Synaptic mechanisms for associative learning in the cerebellar nuclei

Robin Broersen, Catarina Albergaria, Daniela Carulli, Megan R. Carey (), Cathrin B. Canto () and Chris I. Zeeuw ()
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Robin Broersen: Royal Netherlands Academy of Arts and Sciences
Catarina Albergaria: Champalimaud Center for the Unknown
Daniela Carulli: Royal Netherlands Academy of Arts and Sciences
Megan R. Carey: Champalimaud Center for the Unknown
Cathrin B. Canto: Royal Netherlands Academy of Arts and Sciences
Chris I. Zeeuw: Royal Netherlands Academy of Arts and Sciences

Nature Communications, 2023, vol. 14, issue 1, 1-18

Abstract: Abstract Associative learning during delay eyeblink conditioning (EBC) depends on an intact cerebellum. However, the relative contribution of changes in the cerebellar nuclei to learning remains a subject of ongoing debate. In particular, little is known about the changes in synaptic inputs to cerebellar nuclei neurons that take place during EBC and how they shape the membrane potential of these neurons. Here, we probed the ability of these inputs to support associative learning in mice, and investigated structural and cell-physiological changes within the cerebellar nuclei during learning. We find that optogenetic stimulation of mossy fiber afferents to the anterior interposed nucleus (AIP) can substitute for a conditioned stimulus and is sufficient to elicit conditioned responses (CRs) that are adaptively well-timed. Further, EBC induces structural changes in mossy fiber and inhibitory inputs, but not in climbing fiber inputs, and it leads to changes in subthreshold processing of AIP neurons that correlate with conditioned eyelid movements. The changes in synaptic and spiking activity that precede the CRs allow for a decoder to distinguish trials with a CR. Our data reveal how structural and physiological modifications of synaptic inputs to cerebellar nuclei neurons can facilitate learning.

Date: 2023
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DOI: 10.1038/s41467-023-43227-w

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