The organization of the gravity-sensing system in zebrafish

Abstract

Motor circuits develop in sequence from those governing fast movements to those governing slow. Here we examine whether upstream sensory circuits are organized by similar principles. Using serial-section electron microscopy in larval zebrafish, we generated a complete map of the gravity-sensing (utricular) system from the inner ear to the brainstem. We find that both sensory tuning and developmental sequence are organizing principles of vestibular topography. Patterned rostrocaudal innervation from hair cells to afferents creates a directional tuning map in the utricular ganglion, forming segregated pathways for rostral and caudal tilt. Furthermore, the mediolateral axis of the ganglion is linked to both developmental sequence and temporal kinetics. Early-born pathways carrying phasic information preferentially excite fast escape circuits, whereas later-born pathways carrying tonic signals excite slower postural and oculomotor circuits. These results demonstrate that vestibular circuits are organized by tuning direction and kinetics, aligning them with downstream motor circuits and behaviors.

Tiltable objective microscope visualizes discrimination of static and dynamic head movement originates at hair cells

“…This activity pattern was consistent with the morphological hair-bundle polarity (6 utricles, Fig. 2c) 23,27,28 .…”

“…The direction and length of the vector represented the preferred/antipreferred direction and response amplitude, respectively. In a utricle in Figure 2f, response vector orientation was consistent with the morphological hair-bundle polarity 23,27,28 . Response amplitude appeared, on the other hand, inhomogeneous across the utricle; the amplitude was larger in the midrostral and mid-caudal regions in the medial half in the utricle.…”

“…Previous morphological studies showed the hair-bundle polarity in larval zebra sh (Fig. 2a) 23,27,28 , but HC activity during head tilt has never been studied. In order to image utricular HC activity in vivo, we generated a transgenic zebra sh, Tg(myo6b:jGCaMP7f), that expressed a genetically encoded Ca 2+ indicator (GECI) in the HCs, and crossed the sh with Tg(myo6b:tdTomato) 29 , which expressed a red uorescent protein in the HCs.…”

“…This spatial distribution of the HC direction selectivity was consistent with the morphofunctional hair-bundle polarity (Figs. 2g and 3f) 23,27,28 . In the 6 utricles, pitch vibration activated 34 ± 5.9 HCs (46.4 ± 5.8%) whereas 51 ± 8.8 cells were not activated; roll vibration activated 39 ± 3.9 HCs (41.3 ± 8.3%) whereas 47 ± 7.1 cells were not activated (mean ± standard error of the mean [SEM]).…”

“…The transparent brain enabled brain-wide functional imaging during vestibular stimulation 20,21 . Inferred VGN responses to phasic stimulus and morphological connectivity from HCs to the brain have been reported 22,23 . However, due to a lack of appropriate methods, how the spatio-temporal information on head movement is transduced in the vestibular periphery has not yet been functionally examined.…”