Light-dependent cues from the surrounding world are perceived by specialized photoreceptor neurons (PRs) in the eye. Insect compound eyes are elaborate systems capable of mediating flight in a rapidly changing 3D environment. In contrast, larval stages present much simpler visual organs, which combined with their tractability, make them great models to link neural circuit processing and behavior (Kane et al., 2013; Randel et al., 2014; 2015; Gepner et al., 2015). Larvae of the fruit fly Drosophila melanogaster employ their visual system for a range of diverse behaviors including navigation, entrainment of circadian rhythms, formation of associative memories and may respond to the presence of other larvae (Kane et al., 2013; Humberg and Sprecher, 2017; Slepian et al., 2015; Justice et al., 2012; Yamanaka et al., 2013; von Essen et al., 2011; Gong, 2009; Mazzoni et al., 2005; Gerber et al., 2004; Sawin-McCormack et al., 1995). The simple eyes of the larva (also termed Bolwig Organ, BO) consist of only about 12 PRs each and yet drive a wide range of behaviors, raising questions on the organizational logic of the underlying visual circuit. Spectral sensitivity of PRs is defined by the Rhodopsin gene they express. Larval eyes contain two PR-types, either expressing the blue-tuned Rhodopsin5 (Rh5) or the green-tuned Rhodopsin6 (Rh6) (Malpel et al., 2002; Hassan et al., 2005; Rodriguez Moncalvo and Campos, 2005; Sprecher et al., 2007). Interestingly, for rapid navigation away from light exposure only the Rh5-PRs seem essential, whereas to entrain the molecular clock either PR subtype suffices (Keene et al., 2011). In the past, several neurons of the larval visual neural circuit have been identified but the logic of circuit wiring as well as the precise numbers of neurons involved in its first order visual processing center remain unknown.

Larval PRs project their axons in a joint nerve (Bolwig nerve) terminating in a small neuropil domain termed the larval optic neuropil (LON). Previous studies identified eleven neurons innervating the LON in each brain hemisphere. This includes four lateral neurons (LaNs) expressing the pigment dispersing factor (Pdf) neuropeptide (Pdf-LaNs) and a fifth non-Pdf-expressing LaN (5th-LaN), all being part of the clock circuit (Kaneko et al., 1997), as well as a serotonergic neuron and three optic lobe pioneer cells (OLPs) (Helfrich-Förster, 1997; Rodriguez Moncalvo and Campos, 2005; 2009; Tix et al., 1989). Recently, two unpaired median octopaminergic/tyraminergic neurons were described to extend neurites into these neuropils (Selcho et al., 2014). It remained unknown, however, whether these previously identified neurons constitute the entire neuronal components of the LON and how visual neuronal components connect to each other to form a functional network. In a recent study we started to investigate the anatomy of the LON using serial-section transmission electron microscopy (ssTEM) showing that PRs’ axons form large globular boutons with polyadic synapses and that the OLPs were parts of their direct targets (Sprecher et al., 2011).

Here, we mapped the synaptic wiring diagram of the LON by reconstructing all its innervating neurons from a new ssTEM volume of a whole first instar larval central nervous system (Ohyama et al., 2015). We characterized and quantified the connectivity of all previously described LON-associated neurons and identified new components in this circuit. We found per hemisphere eleven second order interneurons, two third-order interneurons and one serotonergic neuron innervating the LON, plus two unpaired octopaminergic/tyraminergic neurons contacting both hemispheres. We highlighted the separation of light signal flow at the first synapse level as the two PR subtypes connect onto distinct subsets of interneurons. Network analysis suggests that the resulting circuits may encode both ambient light intensity information and information about the changes of light intensity. Comparison with the visual circuit of the adult fruit fly highlights common principles in organization of visual information processing, for example the stratification of PRs inputs as well as the existence of distinct photoreceptor pathways that are involved in detecting temporal light cues. Furthermore, the comparison with the olfactory wiring diagram (Berck et al., 2016) highlights common strategies for early sensory information processing, relay to higher order areas such as the mushroom bodies for associative memory, and control from the central brain. By mapping the connectivity of visual circuits and analyzing its architecture we have the opportunity to study the circuit structure-function relationship and advance our understanding of how neural circuits govern behavior.

A shared characteristic of many visual systems is the retinotopic organization allowing visual processing in a spatially segregated fashion by the transformation of the surrounding environment into a 2D virtual map (for review, Sanes and Zipursky, 2010). Within the compound eye of the adult fruit fly, this is achieved by the prominent organization of PRs in ommatidia in the retina that is maintained through underlying cartridges in the lamina and columns in the medulla. The Drosophila larval eye lacks ommatidia or a similar spatial organization of PRs. Nevertheless larvae can navigate directional light gradients and form light associative memories using their simple eyes (Kane et al., 2013; von Essen et al., 2011; Humberg and Sprecher, 2017).

In this study, we described the synapse-level connectome of the larval first visual center by reconstructing neurons recursively from the optic nerves to third-order neurons following all chemical synapses in a nanometer-resolution EM volume of the whole central nervous system. We found that the two PR subtypes synapse onto distinct target interneurons, showing a clear separation of visual information flow at the first synapse level. Rh5-PRs predominantly synapse onto VPNs, which transfer light information to distinct regions including the lateral horn and the mushroom body calyx, whereas Rh6-PRs strongly synapse onto two VLNs (cha- and glu-lOLPs). Moreover, the flow of information is convergent as these two main VLNs in turn synapse onto most VPNs. These two main VLNs also receive input from both the serotonergic as well as the octopaminergic/tyraminergic systems, suggesting that their activity may be modulated by input from central brain circuitry. Thus, a key feature of the larval visual circuit is that the Rh6-PRs-pathway feeds into the Rh5-PRs-pathway, suggesting a tuning function for Rh6-PRs and the two VLNs that also integrate external modulatory inputs (Figure 2F; Figure 3—figure supplement 2). This is not excluding the possibility of electrical connections mediated by gap junctions that are not visible in the ssTEM volume.

Hypothesized functional interpretation of circuit architecture

The Rh5-PRs-VPNs pathway may provide information about the ambient light intensity

Larval PRs responses to light remain currently unknown. Moreover, compared to adult flies PRs, larval PRs lack a clear rhabdomeric structure, do not present intracellular pigment granules and the Bolwig organ is not equipped with focusing optics or other accessory cells (Green et al., 1993; Sprecher et al., 2007). Nevertheless, larval PRs express the main actors of the phototransduction pathway like adult PRs (Rosenbaum et al., 2011; Mishra et al., 2016; Bernardo-Garcia et al., 2016). It therefore remains difficult to predict how larval PRs response to light. Larval PRs might either adapt and detect the mean light intensity, like adult PRs (for review Clark and Demb, 2016), or might detect the absolute light intensity. In either case, one can propose that larval PRs provide information about the ambient light intensity of the larval environment.

In other sensory systems such as the olfactory system of the adult (Rybak et al., 2016) and larval Drosophila (Berck et al., 2016) and in the chordotonal mechanosensory systems of the locust (Yuan et al., 2011) and Drosophila larva (Ohyama et al., 2015; Jovanic et al., 2016) axonal terminals of sensory neurons receive abundant inhibitory inputs from central neurons. Such presynaptic inhibition of sensory terminals may be employed to mediate lateral inhibition (Wilson and Laurent, 2005; Olsen and Wilson, 2008), to implement divisive normalization (Olsen et al., 2010) or to encode a predicted future stimulation (Wolf and Burrows, 1995). However, in the larval visual circuit, we do not observe significant synaptic connections onto the PRs (Figures 2E and 5B), suggesting that the light information encoded by PRs is passed on with no alteration at the level of the first synapse.

We therefore propose that larval Rh5-PRs may provide information about the ambient light intensity directly onto the larval visual system output neurons, the VPNs.

The Rh6-PRs-VLNs pathway may compute variations in light intensity

Compared to Rh5-PRs that directly connect the VPNs, the Rh6-PRs inputs are relayed to the VPNs only via the two VLNs, the cha- and glu-lOLPs. In dissociated larval Pdf-LaNs, it was shown that applying acetylcholine increased their calcium response whereas applying glutamate reduced their calcium response (Wegener et al., 2004; Hamasaka et al., 2007), suggesting that acetylcholine is an excitatory neurotransmitter for these cells whereas glutamate would be inhibitory. Acetylcholine can act as an inhibitory neurotransmitter through a metabotropic muscarinic receptor (Shinomiya et al., 2014; Ren et al., 2015), however, it more often acts as an excitatory neurotransmitter in Drosophila (Baines and Bate, 1998; Burrows, 1996). If both cha and glu-lOLPs were to be excitatory, the positive feedback loop between these two cells would likely result in an enhanced signal propagation of Rh6-PRs inputs towards VPNs. Such a positive feedforward feature downstream of the two PR-subtypes could make sense if they detected qualitatively distinct visual features such as spectral cues or intensity. If for instance Rh6-PRs responded to a vastly distinct light-spectrum than Rh5-PRs or if Rh6-PRs were low-light sensitive, this positive feedforward loop could result in spectral integration or amplification of low-light input. However, absorption spectra of both larval PRs are largely overlapping and there is currently no evidence for distinct detection capacities of both PRs (Salcedo et al., 1999; Humberg and Sprecher, 2017). Therefore, in our view a more favorable scenario is that outputs from cha-lOLP are likely excitatory while the outputs from glu-lOLP are likely inhibitory, similarly as glutamate has been found to mediate inhibition in the adult fly lobula plate (Mauss et al., 2014) and in the antennal lobe (Liu and Wilson, 2013; Berck et al., 2016). Therefore, in Figures 2F and 3 one could interpret cholinergic arrows (black) as excitatory and glutamatergic arrows (red) as inhibitory (also see Figure 3—figure supplement 2).

If we consider cha-lOLP as excitatory and glu-lOLP as inhibitory, then Rh6-PRs signals appears to be positively transferred to VPNs only via the cha-lOLP (Figure 3A). In addition, cha-lOLP then receives strong inputs from the inhibitory glu-lOLP (Figures 2E and 3A), which is also almost exclusively driven by Rh6-PRs inputs. Therefore, this inhibition of glu-lOLP onto cha-lOLP could mediate a form of indirect presynaptic inhibition of the Rh6-PRs inputs. This motif made by the cholinergic Rh6-PRs driving both the cha-lOLP and the glu-lOLP, and with the glu-lOLP inhibiting the cha-lOLP, creates then an incoherent feedforward loop (Alon, 2007). Therefore this motif could make the cha-lOLP responsive to the derivative of Rh6-PRs activity, that is to the variations in light intensity. As cha-lOLP VLN is likely to be a positive relay of Rh6-PRs inputs onto VPNs, VPNs could therefore respond to increments in light intensity (ON response).

Moreover, cha-lOLP inputs onto the glu-lOLP and both cha- and glu-lOLPs further connect onto the VPNs. Considering cha-lOLP as excitatory and glu-lOLP as inhibitory, this creates a second incoherent feedforward motif making VPNs potentially responsive to the derivative of cha-lOLP inputs. As cha-lOLP inputs may already represent the first derivative of Rh6-PRs inputs, this second incoherent feedforward motif may therefore make VPNs responsive to the acceleration of light intensity raises.

In summary, glu-lOLP may provide both presynaptic inhibition of Rh6-PRs inputs by inhibiting the relay neuron cha-lOLP, and postsynaptic inhibition by directly inhibiting most VPNs. Consequently, VPNs could respond to the ambient light intensity (from Rh5-PRs) and to the variations of light intensity (from the Rh6-PRs-VLNs pathway). Interestingly, olfactory projection interneurons in the adult Drosophila also respond to a mixture of odorant concentration and of the acceleration of odorant concentration (Kim et al., 2015). Comparable to other sensory system (Klein et al., 2015; Schulze et al., 2015), a measure of changes in light intensity over time would enable light gradient navigation (Kane et al., 2013; Humberg and Sprecher, 2017).

Phasic inhibition could sharpen ON and OFF responses

In the wiring diagram, we found a glutamatergic (therefore putatively inhibitory) third-order interneuron, named VPLN and mainly driven by cha- and glu-OLPs. The timing of cha- and glu-lOLPs input may be critical for the VPLN function. If cha-lOLP input precedes glu-lOLP input, the VPLN may potentially be activated only upon an increase in light intensity via Rh6-PRs (Figure 3D). This is unlike the other glutamatergic interneuron, glu-lOLP, which receives direct inputs from PRs and therefore can be tonically active in the presence of light. The VPLN specifically synapses onto multiple VPNs (the 5th-LaN, the two nc-LaNs and PVL09) and therefore potentially inhibits these cells that also receive strong inputs from glu-lOLP (Figure 3C,E, Figure 3—figure supplement 1). In consequence, these VPNs may be subject to tonic inhibition (from glu-lOLP) under constant light conditions and to phasic inhibition (from the VPLN) upon an increase in Rh6-PRs dependent light intensity. Therefore, phasic inhibition from the VPLN may potentially refine the temporal resolution of VPNs responses to increment of light intensity (ON response).

An interesting aspect resulting from tonic inhibition of VPNs during constant light stimulation is what happens when the light intensity decreases (OFF response). Some neurons subject to tonic inhibition can have a rebound of activity when inhibition is lifted (Marder and Bucher, 2001; Hedwig, 2016). If, via this mechanism, VPNs were to increase their activity upon a decrease in light intensity, they would be encoding an OFF response. Potentially all VPNs under tonic inhibition from glu-lOLP could have this rebound of activity after a light intensity decrease. Interestingly, two cholinergic VPNs (the nc-LaN 1 and 2) synapse onto the VPLN that could then become more strongly activated by the OFF response (Figure 3D, Figure 2—source data 1). As the VPLN is inhibiting several VPNs (the 5th-LaN, the two nc-LaNs and PVL09), this could therefore create a second period of phasic inhibition allowing to maintain these VPNs OFF responses brief.

In conclusion, the connectivity of the third-order glutamatergic VPLN putatively inhibitory suggests that it may refine the temporal resolution of VPNs ON and OFF responses through phasic inhibition.

The visual circuit supports previous behavioral observations

In addition, this complete wiring diagram of the larval visual system can explain why in previous studies only Rh5-PRs appeared to be required for light avoidance while Rh6-PRs seemed dispensable in most experimental conditions (Keene et al., 2011; Kane et al., 2013; Humberg and Sprecher, 2017). Moreover, Rh6-PRs mutant larvae were shown to avoid light wavelengths from ultra-violet to green, supporting the idea that Rh5-PRs respond to a wider range of wavelength of light than only ‘blue’ light (Humberg and Sprecher, 2017; Salcedo et al., 2009). Taken together, our current data and the lack of evidence of color vision capability in larvae, we propose that the two larval PRs are rather specialized in detection of ambient light intensity and of temporal variations of light intensity.

Based on our connectomic analysis, when Rh6-PRs are mutated or functionally silenced, Rh5-PRs may still provide light ambient intensity information, and the cholinergic inputs from nc-LaNs onto the glutamatergic VPLN could inhibit the VPNs, computing on its own some response to changes in light intensity. Blocking the VPLN activity in a Rh6-PRs depletion background would allow to study whether ambient light information is sufficient for visual navigation. Moreover, when Rh5-PRs are disabled, VPNs do not receive ambient light information while potentially being under tonic inhibition from the glu-lOLP, which therefore could shut down their activity. Given that in Rh5-PRs depletion background, larval visual responses are highly defective, this further suggests that ON and OFF responses alone are not sufficient to allow larval light avoidance. We therefore propose that it may need both a baseline activity of VPNs, provided by ambient light intensity information, and the modulations of this baseline activity in response to light intensity variations.

Only the Pdf-LaNs involved in circadian rhythm receive direct inputs from both PRs subtypes and can therefore still receive ambient light information in either PRs’ depletion condition. This broad light information integration capacity is in agreement with evidence that both PRs subtypes are sufficient to entrain the larval clock (Keene et al., 2011). While further reconstructions of their postsynaptic partners are required, the four Pdf-LaNs appear identical in sensory inputs, local connections and anatomy, raising the question of what such redundancy would allow.

Comparisons between the larval eye and adult compound eye

The basic organization of the visual system in the larva, the adults fly as well as with the visual circuit of vertebrates show several similarities and possible shared characteristics (Figure 6). Several possible interpretations of the photoreceptor types as well as circuit motifs may be derived. One possible scenario lies in the comparison between PR types found in the different eye types and their known or putative roles in temporal coding as discussed here.

Figure 6

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First, these three visual systems have each two main types of photo-sensory neurons: Rh5- and Rh6-PRs for the Drosophila larva, inner and outer PRs for adult flies, cones and rods for vertebrates (Sprecher et al., 2007; Sprecher and Desplan, 2008; Friedrich, 2008; Sanes and Zipursky, 2010). Here we also confirmed that the LON was organized in layers (LONd, LONi, LONp) similarly as the adult flies optic lobe (lamina, medulla) and the vertebrate retina (outer and inner plexiform layers) (Sanes and Zipursky, 2010, Figure 6). Moreover, the mode of development of Drosophila larval and adult eyes reinforces similarities between Rh5-PRs with an inner-PR type and Rh6-PRs with an outer-PR type: in the adult, R8-PR precursors are formed first to recruit outer PRs, likewise in the larva, Rh5-PR precursors develop first and then recruit the Rh6-PRs, in both cases via the EGFR pathway (Sprecher et al., 2007). Also, development of both inner PRs and Rh5-PRs depend on the transcription factors senseless and spalt (Sprecher et al., 2007; Sprecher and Desplan, 2008; Mishra et al., 2013). Finally, the inputs from serotonergic and octopaminergic/tyraminergic neurons onto the LON are also a shared feature with the adult visual system where serotonin has been linked to circadian rhythmicity (Yuan et al., 2005) and where visual cues during flight are modulated by octopaminergic inputs (Suver et al., 2012; Wasserman et al., 2015). In the LON, our data suggest that the serotonergic neuron SP2-1 and octopaminergic/tyraminergic neurons sVUM might modulate the sensitivity to light increment and decrement (ON/OFF) by directly connecting the cha- and glu-lOLPs VLNs. These ON and OFF responses might be further affected by inputs from SP2-1 onto the VPLN.

A potential functional comparison between the larval and the adult visual system emerge from the similar neurotransmitters expressed and the functions proposed for the larval VLNs cha- and glu-lOLPs and the adult glutamatergic L1 and cholinergic L2 interneurons of the lamina (Figure 6A,B; Gao et al., 2008). In the adult fly, the outer R1-6 PRs connect to L1 and L2 interneurons that convey distinct responses to light increment (ON) and decrement (OFF) (Joesch et al., 2010; Clark et al., 2011; Strother et al., 2014; Behnia et al., 2014). The adult PRs are histaminergic and induce hyperpolarization (inhibition) in both L1 and L2 upon light increment, followed by a rebound of activity of these two cells upon light decrement (Hardie, 1987; Reiff et al., 2010; Clark et al., 2011); reviewed in Borst and Helmstaedter, 2015). Therefore upon light increment, PRs inhibit the glutamatergic L1, which results in the disinhibition of the downstream targets of L1 (ON response). In turn, upon light decrement PRs inhibit the cholinergic L2 less, which results in the activation of the downstream targets of L2 (OFF response). However, the larval PRs are cholinergic (Yasuyama et al., 1995; Keene et al., 2011) and, at least for the Pdf-LaNs (Yuan et al., 2011), excite their targets activity in response of light. Therefore in larvae, an ON response could result from an increase of excitation from cha-lOLP onto VPNs when light intensity increases (via the increase of Rh6-PRs inputs) and could be kept transient by inhibition from the glu-lOLP (indirect presynaptic inhibition of Rh6-PRs inputs) and by phasic inhibition from the VPLN. In turn, an OFF response could result from the disinhibition of VPNs from glu-lOLP inhibition when light intensity decreases and may also be kept transient by phasic inhibition from the VPLN. Therefore, whereas the glutamatergic L1 conveys the ON response and the cholinergic L2 conveys the OFF response in adult flies, we propose that the glu-lOLP could convey the OFF response and the cha-lOLP could convey the ON response in larvae (Figure 6A,B). Another similarity between the two lOLPs and the adult L1 and L2 is that each lOLP receives an equivalent number of inputs from each Rh6-PRs (about 20 synapses in average, Figure 2—source data 1), similarly as adult L1 and L2 receives about 50 inputs from each R1-6 PRs (Meinertzhagen, 1989), suggesting that the information transfer could have a similarly high fidelity. However, while ON/OFF responses in adult flies and vertebrates (Figure 6B,C) are involved in motion detection, such ability within one eye is achieved through downstream direction-sensitive cells that integrate information from several points in space (Clark and Demb, 2016). As larval eyes lack ommatidia such capacity seems unlikely, however the ON/OFF detection could already suffice for larval visual navigation (Kane et al., 2013; Klein et al., 2015; Schulze et al., 2015; Humberg and Sprecher, 2017). Another important difference between the larval and adult systems is that in the LON the cha- and glu-lOLPs are strongly interconnected and both input onto the same targets, whereas in the adult fly, the L1 and L2 are not chemically connected (only electrically, Joesch et al., 2010) and the ON/OFF pathways are separated for two additional synaptic levels before converging on direction-sensitive cells in the lobula plate (Takemura et al., 2013; Clark and Demb, 2016). Consequently, whereas the adult L1 and L2 have similar responses to light (Clark et al., 2011; Borst and Helmstaedter, 2015), the reciprocal connections between cha- and glu-lOLPs may uniquely shape the light response of these two cells.

If the Rh6-PRs-VLNs pathway contributes indeed to a function related to light increment or decrement remains hypothetical. Moreover, since Rh5-PRs survive metamorphosis giving rise to the adult Hofbauer-Buchner eyelet, it is possible that the larval visual circuit more closely resembles the eyelet circuitry than the one of the adult compound eye (Sprecher and Desplan, 2008).

Comparison between the visual and the olfactory first-order processing centers

The LON neural network presents many similarities with the larval olfactory wiring diagram (Berck et al., 2016), favoring a potential common organizational origin of these sensory neuropils as suggested before (Strausfeld, 1989; Strausfeld et al., 2007). Odorant cues are perceived by olfactory receptor neurons that project to the antennal lobe where they contact olfactory projection interneurons and olfactory local interneurons. Similarly to visual circuits, sensory inputs in the antennal lobe are segregated in olfactory receptor specific domains termed glomeruli (Fishilevich et al., 2005; Masuda-Nakagawa et al., 2009). Most olfactory receptor neurons and olfactory projection interneurons are cholinergic like PRs and VPNs (Keene et al., 2011; Yasuyama and Salvaterra, 1999; Python and Stocker, 2002), and we find glutamatergic, potentially inhibitory, local interneurons in both systems (Berck et al., 2016). Reciprocal synapses between cha-lOLP and glu-lOLP in the visual circuit may be functionally equivalent to the connections between some olfactory receptor neurons and the glutamatergic Picky olfactory local interneuron 0 of the antennal lobe, suggesting that this reciprocal motif in the LON could indeed contribute to detecting changes in light intensity by computing the first derivative of the stimulus (Berck et al., 2016). Additionally, we can observe presynaptic and postsynaptic inhibition in both sensory systems while the strategies of implementation are somewhat different. Interestingly, we observed that most projection interneurons of both sensory systems may bring a mixture of stimulus intensity and acceleration in stimulus intensity to the lateral horn and to the mushroom body calyx (Figure 1—figure supplement 3; Kim et al., 2015). Finally, both sensory systems are modulated by aminergic neurons inputs on specifics local interneurons. Interestingly, both the lOLPs VLNs and the olfactory Broad local interneurons Trio form feedback synapses onto the axonal termini of their respective bilateral octopaminergic/tyraminerigc neurons while this is not the case for serotonergic neurons (Berck et al., 2016).

Concluding remarks

Identification of synaptic connectivity and neurotransmitter identity within the larval visual circuit allows us to formulate clear predictions on the response profile and function of individual network components. Based on the circuit map we suggest that the Rh6-PRs-VLNs pathway might be required for the detection of light intensity changes, whereas the Rh5-PRs-VPNs pathway could provide direct ambient light intensity information. In the future, behavioral studies or physiological activity recording of visual circuit neurons will allow to add additional layers onto this functional map.

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Author details

1. Ivan Larderet

   Department of Biology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Contributed equally with

   Pauline MJ Fritsch

   Competing interests

   No competing interests declared

2. Pauline MJ Fritsch

   Department of Biology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Contributed equally with

   Ivan Larderet

   Competing interests

   No competing interests declared

3. Nanae Gendre

   Department of Biology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Data curation, Visualization, Methodology

   Competing interests

   No competing interests declared

4. G Larisa Neagu-Maier

   Department of Biology, University of Fribourg, Fribourg, Switzerland

   Contribution

   Data curation, Formal analysis, Visualization, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

5. Richard D Fetter

   Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

   Contribution

   Resources, Data curation, Methodology

   Competing interests

   No competing interests declared

6. Casey M Schneider-Mizell

   Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

   Contribution

   Resources, Data curation, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9477-3853

7. James W Truman

   Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

   Contribution

   Conceptualization, Resources, Formal analysis, Investigation, Visualization, Writing—review and editing

   Competing interests

   No competing interests declared

8. Marta Zlatic

   Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

   Contribution

   Resources, Data curation, Investigation

   Competing interests

   No competing interests declared

9. Albert Cardona

   Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States

   Contribution

   Conceptualization, Resources, Data curation, Software, Investigation, Visualization, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4941-6536

10. Simon G Sprecher

    Department of Biology, University of Fribourg, Fribourg, Switzerland

    Contribution

    Conceptualization, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

    For correspondence

    simon.sprecher@gmail.com

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0001-9060-3750

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