J.E.
- Clark D.A.
Nonlinear circuits for naturalistic visual motion estimation.
,
46
- Fitzgerald J.E.
- Katsov A.Y.
- Clandinin T.R.
- Schnitzer M.J.
Symmetries in stimulus statistics shape the form of visual motion estimators.
,
47
- Chen J.
- Mandel H.B.
- Fitzgerald J.E.
- Clark D.A.
Asymmetric ON-OFF processing of visual motion cancels variability induced by the structure of natural scenes.
]. In this study, we discovered that third-order cues robustly elicit motion-guided behaviors in larval zebrafish, with patterns that strikingly match those of flies [
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
]. Interestingly, basic statistics of natural visual scenes are shared across a wide range of visual environments [
36
- Simoncelli E.P.
- Olshausen B.A.
Natural image statistics and neural representation.
,
42
Statistics of natural images: Scaling in the woods.
], and the visual systems of multiple species, including fruit flies, dragonflies, larval zebrafish, macaques, and humans, have found ways to incorporate second-, third-, and higher-order correlations into their motion-processing algorithms [
20
A set of high-order spatiotemporal stimuli that elicit motion and reverse-phi percepts.
,
38
- Nitzany E.I.
- Menda G.
- Shamble P.S.
- Golden J.R.
- Hu Q.Q.
- Hoy R.R.
- et al.
Neural computations combine low-and high-order motion cues similarly, in dragonfly and monkey.
,
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
,
53
- Orger M.B.
- Smear M.C.
- Anstis S.M.
- Baier H.
Perception of Fourier and non-Fourier motion by larval zebrafish.
,
80
Drift-balanced random stimuli: a general basis for studying non-Fourier motion perception.
,
81
- Theobald J.C.
- Duistermars B.J.
- Ringach D.L.
- Frye M.A.
Flies see second-order motion.
]. The observed directionalities of zebrafish and fly turning behaviors agree with the hypotheses of prior theoretical work that calculated how flies should combine low-order correlational cues to best estimate the velocity of whole-field motion [
41
- Fitzgerald J.E.
- Clark D.A.
Nonlinear circuits for naturalistic visual motion estimation.
]. Thus, the algorithms of visual motion estimation are strikingly convergent across the animal kingdom, and natural sensory statistics provide a valuable guide for understanding these algorithms. Because prior models were built from the statistics of natural terrestrial environments, it will be interesting to determine whether any predictions change for the underwater environments experienced by zebrafish [
37
- Zimmermann M.J.Y.
- Nevala N.E.
- Yoshimatsu T.
- Osorio D.
- Nilsson D.E.
- Berens P.
- Baden T.
Zebrafish Differentially Process Color across Visual Space to Match Natural Scenes.
,
82
- Balboa R.M.
- Grzywacz N.M.
Power spectra and distribution of contrasts of natural images from different habitats.
].
Understanding how these algorithms are implemented within visual systems can provide additional insight into the logic and mechanisms of neuronal computation. Direction selectivity arises in the retina of many vertebrate species, including rabbits, mice, and zebrafish [
74
- Nikolaou N.
- Lowe A.S.
- Walker A.S.
- Abbas F.
- Hunter P.R.
- Thompson I.D.
- Meyer M.P.
Parametric functional maps of visual inputs to the tectum.
,
83
- Baden T.
- Berens P.
- Franke K.
- Román Rosón M.
- Bethge M.
- Euler T.
The functional diversity of retinal ganglion cells in the mouse.
,
84
Selective sensitivity to direction of movement in ganglion cells of the rabbit retina.
]. However, not all motion cues are present in the earliest direction-selective cells [
40
- Leonhardt A.
- Ammer G.
- Meier M.
- Serbe E.
- Bahl A.
- Borst A.
Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation.
,
85
- Rust N.C.
- Mante V.
- Simoncelli E.P.
- Movshon J.A.
How MT cells analyze the motion of visual patterns.
], and which motion cues are computed in the retina versus central brain remains unclear [
86
- Dhande O.S.
- Stafford B.K.
- Franke K.
- El-Danaf R.
- Percival K.A.
- Phan A.H.
- Li P.
- Hansen B.J.
- Nguyen P.L.
- Berens P.
- et al.
Molecular Fingerprinting of On-Off Direction-Selective Retinal Ganglion Cells Across Species and Relevance to Primate Visual Circuits.
,
87
- Cruz-Martín A.
- El-Danaf R.N.
- Osakada F.
- Sriram B.
- Dhande O.S.
- Nguyen P.L.
- Callaway E.M.
- Ghosh A.
- Huberman A.D.
A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex.
]. Here we used functional calcium imaging of retinal ganglion cell axon terminals to show that the zebrafish retina computes direction-selective motion signals for reverse-phi stimuli and three-point glider stimuli. The pattern of direction selectivity precisely matched the directionality of optomotor turning behavior. Interestingly, the fly’s earliest direction-selective neurons also respond to reverse-phi stimuli with a directionality matched to behavior [
50
- Salazar-Gatzimas E.
- Chen J.
- Creamer M.S.S.
- Mano O.
- Mandel H.B.B.
- Matulis C.A.A.
- Pottackal J.
- Clark D.A.A.
Direct Measurement of Correlation Responses in Drosophila Elementary Motion Detectors Reveals Fast Timescale Tuning.
,
67
- Salazar-Gatzimas E.
- Agrochao M.
- Fitzgerald J.E.
- Clark D.A.
The Neuronal Basis of an Illusory Motion Percept Is Explained by Decorrelation of Parallel Motion Pathways.
]. Fly researchers have recognized that this response pattern is inconsistent with a naive neuronal implementation of the HRC’s multiplication operation [
67
- Salazar-Gatzimas E.
- Agrochao M.
- Fitzgerald J.E.
- Clark D.A.
The Neuronal Basis of an Illusory Motion Percept Is Explained by Decorrelation of Parallel Motion Pathways.
], yet it can emerge from a motion energy model [
88
- Leong J.C.S.
- Esch J.J.
- Poole B.
- Ganguli S.
- Clandinin T.R.
Direction Selectivity in Drosophila Emerges from Preferred-Direction Enhancement and Null-Direction Suppression.
], a spatially distributed implementation of the HRC [
67
- Salazar-Gatzimas E.
- Agrochao M.
- Fitzgerald J.E.
- Clark D.A.
The Neuronal Basis of an Illusory Motion Percept Is Explained by Decorrelation of Parallel Motion Pathways.
], or a biophysically realistic neuron model [
89
- Zavatone-Veth J.A.
- Badwan B.A.
- Clark D.A.
A minimal synaptic model for direction selective neurons in Drosophila.
]. On the other hand, the correct directional preferences for third-order glider stimuli only emerge in flies after separate ON-edge and OFF-edge motion signals are combined [
40
- Leonhardt A.
- Ammer G.
- Meier M.
- Serbe E.
- Bahl A.
- Borst A.
Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation.
,
90
- Joesch M.
- Schnell B.
- Raghu S.V.
- Reiff D.F.
- Borst A.
ON and OFF pathways in Drosophila motion vision.
]. This suggests that AF5&6 encode both ON-edge and OFF-edge motions. Our results generally support the hypothesis that the elementary motion signals needed for the zebrafish optomotor response are computed in the retina [
53
- Orger M.B.
- Smear M.C.
- Anstis S.M.
- Baier H.
Perception of Fourier and non-Fourier motion by larval zebrafish.
,
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
]. Because the directionality of glider behavior can be predicted from the demands of accurate motion estimation with natural scenes [
41
- Fitzgerald J.E.
- Clark D.A.
Nonlinear circuits for naturalistic visual motion estimation.
], this suggests that the retina’s algorithms for motion processing are tailored to the structure of natural sensory environments. Furthermore, the direction-selective signatures associated with whole-field motion are targeted specifically to AF5 and AF6 [
61
- Kramer A.
- Wu Y.
- Baier H.
- Kubo F.
Neuronal Architecture of a Visual Center that Processes Optic Flow.
], which have previously been shown to causally affect optomotor responses to drifting grating stimuli [
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
]. We were thus able to link a naturalistic retinal computation to behavior via specific retinal projection patterns in the central brain.
Retinal signals do not project directly to the hindbrain motor centers generating behavior [
59
- Robles E.
- Laurell E.
- Baier H.
The retinal projectome reveals brain-area-specific visual representations generated by ganglion cell diversity.
,
72
- Burrill J.D.
- Easter Jr., S.S.
Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio).
], and our data support the emerging view that the pretectum is a midbrain visual area that integrates and refines visual motion cues in support of several stabilization behaviors [
56
- Kubo F.
- Hablitzel B.
- Dal Maschio M.
- Driever W.
- Baier H.
- Arrenberg A.B.
Functional architecture of an optic flow-responsive area that drives horizontal eye movements in zebrafish.
,
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
,
60
- Wang K.
- Hinz J.
- Haikala V.
- Reiff D.F.
- Arrenberg A.B.
Selective processing of all rotational and translational optic flow directions in the zebrafish pretectum and tectum.
,
61
- Kramer A.
- Wu Y.
- Baier H.
- Kubo F.
Neuronal Architecture of a Visual Center that Processes Optic Flow.
]. For example, the pretectum has been shown to binocularly integrate several directions of visual motion information in a manner that recapitulates the magnitudes and latencies of optomotor behaviors [
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
,
91
Neural circuits for evidence accumulation and decision making in larval zebrafish.
,
92
- Dragomir E.I.
- Štih V.
- Portugues R.
Evidence accumulation during a sensorimotor decision task revealed by whole-brain imaging.
]. Here we extend this argument and suggest that the pretectum also integrates direction-selective retinal signals to represent more complex motion cues, including those in reverse-phi and glider stimuli, with magnitudes that facilitate behavior. We further hypothesize that this functional organization will underlie optomotor responses to second-order motion stimuli [
53
- Orger M.B.
- Smear M.C.
- Anstis S.M.
- Baier H.
Perception of Fourier and non-Fourier motion by larval zebrafish.
,
75
Visuomotor behaviors in larval zebrafish after GFP-guided laser ablation of the optic tectum.
], and these properties generally make the pretectum well suited to process higher-order motion cues that require long-range nonlinear integration of local motion signals [
21
Three-systems theory of human visual motion perception: review and update.
,
24
- Nishida S.
- Kawabe T.
- Sawayama M.
- Fukiage T.
Motion Perception: From Detection to Interpretation.
]. Overall, this results in a representation that closely correlates with the behavioral outcomes induced by a diversity of visual motion stimuli [
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
,
76
- Chen X.
- Mu Y.
- Hu Y.
- Kuan A.T.
- Nikitchenko M.
- Randlett O.
- Chen A.B.
- Gavornik J.P.
- Sompolinsky H.
- Engert F.
- Ahrens M.B.
Brain-wide Organization of Neuronal Activity and Convergent Sensorimotor Transformations in Larval Zebrafish.
]. This representation is anatomically organized into lateralized populations of neurons with similar directional tuning, which could permit ipsilateral long-range connections from the pretectum to lateralized hindbrain nuclei associated with turning behaviors. More generally, the afferents and efferents of the pretectum are varied and numerous [
62
- Yáñez J.
- Suárez T.
- Quelle A.
- Folgueira M.
- Anadón R.
Neural connections of the pretectum in zebrafish (Danio rerio).
], which might permit the pretectum to flexibly influence multiple behaviors.
Our data support the idea that the retina extracts multiple features of naturalistic visual stimuli, whereas central brain areas integrate and refine these features according to their relevance for specific behaviors [
56
- Kubo F.
- Hablitzel B.
- Dal Maschio M.
- Driever W.
- Baier H.
- Arrenberg A.B.
Functional architecture of an optic flow-responsive area that drives horizontal eye movements in zebrafish.
,
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
,
71
- Randlett O.
- Wee C.L.
- Naumann E.A.
- Nnaemeka O.
- Schoppik D.
- Fitzgerald J.E.
- Portugues R.
- Lacoste A.M.B.
- Riegler C.
- Engert F.
- Schier A.F.
Whole-brain activity mapping onto a zebrafish brain atlas.
,
93
- Wu M.
- Nern A.
- Williamson W.R.
- Morimoto M.M.
- Reiser M.B.
- Card G.M.
- et al.
Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs.
,
94
Eye smarter than scientists believed: neural computations in circuits of the retina.
]. This idea is likely to generalize across species and visually guided behaviors. Mice have dozens of functionally distinct RGC types [
83
- Baden T.
- Berens P.
- Franke K.
- Román Rosón M.
- Bethge M.
- Euler T.
The functional diversity of retinal ganglion cells in the mouse.
]. In larval zebrafish, many anatomically distinct RGCs project contralaterally to ten AFs [
59
- Robles E.
- Laurell E.
- Baier H.
The retinal projectome reveals brain-area-specific visual representations generated by ganglion cell diversity.
,
72
- Burrill J.D.
- Easter Jr., S.S.
Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio).
]. The non-uniformity of these projections could easily route visual features to their appropriate targets. For instance, RGCs in AF7 specifically respond to natural and artificial prey stimuli [
3
- Semmelhack J.L.
- Donovan J.C.
- Thiele T.R.
- Kuehn E.
- Laurell E.
- Baier H.
A dedicated visual pathway for prey detection in larval zebrafish.
], which in turn drive prey capture related circuitry in the optic tectum [
5
Visuomotor transformations underlying hunting behavior in zebrafish.
]. Moreover, AF6, AF8, and AF9 process dark looming and dimming stimuli [
7
- Temizer I.
- Donovan J.C.
- Baier H.
- Semmelhack J.L.
A Visual Pathway for Looming-Evoked Escape in Larval Zebrafish.
], with AF9 being even more strongly activated by bright looming and luminance increases, and these retinal responses could drive escape behaviors via visual processing in the optic tectum [
17
- Dunn T.W.
- Gebhardt C.
- Naumann E.A.
- Riegler C.
- Ahrens M.B.
- Engert F.
- Del Bene F.
Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish.
]. Finally, optomotor and optokinetic responses combine several behavioral motifs, and AF4, AF5, AF6, AF9, as well as the pretectum have each been implicated in some of their aspects [
56
- Kubo F.
- Hablitzel B.
- Dal Maschio M.
- Driever W.
- Baier H.
- Arrenberg A.B.
Functional architecture of an optic flow-responsive area that drives horizontal eye movements in zebrafish.
,
57
- Naumann E.A.
- Fitzgerald J.E.
- Dunn T.W.
- Rihel J.
- Sompolinsky H.
- Engert F.
From Whole-Brain Data to Functional Circuit Models: The Zebrafish Optomotor Response.
,
61
- Kramer A.
- Wu Y.
- Baier H.
- Kubo F.
Neuronal Architecture of a Visual Center that Processes Optic Flow.
,
95
- Muto A.
- Orger M.B.
- Wehman A.M.
- Smear M.C.
- Kay J.N.
- Page-McCaw P.S.
- Gahtan E.
- Xiao T.
- Nevin L.M.
- Gosse N.J.
- et al.
Forward genetic analysis of visual behavior in zebrafish.
]. Future work is needed to more fully identify the functional mapping of retinal features to specific AFs, downstream brain regions, and resultant behaviors.
Visual motion estimation is a computation that all animals need to perform [
1
Biological image motion processing: a review.
]. By comparing the solutions of evolution to this problem, we can better understand similarities and differences between neural circuits. Similarities point to evolutionary convergence. For example, light-dark asymmetries are fundamental to glider processing [
41
- Fitzgerald J.E.
- Clark D.A.
Nonlinear circuits for naturalistic visual motion estimation.
,
46
- Fitzgerald J.E.
- Katsov A.Y.
- Clandinin T.R.
- Schnitzer M.J.
Symmetries in stimulus statistics shape the form of visual motion estimators.
], and the neural implementation of glider processing in both flies and primates involves a separation of signals into ON-edge and OFF-edge channels [
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
,
40
- Leonhardt A.
- Ammer G.
- Meier M.
- Serbe E.
- Bahl A.
- Borst A.
Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation.
]. Our current results suggest that ON/OFF separations within the vertebrate retina might be utilized to generate responses to glider stimuli in zebrafish [
25
Common circuit design in fly and mammalian motion vision.
,
26
Parallel Computations in Insect and Mammalian Visual Motion Processing.
,
96
Optomotor Swimming in Larval Zebrafish Is Driven by Global Whole-Field Visual Motion and Local Light-Dark Transitions.
]. Differences are also important, because they could reveal multiple implementations of common computational algorithms. For example, many circuit architectures might extract glider signals [
38
- Nitzany E.I.
- Menda G.
- Shamble P.S.
- Golden J.R.
- Hu Q.Q.
- Hoy R.R.
- et al.
Neural computations combine low-and high-order motion cues similarly, in dragonfly and monkey.
,
40
- Leonhardt A.
- Ammer G.
- Meier M.
- Serbe E.
- Bahl A.
- Borst A.
Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation.
,
41
- Fitzgerald J.E.
- Clark D.A.
Nonlinear circuits for naturalistic visual motion estimation.
,
88
- Leong J.C.S.
- Esch J.J.
- Poole B.
- Ganguli S.
- Clandinin T.R.
Direction Selectivity in Drosophila Emerges from Preferred-Direction Enhancement and Null-Direction Suppression.
]. Furthermore, prior work implicates the primate cortex in glider processing [
38
- Nitzany E.I.
- Menda G.
- Shamble P.S.
- Golden J.R.
- Hu Q.Q.
- Hoy R.R.
- et al.
Neural computations combine low-and high-order motion cues similarly, in dragonfly and monkey.
,
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
], but our current data suggest that in the zebrafish these signals are present in the retina. This suggests that vertebrate brains have explored multiple strategies for visual processing. For example, some species might have highly specific feature detectors in the retina whereas others might rely on more generic retinal representations [
86
- Dhande O.S.
- Stafford B.K.
- Franke K.
- El-Danaf R.
- Percival K.A.
- Phan A.H.
- Li P.
- Hansen B.J.
- Nguyen P.L.
- Berens P.
- et al.
Molecular Fingerprinting of On-Off Direction-Selective Retinal Ganglion Cells Across Species and Relevance to Primate Visual Circuits.
,
87
- Cruz-Martín A.
- El-Danaf R.N.
- Osakada F.
- Sriram B.
- Dhande O.S.
- Nguyen P.L.
- Callaway E.M.
- Ghosh A.
- Huberman A.D.
A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex.
]. Similarly, saliency maps guiding attention might occur in variable brain regions across vertebrate species [
97
From the optic tectum to the primary visual cortex: migration through evolution of the saliency map for exogenous attentional guidance.
]. Such species-level differences could provide hints into how subtle evolutionary and ethological factors impact neural computation [
38
- Nitzany E.I.
- Menda G.
- Shamble P.S.
- Golden J.R.
- Hu Q.Q.
- Hoy R.R.
- et al.
Neural computations combine low-and high-order motion cues similarly, in dragonfly and monkey.
,
39
- Clark D.A.
- Fitzgerald J.E.
- Ales J.M.
- Gohl D.M.
- Silies M.A.
- Norcia A.M.
- Clandinin T.R.
Flies and humans share a motion estimation strategy that exploits natural scene statistics.
,
97
From the optic tectum to the primary visual cortex: migration through evolution of the saliency map for exogenous attentional guidance.
,
98
- Atick J.J.
- Li Z.
- Redlich A.N.
Understanding Retinal Color Coding from First Principles.
]. Here we have taken important steps toward establishing the larval zebrafish as a powerful system for comparative studies of the neural computations underlying visual motion processing. We anticipate that the unique possibilities afforded by brain-wide imaging in this behaving vertebrate will play crucial roles in comparative studies that address complex aspects of motion-guided behavior and decision making.
Acknowledgments
We would like to thank Florian Engert and Haim Sompolinsky for early input on this project and partial funding of C.R. and J.E.F., Iris Odstrcil and Rob Johnson for valuable technical input, and Eva Naumann for insightful conversations regarding optomotor behavior and pretectal representations. We would also like to thank Damon Clark for comments on the manuscript. Finally, we would like to thank Fumi Kubo and Herwig Baier for providing the Tg:UAS-SyGCaMP6s line. T.Y. and R.P. were partly funded by grant RGP0027/2016 from the Human Frontier Science Program and by the Max Planck Foundation. This work was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy within the framework of the Munich Cluster for Systems Neurology (EXC 2145 SyNergy – ID 390857198 ). C.R. and J.E.F. were supported by NIH grant U01 NS090449 , and C.R. was additionally supported by NIH grant U19 NS104653 . J.E.F. was additionally supported by the Swartz Foundation and the Howard Hughes Medical Institute.
Author Contributions
J.E.F. and R.P. conceived the project. T.Y. performed the experiments, with help from C.R. and R.P. T.Y., J.E.F., and R.P. analyzed and interpreted the data. T.Y., J.E.F., and R.P. wrote the manuscript with input from C.R. J.E.F. and R.P. supervised the project and acquired funding.
Declaration Of Interests
The authors declare no competing interests.
