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Link to original content: http://www.ncbi.nlm.nih.gov/pubmed/30925897
Selective processing of all rotational and translational optic flow directions in the zebrafish pretectum and tectum - PubMed Skip to main page content
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. 2019 Mar 29;17(1):29.
doi: 10.1186/s12915-019-0648-2.

Selective processing of all rotational and translational optic flow directions in the zebrafish pretectum and tectum

Kun Wang  1   2 , Julian Hinz  1   2   3 , Väinö Haikala  4 , Dierk F Reiff  4 , Aristides B Arrenberg  5
Affiliations

Selective processing of all rotational and translational optic flow directions in the zebrafish pretectum and tectum

Kun Wang et al. BMC Biol. .

Abstract

Background: The processing of optic flow in the pretectum/accessory optic system allows animals to stabilize retinal images by executing compensatory optokinetic and optomotor behavior. The success of this behavior depends on the integration of information from both eyes to unequivocally identify all possible translational or rotational directions of motion. However, it is still unknown whether the precise direction of ego-motion is already identified in the zebrafish pretectum or later in downstream premotor areas.

Results: Here, we show that the zebrafish pretectum and tectum each contain four populations of motion-sensitive direction-selective (DS) neurons, with each population encoding a different preferred direction upon monocular stimulation. In contrast, binocular stimulation revealed the existence of pretectal and tectal neurons that are specifically tuned to only one of the many possible combinations of monocular motion, suggesting that further downstream sensory processing might not be needed to instruct appropriate optokinetic and optomotor behavior.

Conclusion: Our results suggest that local, task-specific pretectal circuits process DS retinal inputs and carry out the binocular sensory computations necessary for optokinetic and optomotor behavior.

Keywords: Binocular integration; Calcium imaging; Optic flow; Optic tectum; Optokinetic response; Optomotor response; Pretectum; Zebrafish.

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Conflict of interest statement

Ethics approval and consent to participate

The animal experiments were licensed by the local authorities (Regierungspräsidium Tübingen) in accordance with German federal law and Baden-Württemberg state law.

Competing interests

All authors declare that they have no competing interests.

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Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Monocular motion stimuli reveal four orthogonal preferred directions in the zebrafish pretectum and optic tectum. a A half-cylindrical stimulus arena was used to present motion in eight different directions to the zebrafish (not drawn to scale). b Time-averaged optical slice of tectal GCaMP5G expression (left). The z-score heat map (right) was used to detect motion-sensitive pixels and circular regions of interest (ROIs) were drawn manually (left). Scale bar, 50 μm (c) Top: ΔF/F responses (of three stimulus repetitions) of two example neurons. Grey lines indicate the motion phases; their shape corresponds to the signal expected for a motion-sensitive cell (regressor, see “Materials and methods”). Bottom: Polar plots illustrating responses for each stimulus phase for one direction-selective (left) and one orientation-selective (right) cell. Blue lines correspond to the median ΔF/F from three repetitions, red lines to the fitted von-Mises function used to infer the preferred direction (PD), the direction and orientation selectivity indices (DSI and OSI), and the goodness of fit (R2). d Number of identified DS and OS cells per recorded brain in optic tectum (OT) and pretectum (PT). Motion-sensitive cells that are neither DS nor OS are classified as “Remaining.” e Histograms of the preferred directions of direction-selective neurons in pretectum (top) and optic tectum (bottom) (pooled from nine imaged brains). The four peaks were fitted with a sum of four von-Mises functions (red line). f The four fitted peak directions from e are plotted for pretectum (blue) and optic tectum (red). Please note that in panels e and f the illustration arrow for NT points in a different direction than in panels a and c. We chose to switch arrangement to allow an easier comparison of panel (e) to the plots published in a previous report (Fig. 2a of Hunter et al [14]). g Anatomical maps of DS neurons (color-coded according to PD) in the tectum and pretectum. AF-9, arborization field 9-containing neuropil; nMLF, nucleus of the medial longitudinal fasciculus; vEMN/dEMN, ventral and dorsal extraocular motoneurons. Error bars correspond to SEM. A, anterior; P, posterior; L, left; R, right; D, dorsal; V, ventral
Fig. 2
Fig. 2
Binocular selective neurons in the optic tectum and pretectum. a Two half-cylindrical arenas were used to present moving gratings. The binocular zone (nasal 36°) was blocked. b The stimulus protocol consisted of 7 × 7 binocular motion phases. A unique combination of stimuli (stationary: St, temporal-to-nasal: TN, upwards: Up, nasal-to-temporal: NT, downwards: Down, pitch up: PiUp, pitch down: PiDo) was shown to both eyes in each phase. For each stimulus combination, the summed activity (z-score) across motion-sensitive neurons is indicated in arbitrary units (a.u.). The red rectangle indicates the 5 × 5 stimulus phases further analyzed in panels d–g. Rp, Rr, Ry: binocular pitch, roll and yaw rotational stimulus phases. Tt, Tl: binocular thrust (forward/backward) and lift (up/down) translational stimulus phases (also see Fig. 4a). c Calcium responses of three example cells (median activity across three repetitions). The rectangular gray shades correspond to the 64 motion stimulus phases (Additional file 1: Figure S1E). d Calcium activity heat maps, classified binary response types and linear model fits of the cells from (c). e Binary response type analysis. The number of neurons (in pretectum and tectum, n = 8 animals, four composite brains, see “Materials and methods”) is plotted versus the ~ 34 million (225) theoretically possible binary response types. Green, monocular response types; magenta and gray, binocular-selective response types; light blue: indistinct binocular response types. The first 34 frequent response types are illustrated below. Yellow, responsive phases; blue, non-responsive phases. f The number of neurons for the frequent monocular response types (each line corresponds to one response type), g binocular-selective response types (active only during one binocular stimulus combination) and h monocular pitch-responding type (only active during the indicated monocular pitch phases) are indicated in green (monocular responsive), magenta (binocular selective), gray (stationary selective), and red (pitch responsive). LE/RE: left/right eye
Fig. 3
Fig. 3
Pretectal binocular selective neurons processing visual stimuli presented from below. a The visual stimulus was presented from below the animal, while calcium activity was recorded from above. b Top: Ten binocular stimulus phases were repeated 3 to 10 times. The black arrowheads indicate the gratings’ moving directions. Bottom: normalized ΔF/F calcium responses for three examples, forward-selective, sideward-selective, and forward-and-sideward-selective neurons. White bars indicate the gratings’ moving directions for the corresponding eyes (colored circles); black circles represent eyes when stationary gratings were presented. c Neuronal response types were classified based on the calcium activity during the ten stimulation phases (y-axis, black: active). The width in the x-axis corresponds to the cell number for each response type. Response types are ordered according to frequency. d Response profiles of the eight most frequent response types (Additional file 3: Figure S3 for the mirror-symmetrical response types). Response types labeled “non-selective” are active for more than one stimulus phase. Response types labeled “binocular” are influenced by stimulus motion presented to either eye. e Grouped and averaged response profiles of all neurons (leftward or rightward) that are sideward-selective, when only the first 8 stimulus phases are considered, corresponding to response type “S” in the previous study [9]. The first four rows show all possible response combinations for S type cells (including all 10 — not just 8 — stimulus phases) and the last row shows the weighted average of all S type neurons. The cell numbers correspond to the sum of S type cells and the mirror-symmetrical S′ type cells. Note that the response type exclusively active for leftward motion (S w/o FW w/o BW, first row) cannot be detected when all responses are merged together (fifth row). In the study by Naumann et al., only this fifth merged response type has been reported
Fig. 4
Fig. 4
Proposed circuit model for binocular processing of optic flow in the pretectum. a The pretectum receives its DS-RGC inputs mainly via the pretectal arborization field AF5 (F. Kubo, personal communication, October 2018) and a transformation of represented motion axes occurs between retina (three PDs [14, 15]) and pretectum (four PDs). The monocularly responsive pretectal DS cells (green) send commissural projections (via the posterior commissure) to the contralateral pretectum, resulting in binocular non-selective response types (half green/half magenta) and binocular selective (magenta) response types. The binocular-selective neurons code for a single rotational or translational optic flow direction and could directly drive appropriate optomotor and optokinetic behavior via premotor structures such as the nucleus of the medial longitudinal fasciculus and oculomotor nuclei. Rp, Rr, Ry: neurons selective for rotations about the pitch, roll and yaw axes, respectively. Ts, Tt, Tl: neurons selective for translations along the sideslip (sidewards left/right), thrust (forward/backward), and lift (up/down) axes, respectively. Please note that only these six axes were tested in this study and it is possible that other (oblique) global optic flow axes result in even stronger responses, as suggested by previous reports on other species (see “Discussion”). b A proposed common computational motif shared across different planes of motion is antagonistic inputs from monocular pretectal neurons to binocular-selective neurons coding for motion in the same plane (here in the horizontal plane): A left eye monocular neuron in the right pretectal half excites the Forward-selective neuron (Tt) during forward translation, while a right eye monocular neuron in the left pretectal half inhibits the selective neuron during nasal-to-temporal motion in the right eye, thus establishing forward selectivity
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