Central Vestibular Tuning Arises from Patterned Convergence of Otolith Afferents

Neuron. 2020 Nov 25;108(4):748-762.e4. doi: 10.1016/j.neuron.2020.08.019. Epub 2020 Sep 15.


As sensory information moves through the brain, higher-order areas exhibit more complex tuning than lower areas. Though models predict that complexity arises via convergent inputs from neurons with diverse response properties, in most vertebrate systems, convergence has only been inferred rather than tested directly. Here, we measure sensory computations in zebrafish vestibular neurons across multiple axes in vivo. We establish that whole-cell physiological recordings reveal tuning of individual vestibular afferent inputs and their postsynaptic targets. Strong, sparse synaptic inputs can be distinguished by their amplitudes, permitting analysis of afferent convergence in vivo. An independent approach, serial-section electron microscopy, supports the inferred connectivity. We find that afferents with similar or differing preferred directions converge on central vestibular neurons, conferring more simple or complex tuning, respectively. Together, these results provide a direct, quantifiable demonstration of feedforward input convergence in vivo.

Keywords: body balance; electrical synapse; feedforward excitation; high-pass tuning; neural computation; sensorimotor transformation; sensory encoding; vestibulospinal neuron.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Electric Stimulation
  • Evoked Potentials, Somatosensory / physiology
  • Gene Knock-In Techniques
  • Microscopy, Electron
  • Neurons / physiology
  • Neurons / ultrastructure
  • Neurons, Afferent / physiology*
  • Neurons, Afferent / ultrastructure
  • Otolithic Membrane / physiology*
  • Vestibular Nuclei / physiology*
  • Vestibular Nuclei / ultrastructure
  • Zebrafish