Input-Specific Plasticity and Homeostasis at the Drosophila Larval Neuromuscular Junction

Zachary L Newman; Adam Hoagland; Krishan Aghi; Kurtresha Worden; Sabrina L Levy; Jun Ho Son; Luke P Lee; Ehud Y Isacoff

doi:10.1016/j.neuron.2017.02.028

Input-Specific Plasticity and Homeostasis at the Drosophila Larval Neuromuscular Junction

Neuron. 2017 Mar 22;93(6):1388-1404.e10. doi: 10.1016/j.neuron.2017.02.028. Epub 2017 Mar 9.

Authors

Zachary L Newman¹, Adam Hoagland¹, Krishan Aghi², Kurtresha Worden¹, Sabrina L Levy¹, Jun Ho Son³, Luke P Lee⁴, Ehud Y Isacoff⁵

Affiliations

¹ Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
² Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA.
³ Department of Bioengineering, University of California, Berkeley, Berkeley, CA 94720, USA; Berkeley Sensor and Actuator Center, University of California, Berkeley, Berkeley, CA 94720, USA.
⁴ Department of Bioengineering, University of California, Berkeley, Berkeley, CA 94720, USA; Berkeley Sensor and Actuator Center, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Electrical Engineering and Computer Sciences, University of California, Berkeley, Berkeley, CA 94720, USA; Biomedical Institute for Global Health Research and Technology, National University of Singapore, 119077 Singapore, Singapore.
⁵ Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA; Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA; Bioscience Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA. Electronic address: ehud@berkeley.edu.

Abstract

Synaptic connections undergo activity-dependent plasticity during development and learning, as well as homeostatic re-adjustment to ensure stability. Little is known about the relationship between these processes, particularly in vivo. We addressed this with novel quantal resolution imaging of transmission during locomotive behavior at glutamatergic synapses of the Drosophila larval neuromuscular junction. We find that two motor input types, Ib and Is, provide distinct forms of excitatory drive during crawling and differ in key transmission properties. Although both inputs vary in transmission probability, active Is synapses are more reliable. High-frequency firing "wakes up" silent Ib synapses and depresses Is synapses. Strikingly, homeostatic compensation in presynaptic strength only occurs at Ib synapses. This specialization is associated with distinct regulation of postsynaptic CaMKII. Thus, basal synaptic strength, short-term plasticity, and homeostasis are determined input-specifically, generating a functional diversity that sculpts excitatory transmission and behavioral function.

Keywords: CaMKII; Drosophila melanogaster; homeostatic plasticity; input-specific plasticity; neuromuscular junction; optical quantal analysis; release probability; short-term plasticity.

MeSH terms

Animals
Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
Drosophila melanogaster* / cytology
Drosophila melanogaster* / growth & development
Homeostasis / physiology*
Larva / cytology
Larva / physiology
Locomotion / physiology*
Neural Inhibition / physiology
Neuromuscular Junction / metabolism
Neuromuscular Junction / physiology*
Neuronal Plasticity / physiology*
Synaptic Transmission

Substances

Calcium-Calmodulin-Dependent Protein Kinase Type 2

Abstract

MeSH terms

Substances

Grants and funding