Literature DB >> 21436050

Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition.

Sonya Giridhar1, Brent Doiron, Nathaniel N Urban.   

Abstract

Neurons respond to sensory stimuli by altering the rate and temporal pattern of action potentials. These spike trains both encode and propagate information that guides behavior. Local inhibitory networks can affect the information encoded and propagated by neurons by altering correlations between different spike trains. Correlations introduce redundancy that can reduce encoding but also facilitate propagation of activity to downstream targets. Given this trade-off, how can networks maximize both encoding and propagation efficacy? Here, we examine this problem by measuring the effects of olfactory bulb inhibition on the pairwise statistics of mitral cell spiking. We evoked spiking activity in the olfactory bulb in vitro and measured how lateral inhibition shapes correlations across timescales. We show that inhibitory circuits simultaneously increase fast correlation (i.e., synchrony increases) and decrease slow correlation (i.e., firing rates become less similar). Further, we use computational models to show the benefits of fast correlation/slow decorrelation in the context of odor coding. Olfactory bulb inhibition enhances population-level discrimination of similar inputs, while improving propagation of mitral cell activity to cortex. Our findings represent a targeted strategy by which a network can optimize the correlation structure of its output in a dynamic, activity-dependent manner. This trade-off is not specific to the olfactory system, but rather our work highlights mechanisms by which neurons can simultaneously accomplish multiple, and sometimes competing, aspects of sensory processing.

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Year:  2011        PMID: 21436050      PMCID: PMC3078353          DOI: 10.1073/pnas.1015165108

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  63 in total

Review 1.  Neural mechanisms of orientation selectivity in the visual cortex.

Authors:  D Ferster; K D Miller
Journal:  Annu Rev Neurosci       Date:  2000       Impact factor: 12.449

2.  Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns.

Authors:  Christoph Kayser; Marcelo A Montemurro; Nikos K Logothetis; Stefano Panzeri
Journal:  Neuron       Date:  2009-02-26       Impact factor: 17.173

Review 3.  Sensory neural codes using multiplexed temporal scales.

Authors:  Stefano Panzeri; Nicolas Brunel; Nikos K Logothetis; Christoph Kayser
Journal:  Trends Neurosci       Date:  2010-01-04       Impact factor: 13.837

4.  Rat olfactory bulb mitral cells receive sparse glomerular inputs.

Authors:  Antoniu L Fantana; Edward R Soucy; Markus Meister
Journal:  Neuron       Date:  2008-09-11       Impact factor: 17.173

5.  Spatial and temporal scales of neuronal correlation in primary visual cortex.

Authors:  Matthew A Smith; Adam Kohn
Journal:  J Neurosci       Date:  2008-11-26       Impact factor: 6.167

6.  Disruption of GABAA in the insect antennal lobe generally increases odor detection and discrimination thresholds.

Authors:  Esther K Mwilaria; Chitrita Ghatak; Kevin C Daly
Journal:  Chem Senses       Date:  2008-01-16       Impact factor: 3.160

7.  Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice.

Authors:  Nixon M Abraham; Veronica Egger; Derya R Shimshek; Robert Renden; Izumi Fukunaga; Rolf Sprengel; Peter H Seeburg; Matthias Klugmann; Troy W Margrie; Andreas T Schaefer; Thomas Kuner
Journal:  Neuron       Date:  2010-02-11       Impact factor: 17.173

Review 8.  Regulation of spike timing in visual cortical circuits.

Authors:  Paul Tiesinga; Jean-Marc Fellous; Terrence J Sejnowski
Journal:  Nat Rev Neurosci       Date:  2008-02       Impact factor: 34.870

9.  Properties of piriform cortex pyramidal cell dendrites: implications for olfactory circuit design.

Authors:  Brice Bathellier; Troy W Margrie; Matthew E Larkum
Journal:  J Neurosci       Date:  2009-10-07       Impact factor: 6.167

10.  Synchrony of thalamocortical inputs maximizes cortical reliability.

Authors:  Hsi-Ping Wang; Donald Spencer; Jean-Marc Fellous; Terrence J Sejnowski
Journal:  Science       Date:  2010-04-02       Impact factor: 47.728

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  41 in total

1.  Intraglomerular inhibition shapes the strength and temporal structure of glomerular output.

Authors:  Zuoyi Shao; Adam C Puche; Shaolin Liu; Michael T Shipley
Journal:  J Neurophysiol       Date:  2012-05-16       Impact factor: 2.714

2.  Origins of correlated spiking in the mammalian olfactory bulb.

Authors:  Richard C Gerkin; Shreejoy J Tripathy; Nathaniel N Urban
Journal:  Proc Natl Acad Sci U S A       Date:  2013-09-30       Impact factor: 11.205

3.  Distinct lateral inhibitory circuits drive parallel processing of sensory information in the mammalian olfactory bulb.

Authors:  Matthew A Geramita; Shawn D Burton; Nathan N Urban
Journal:  Elife       Date:  2016-06-28       Impact factor: 8.140

4.  Short-term synaptic depression and stochastic vesicle dynamics reduce and shape neuronal correlations.

Authors:  Robert Rosenbaum; Jonathan E Rubin; Brent Doiron
Journal:  J Neurophysiol       Date:  2012-10-31       Impact factor: 2.714

5.  Intrinsic heterogeneity in oscillatory dynamics limits correlation-induced neural synchronization.

Authors:  Shawn D Burton; G Bard Ermentrout; Nathaniel N Urban
Journal:  J Neurophysiol       Date:  2012-07-18       Impact factor: 2.714

6.  Intermediate intrinsic diversity enhances neural population coding.

Authors:  Shreejoy J Tripathy; Krishnan Padmanabhan; Richard C Gerkin; Nathaniel N Urban
Journal:  Proc Natl Acad Sci U S A       Date:  2013-04-29       Impact factor: 11.205

7.  Postnatal Odor Exposure Increases the Strength of Interglomerular Lateral Inhibition onto Olfactory Bulb Tufted Cells.

Authors:  Matthew Geramita; Nathan N Urban
Journal:  J Neurosci       Date:  2016-12-07       Impact factor: 6.167

8.  Sparse coding and lateral inhibition arising from balanced and unbalanced dendrodendritic excitation and inhibition.

Authors:  Yuguo Yu; Michele Migliore; Michael L Hines; Gordon M Shepherd
Journal:  J Neurosci       Date:  2014-10-08       Impact factor: 6.167

9.  Adenosine A1 receptor activates background potassium channels and modulates information processing in olfactory bulb mitral cells.

Authors:  Natalie Rotermund; Svenja Winandy; Timo Fischer; Kristina Schulz; Torsten Fregin; Nadine Alstedt; Melanie Buchta; Janick Bartels; Mattias Carlström; Christian Lohr; Daniela Hirnet
Journal:  J Physiol       Date:  2018-01-24       Impact factor: 5.182

Review 10.  Inhibitory Interneurons Regulate Temporal Precision and Correlations in Cortical Circuits.

Authors:  Jessica A Cardin
Journal:  Trends Neurosci       Date:  2018-09-25       Impact factor: 13.837

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