Electrical coupling controls dimensionality and chaotic firing of inferior olive neurons.
Action Potentials
Animals
Bayes Theorem
Cerebellum
/ physiology
Computer Simulation
Female
Gap Junctions
/ physiology
Models, Neurological
Models, Statistical
Neurons
/ physiology
Nonlinear Dynamics
Olivary Nucleus
/ physiology
Picrotoxin
/ pharmacology
Probability
Purkinje Cells
/ physiology
Rats
Rats, Sprague-Dawley
Synapses
/ physiology
gamma-Aminobutyric Acid
/ physiology
Journal
PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
05
11
2019
accepted:
18
06
2020
revised:
11
08
2020
pubmed:
31
7
2020
medline:
4
9
2020
entrez:
31
7
2020
Statut:
epublish
Résumé
We previously proposed, on theoretical grounds, that the cerebellum must regulate the dimensionality of its neuronal activity during motor learning and control to cope with the low firing frequency of inferior olive neurons, which form one of two major inputs to the cerebellar cortex. Such dimensionality regulation is possible via modulation of electrical coupling through the gap junctions between inferior olive neurons by inhibitory GABAergic synapses. In addition, we previously showed in simulations that intermediate coupling strengths induce chaotic firing of inferior olive neurons and increase their information carrying capacity. However, there is no in vivo experimental data supporting these two theoretical predictions. Here, we computed the levels of synchrony, dimensionality, and chaos of the inferior olive code by analyzing in vivo recordings of Purkinje cell complex spike activity in three different coupling conditions: carbenoxolone (gap junctions blocker), control, and picrotoxin (GABA-A receptor antagonist). To examine the effect of electrical coupling on dimensionality and chaotic dynamics, we first determined the physiological range of effective coupling strengths between inferior olive neurons in the three conditions using a combination of a biophysical network model of the inferior olive and a novel Bayesian model averaging approach. We found that effective coupling co-varied with synchrony and was inversely related to the dimensionality of inferior olive firing dynamics, as measured via a principal component analysis of the spike trains in each condition. Furthermore, for both the model and the data, we found an inverted U-shaped relationship between coupling strengths and complexity entropy, a measure of chaos for spiking neural data. These results are consistent with our hypothesis according to which electrical coupling regulates the dimensionality and the complexity in the inferior olive neurons in order to optimize both motor learning and control of high dimensional motor systems by the cerebellum.
Identifiants
pubmed: 32730255
doi: 10.1371/journal.pcbi.1008075
pii: PCOMPBIOL-D-19-01931
pmc: PMC7419012
doi:
Substances chimiques
Picrotoxin
124-87-8
gamma-Aminobutyric Acid
56-12-2
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1008075Subventions
Organisme : NINDS NIH HHS
ID : R56 NS100528
Pays : United States
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
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