Abstract
Animals use spatial differences in environmental light levels for visual navigation; however, how light inputs are translated into coordinated motor outputs remains poorly understood. Here we reconstruct the neuronal connectome of a four-eye visual circuit in the larva of the annelid Platynereis using serial-section transmission electron microscopy. In this 71-neuron circuit, photoreceptors connect via three layers of interneurons to motorneurons, which innervate trunk muscles. By combining eye ablations with behavioral experiments, we show that the circuit compares light on either side of the body and stimulates body bending upon left-right light imbalance during visual phototaxis. We also identified an interneuron motif that enhances sensitivity to different light intensity contrasts. The Platynereis eye circuit has the hallmarks of a visual system, including spatial light detection and contrast modulation, illustrating how image-forming eyes may have evolved via intermediate stages contrasting only a light and a dark field during a simple visual task.
Highlights
Guided behavior is widespread in animals (Ullén et al, 1997; Garm et al, 2007; Orger et al, 2008; Burgess et al, 2010; Huang et al, 2013), yet the underlying neuronal circuits and their evolutionary origins remain poorly understood
We identified the eyes based on the presence of pigment-filled vesicles in the pigment cells, the presence of a lens formed by the apical extensions of the pigment cells, and the presence of the apical microvillar extensions of the photoreceptors (Rhode, 1992; Randel et al, 2013; Figure 1D; Video 2)
We identified 21 photoreceptor cells (PRC), 42 interneurons (IN) and 8 motorneurons (MN) (Figure 1—figure supplement 1–4), forming a ‘minimal eye circuit’ from sensors to effectors
Summary
Guided behavior is widespread in animals (Ullén et al, 1997; Garm et al, 2007; Orger et al, 2008; Burgess et al, 2010; Huang et al, 2013), yet the underlying neuronal circuits and their evolutionary origins remain poorly understood. A comprehensive description of the sensory-motor visual circuitry, including all neurons and their synaptic connectivity, is required for a plausible explanation of how visual inputs drive motor output during animal behavior. This can only be achieved using electron microscopic imaging to construct connectomes, comprehensive synaptic-level connectivity maps for large blocks of neural tissue containing behaviorally relevant circuits (Bock et al, 2011; Briggman et al, 2011; Jarrell et al, 2012; Bumbarger et al, 2013; Helmstaedter et al, 2013). Despite recent advances in the connectomics of visual systems (Briggman et al, 2011; Rivera-Alba et al, 2011; Sprecher et al, 2011; Takemura et al, 2011, 2013), a complete synaptic-level connectivity-map of a visual circuit, including sensory-, inter-, and motorneurons, has not yet been described
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