Antagonistic Inhibitory Circuits Integrate Visual and Gravitactic Behaviors

Michaela Bostwick; Eleanor L Smith; Cezar Borba; Erin Newman-Smith; Iraa Guleria; Matthew J Kourakis; William C Smith

doi:10.1016/j.cub.2019.12.017

Antagonistic Inhibitory Circuits Integrate Visual and Gravitactic Behaviors

Curr Biol. 2020 Feb 24;30(4):600-609.e2. doi: 10.1016/j.cub.2019.12.017. Epub 2020 Jan 30.

Authors

Michaela Bostwick¹, Eleanor L Smith², Cezar Borba³, Erin Newman-Smith⁴, Iraa Guleria³, Matthew J Kourakis⁵, William C Smith⁶

Affiliations

¹ Department of Psychological and Brain Sciences, University of California, Santa Barbara, Santa Barbara, CA 93106, USA.
² Department of Neurobiology, Physiology, and Behavior, University of California, Davis, Davis, CA 95616, USA.
³ Department of Molecular, Cell and Developmental Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA.
⁴ Department of Molecular, Cell and Developmental Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA; Neuroscience Research Institute, University of California, Santa Barbara, Santa Barbara, CA 93106, USA.
⁵ Neuroscience Research Institute, University of California, Santa Barbara, Santa Barbara, CA 93106, USA.
⁶ Department of Molecular, Cell and Developmental Biology, University of California, Santa Barbara, Santa Barbara, CA 93106, USA; Neuroscience Research Institute, University of California, Santa Barbara, Santa Barbara, CA 93106, USA. Electronic address: w_smith@ucsb.edu.

Abstract

Larvae of the tunicate Ciona intestinalis possess a central nervous system of 177 neurons. This simplicity has facilitated the generation of a complete synaptic connectome. As chordates and the closest relatives of vertebrates, tunicates promise insight into the organization and evolution of vertebrate nervous systems. Ciona larvae have several sensory systems, including the ocellus and otolith, which are sensitive to light and gravity, respectively. Here, we describe circuitry by which these two are integrated into a complex behavior: the rapid reorientation of the body followed by upward swimming in response to dimming. Significantly, the gravity response causes an orienting behavior consisting of curved swims in downward-facing larvae but only when triggered by dimming. In contrast, the majority of larvae facing upward do not respond to dimming with orientation swims-but instead swim directly upward. Under constant light conditions, the gravity circuit appears to be inoperable, and both upward and downward swims were observed. Using connectomic and neurotransmitter data, we propose a circuit model that can account for these behaviors. The otolith consists of a statocyst cell and projecting excitatory sensory neurons (antenna cells). Postsynaptic to the antenna cells are a group of inhibitory primary interneurons, the antenna relay neurons (antRNs), which then project asymmetrically to the right and left motor units, thereby mediating curved orientation swims. Also projecting to the antRNs are inhibitory photoreceptor relay interneurons. These interneurons appear to antagonize the otolith circuit until they themselves are inhibited by photoreceptors in response to dimming, thus providing a triggering circuit.

Keywords: Ciona; connectome; gravitaxis; multisensory integration; neural circuit.

Publication types

Research Support, N.I.H., Extramural

MeSH terms

Animals
Central Nervous System / physiology
Ciona intestinalis / growth & development
Ciona intestinalis / physiology*
Gravitation
Larva / growth & development
Larva / physiology
Neurons / physiology
Phototaxis
Swimming / physiology*
Taxis Response*

Grants and funding

R01 NS103774/NS/NINDS NIH HHS/United States