title: Sloppiness in spontaneously active neuronal networks.
abstract: Various plasticity mechanisms, including experience-dependent, spontaneous, as well as homeostatic ones, continuously remodel neural circuits. Yet, despite fluctuations in the properties of single neurons and synapses, the behavior and function of neuronal assemblies are generally found to be very stable over time. This raises the important question of how plasticity is coordinated across the network. To address this, we investigated the stability of network activity in cultured rat hippocampal neurons recorded with high-density multielectrode arrays over several days. We used parametric models to characterize multineuron activity patterns and analyzed their sensitivity to changes. We found that the models exhibited sloppiness, a property where the model behavior is insensitive to changes in many parameter combinations, but very sensitive to a few. The activity of neurons with sloppy parameters showed faster and larger fluctuations than the activity of a small subset of neurons associated with sensitive parameters. Furthermore, parameter sensitivity was highly correlated with firing rates. Finally, we tested our observations from cell cultures on an in vivo recording from monkey visual cortex and we confirm that spontaneous cortical activity also shows hallmarks of sloppy behavior and firing rate dependence. Our findings suggest that a small subnetwork of highly active and stable neurons supports group stability, and that this endows neuronal networks with the flexibility to continuously remodel without compromising stability and function.
authors.affiliation: Institute for Adaptive and Neural Computation, School of Informatics, The University of Edinburgh, Edinburgh EH8 9AB, United Kingdom.
authors.forename: Dagmara
authors.initials: D
authors.lastname: Panas
authors.affiliation: Istituto Italiano di Tecnologia, Department of Neuroscience and Brain Technologies, 16163 Genoa, Italy.
authors.forename: Hayder
authors.initials: H
authors.lastname: Amin
authors.affiliation: Istituto Italiano di Tecnologia, Department of Neuroscience and Brain Technologies, 16163 Genoa, Italy.
authors.forename: Alessandro
authors.initials: A
authors.lastname: Maccione
authors.affiliation: Institute for Adaptive and Neural Computation, School of Informatics, The University of Edinburgh, Edinburgh EH8 9AB, United Kingdom, National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, Karnataka 560065, India, and Manipal University, Manipal 576104, India.
authors.forename: Oliver
authors.initials: O
authors.lastname: Muthmann
authors.affiliation: Institute for Adaptive and Neural Computation, School of Informatics, The University of Edinburgh, Edinburgh EH8 9AB, United Kingdom.
authors.forename: Mark
authors.identifier: http://orcid.org/0000-0001-6525-6814
authors.initials: M
authors.lastname: van Rossum
authors.affiliation: Istituto Italiano di Tecnologia, Department of Neuroscience and Brain Technologies, 16163 Genoa, Italy.
authors.forename: Luca
authors.identifier: http://orcid.org/0000-0001-9521-2812
authors.initials: L
authors.lastname: Berdondini
authors.affiliation: Institute for Adaptive and Neural Computation, School of Informatics, The University of Edinburgh, Edinburgh EH8 9AB, United Kingdom, m.hennig@ed.ac.uk.
authors.forename: Matthias H
authors.identifier: http://orcid.org/0000-0001-7270-5817
authors.initials: MH
authors.lastname: Hennig
mesh_terms: D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D001921:Brain / Q000166:cytology; D002478:Cells, Cultured; D004558:Electric Stimulation; D004622:Embryo, Mammalian; D019277:Entropy; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D051381:Rats; D013569:Synapses / Q000502:physiology; D014793:Visual Cortex / Q000166:cytology
keywords: multielectrode array; network remodeling; neural culture; spike train analysis; statistical models