Dataset Information

Developmental Easing of Short-Term Depression in "Winner" Climbing Fibers.

ABSTRACT: The postnatal development of cerebellar climbing fiber (CF) to Purkinje neuron (PN) synapses is characterized by a substantial pruning during the first 3 weeks after birth, switching from multiple- to single-CF innervation. Previous studies suggested that CF maturation is governed by bidirectional changes of synaptic plasticity. The strengthening of surviving "winner" CFs, which translocate from the PN soma to the dendrite, is thought to be guided by long-term potentiation (LTP), while weakening of to-be-eliminated "loser" CFs, which remain on the soma, was proposed to be due to long-term depression (LTD). However, there are conflicting results from previous studies, whether or not strengthening of winner and weakening of loser CFs during postnatal development is accompanied by changes in short-term plasticity and, thus, whether pre- or postsynaptic forms of LTD and LTP are operational. We, therefore, analyzed the developmental profile of paired-pulse depression (PPD) in "weak" and "strong" CFs in 3-21-day old Igsf9-eGFP mice, which allow visual identification of GFP-labeled CFs. We found that in 3-8-day old mice strong CFs are marked by a stronger PPD compared to weak CFs. Surprisingly, PPD of strong CFs eases during maturation, while PPD in weak CFs remains unchanged. This easing of PPD is neither due to changes in presynaptic influx-release coupling nor to an increased saturation of postsynaptic receptors. Thus, our results imply that synaptic contacts of CFs show distinct features of PPD depending on their affiliation to winner or loser CFs and depending on their somatic or dendritic location.

SUBMITTER: Patz C

PROVIDER: S-EPMC6504704 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Developmental Easing of Short-Term Depression in "Winner" Climbing Fibers.

Pätz Christina C Brachtendorf Simone S Eilers Jens J

Frontiers in cellular neuroscience 20190501

The postnatal development of cerebellar climbing fiber (CF) to Purkinje neuron (PN) synapses is characterized by a substantial pruning during the first 3 weeks after birth, switching from multiple- to single-CF innervation. Previous studies suggested that CF maturation is governed by bidirectional changes of synaptic plasticity. The strengthening of surviving "winner" CFs, which translocate from the PN soma to the dendrite, is thought to be guided by long-term potentiation (LTP), while weakening ...[more]

PMID: 31118890

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Project description:A crucial issue in understanding cerebellar function is the interaction between simple spike (SS) and complex spike (CS) discharge, the two fundamentally different activity modalities of Purkinje cells. Although several hypotheses have provided insights into the interaction, none fully explains or is completely consistent with the spectrum of experimental observations. Here, we show that during a pseudo-random manual tracking task in the monkey (Macaca mulatta), climbing fiber discharge dynamically controls the information present in the SS firing, triggering robust and rapid changes in the SS encoding of motor signals in 67% of Purkinje cells. The changes in encoding, tightly coupled to CS occurrences, consist of either increases or decreases in the SS sensitivity to kinematics or position errors and are not due to differences in SS firing rates or variability. Nor are the changes in sensitivity due to CS rhythmicity. In addition, the CS-coupled changes in encoding are not evoked by changes in kinematics or position errors. Instead, CS discharge most often leads alterations in behavior. Increases in SS encoding of a kinematic parameter are associated with larger changes in that parameter than are decreases in SS encoding. Increases in SS encoding of position error are followed by and scale with decreases in error. The results suggest a novel function of CSs, in which climbing fiber input dynamically controls the state of Purkinje cell SS encoding in advance of changes in behavior.SIGNIFICANCE STATEMENT Purkinje cells, the sole output of the cerebellar cortex, manifest two fundamentally different activity modalities, complex spike (CS) discharge and simple spike (SS) firing. Elucidating cerebellar function will require an understanding of the interactions, both short- and long-term, between CS and SS firing. This study shows that CSs dynamically control the information encoded in a Purkinje cell's SS activity by rapidly increasing or decreasing the SS sensitivity to kinematics and/or performance errors independent of firing rate. In many cases, the CS-coupled shift in SS encoding leads a change in behavior. These novel findings on the interaction between CS and SS firing provide for a new hypothesis in which climbing fiber input adjusts the encoding of SS information in advance of a change in behavior.

Dataset Information

Developmental Easing of Short-Term Depression in "Winner" Climbing Fibers.

Publications

Developmental Easing of Short-Term Depression in "Winner" Climbing Fibers.

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