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      Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content

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      1 , 2 , 1 , 2 , 3
      Nature neuroscience

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          Abstract

          While examples of variation and diversity exist throughout the nervous system, their importance remains a source of debate. Even neurons of the same molecular type show notable intrinsic differences. Largely unknown however is the degree to which these differences impair or assist neural coding. When outputs from a single type of neuron were examined - the mitral cells of the mouse olfactory bulb - to identical stimuli, we found that each cell's spiking response was dictated by its unique biophysical fingerprint. By exploiting this intrinsic heterogeneity, diverse populations coded for 2-fold more information than their homogeneous counterparts. Additionally, biophysical variability alone reduced pairwise output spike correlations to low levels. Our results demonstrate that intrinsic neuronal diversity serves an important role in neural coding and is not simply the result of biological imprecision.

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          Most cited references40

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          Variability, compensation and homeostasis in neuron and network function.

          Neurons in most animals live a very long time relative to the half-lives of all of the proteins that govern excitability and synaptic transmission. Consequently, homeostatic mechanisms are necessary to ensure stable neuronal and network function over an animal's lifetime. To understand how these homeostatic mechanisms might function, it is crucial to understand how tightly regulated synaptic and intrinsic properties must be for adequate network performance, and the extent to which compensatory mechanisms allow for multiple solutions to the production of similar behaviour. Here, we use examples from theoretical and experimental studies of invertebrates and vertebrates to explore several issues relevant to understanding the precision of tuning of synaptic and intrinsic currents for the operation of functional neuronal circuits.
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            Influence of dendritic structure on firing pattern in model neocortical neurons.

            Neocortical neurons display a wide range of dendritic morphologies, ranging from compact arborizations to highly elaborate branching patterns. In vitro electrical recordings from these neurons have revealed a correspondingly diverse range of intrinsic firing patterns, including non-adapting, adapting and bursting types. This heterogeneity of electrical responsivity has generally been attributed to variability in the types and densities of ionic channels. We show here, using compartmental models of reconstructed cortical neurons, that an entire spectrum of firing patterns can be reproduced in a set of neurons that share a common distribution of ion channels and differ only in their dendritic geometry. The essential behaviour of the model depends on partial electrical coupling of fast active conductances localized to the soma and axon and slow active currents located throughout the dendrites, and can be reproduced in a two-compartment model. The results suggest a causal relationship for the observed correlations between dendritic structure and firing properties and emphasize the importance of active dendritic conductances in neuronal function.
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              Decorrelated neuronal firing in cortical microcircuits.

              Correlated trial-to-trial variability in the activity of cortical neurons is thought to reflect the functional connectivity of the circuit. Many cortical areas are organized into functional columns, in which neurons are believed to be densely connected and to share common input. Numerous studies report a high degree of correlated variability between nearby cells. We developed chronically implanted multitetrode arrays offering unprecedented recording quality to reexamine this question in the primary visual cortex of awake macaques. We found that even nearby neurons with similar orientation tuning show virtually no correlated variability. Our findings suggest a refinement of current models of cortical microcircuit architecture and function: Either adjacent neurons share only a few percent of their inputs or, alternatively, their activity is actively decorrelated.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nature neuroscience
                1097-6256
                1546-1726
                20 September 2010
                29 August 2010
                October 2010
                1 April 2011
                : 13
                : 10
                : 1276-1282
                Affiliations
                [1 ] Dept of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA
                [2 ] Center for the Neural Basis of Cognition, Pittsburgh, PA
                [3 ] Department of Neuroscience, University of Pittsburgh, Pittsburgh PA
                Author notes
                Correspondence should be addressed to Dr. Nathan Urban, Department of Biological Sciences and Center for the Neural Basis of Cognition, 4400 Fifth Avenue, Mellon Institute, Room 173, Carnegie Mellon University, Pittsburgh, PA 15213. nurban@ 123456cmu.edu
                Article
                nihpa226409
                10.1038/nn.2630
                2975253
                20802489
                c1c8c727-a6ce-40d2-a5ee-56f893d06c90

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

                History
                Funding
                Funded by: National Institute on Deafness and Other Communication Disorders : NIDCD
                Award ID: R01 DC011184-05 ||DC
                Funded by: National Institute on Deafness and Other Communication Disorders : NIDCD
                Award ID: R01 DC005798-09 ||DC
                Funded by: National Institute on Deafness and Other Communication Disorders : NIDCD
                Award ID: R01 DC005798-08 ||DC
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                Neurosciences
                Neurosciences

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