The Synaptic Vesicle Priming Protein CAPS-1 Shapes the Adaptation of Sensory Evoked Responses in Mouse Visual Cortex

• Published in: Cell reports (Cambridge) 2020-03, Vol.30 (10), p.3261-3269.e4
• Main Authors: Nestvogel, Dennis B., Merino, Ricardo Martins, Leon-Pinzon, Carolina, Schottdorf, Manuel, Lee, ChoongKu, Imig, Cordelia, Brose, Nils, Rhee, Jeong-Seop
• Format: Article
• Language: English
• Subjects: Acute Brain slice Patch technique; Adaptation, Ocular; Animals; Ca2+- dependent Activator Protein for Secretion (CAPS); Calcium-Binding Proteins - metabolism; Evoked Potentials - physiology; Gene Deletion; in-vivo patch clamp technique; Mice, Knockout; Nerve Tissue Proteins - metabolism; Neurons - metabolism; Optogenetic Stimulation; Sensation; Sensory Adaptation; Synaptic Transmission; Synaptic Vesicle Priming; Synaptic Vesicles - metabolism; Visual Cortex; Visual Cortex - physiology
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2020.02.045

Short-term plasticity gates information transfer across neuronal synapses and is thought to be involved in fundamental brain processes, such as cortical gain control and sensory adaptation. Neurons employ synaptic vesicle priming proteins of the CAPS and Munc13 families to shape short-term plasticity in vitro, but the relevance of this phenomenon for information processing in the intact brain is unknown. By combining sensory stimulation with in vivo patch-clamp recordings in anesthetized mice, we show that genetic deletion of CAPS-1 in thalamic neurons results in more rapid adaptation of sensory-evoked subthreshold responses in layer 4 neurons of the primary visual cortex. Optogenetic experiments in acute brain slices further reveal that the enhanced adaptation is caused by more pronounced short-term synaptic depression. Our data indicate that neurons engage CAPS-family priming proteins to shape short-term plasticity for optimal sensory information transfer between thalamic and cortical neurons in the intact brain in vivo. [Display omitted] •Analysis of CAPS-family priming proteins in thalamocortical synapses in vitro and in vivo•CAPSs control synaptic depression triggered by action potential trains in vitro•CAPSs control adaptation of sensory-evoked responses in layer 4 neurons of V1 in vivo Nestvogel et al. perform patch-clamp recordings of layer 4 neurons in the primary visual cortex of anesthetized mice to demonstrate that CAPS-family vesicle priming proteins control synaptic short-term plasticity and adaptation of sensory-evoked thalamocortical synaptic transmission, linking the action of dedicated vesicle priming proteins to sensory processing in vivo.