Directional mechanoreception by hair cells is transmitted to the brain via afferent neurons to enable postural control and rheotaxis. Neuronal tuning to individual directions of mechanical flow occurs when each peripheral axon selectively synapses with multiple hair cells of identical planar polarization. How such mechanosensory labeled lines are established and maintained remains unsolved. Here, we use the zebrafish lateral line to reveal that asymmetric activity of the transcription factor Emx2 diversifies hair cell identity to instruct polarity-selective synaptogenesis. Unexpectedly, presynaptic scaffolds and coherent hair cell orientation are dispensable for synaptic selectivity, indicating that epithelial planar polarity and synaptic partner matching are separable. Moreover, regenerating axons recapitulate synapses with hair cells according to Emx2 expression but not global orientation. Our results identify a simple cellular algorithm that solves the selectivity task even in the presence of noise generated by the frequent receptor cell turnover. They also suggest that coupling connectivity patterns to cellular identity rather than polarity relaxes developmental and evolutionary constraints to innervation of organs with differing orientation.

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Summary We present a protocol to characterize the morphological properties of individual neurons reconstructed from microscopic imaging. We first describe a simple procedure to extract relevant morphological features from digital tracings of neural arbors. Then, we provide detailed steps on classification, clustering, and statistical analysis of the traced cells based on morphological features. We illustrate the pipeline design using specific examples from zebrafish anatomy. Our approach can be readily applied and generalized to the characterization of axonal, dendritic, or glial geometry. For complete context and scientific motivation for the studies and datasets used here, refer to Valera et al. (2021) .

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