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High Stimulus-Related Information in Barrel Cortex Inhibitory Interneurons.

Reyes-Puerta V, Kim S, Sun JJ, Imbrosci B, Kilb W, Luhmann HJ - PLoS Comput. Biol. (2015)

Bottom Line: We also demonstrate that ensembles of INH cells jointly provide as much information about such stimuli as comparable ensembles containing the ~20% most informative EXC neurons, however presenting less information redundancy - a result which was consistent when applying both theoretical information measurements and linear discriminant analysis classifiers.These results suggest that a consortium of INH neurons dominates the information conveyed to the neocortical network, thereby efficiently processing incoming sensory activity.This conclusion extends our view on the role of the inhibitory system to orchestrate cortical activity.

View Article: PubMed Central - PubMed

Affiliation: Institute of Physiology, University Medical Center of the Johannes Gutenberg University, Mainz, Germany.

ABSTRACT
The manner in which populations of inhibitory (INH) and excitatory (EXC) neocortical neurons collectively encode stimulus-related information is a fundamental, yet still unresolved question. Here we address this question by simultaneously recording with large-scale multi-electrode arrays (of up to 128 channels) the activity of cell ensembles (of up to 74 neurons) distributed along all layers of 3-4 neighboring cortical columns in the anesthetized adult rat somatosensory barrel cortex in vivo. Using two different whisker stimulus modalities (location and frequency) we show that individual INH neurons--classified as such according to their distinct extracellular spike waveforms--discriminate better between restricted sets of stimuli (≤6 stimulus classes) than EXC neurons in granular and infra-granular layers. We also demonstrate that ensembles of INH cells jointly provide as much information about such stimuli as comparable ensembles containing the ~20% most informative EXC neurons, however presenting less information redundancy - a result which was consistent when applying both theoretical information measurements and linear discriminant analysis classifiers. These results suggest that a consortium of INH neurons dominates the information conveyed to the neocortical network, thereby efficiently processing incoming sensory activity. This conclusion extends our view on the role of the inhibitory system to orchestrate cortical activity.

No MeSH data available.


More efficient encoding of stimulus frequency by INH neuronal ensembles.(A1) Comparison of information redundancy present in groups of INH neurons to that in equally informative groups of best EXC neurons. Each line represents the corresponding values of an individual dataset, including the stimulation blocks at all tested frequencies for a specific whisker and animal (n = 16 datasets from 8 animals). Circles and error bars denote mean±SD. *P<0.05. (A2) Number of neurons constituting the groups of INH and best EXC cells. Bars and error bars denote mean±SEM. (A3) Level of stimulus-independent noise correlations averaged across datasets. (B) Impact of trial-shuffling on decoding performance of the liner discriminant analysis decoders (same as in Fig 7A). ***P<0.001. (C) For each neuronal group, comparison of the relative increase obtained in decoding performance after trial-shuffling to the decrease in the variability of the ensemble activity level averaged across trials. Crosses represent mean±SD of the computed values for each neuronal group.
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pcbi.1004121.g008: More efficient encoding of stimulus frequency by INH neuronal ensembles.(A1) Comparison of information redundancy present in groups of INH neurons to that in equally informative groups of best EXC neurons. Each line represents the corresponding values of an individual dataset, including the stimulation blocks at all tested frequencies for a specific whisker and animal (n = 16 datasets from 8 animals). Circles and error bars denote mean±SD. *P<0.05. (A2) Number of neurons constituting the groups of INH and best EXC cells. Bars and error bars denote mean±SEM. (A3) Level of stimulus-independent noise correlations averaged across datasets. (B) Impact of trial-shuffling on decoding performance of the liner discriminant analysis decoders (same as in Fig 7A). ***P<0.001. (C) For each neuronal group, comparison of the relative increase obtained in decoding performance after trial-shuffling to the decrease in the variability of the ensemble activity level averaged across trials. Crosses represent mean±SD of the computed values for each neuronal group.

Mentions: We further computed the amount of redundancy related to stimulus frequency information. As previously, we compared groups of INH (n = 5.6±0.56) and EXC (n = 6.8±1.3) neurons selected in descending order and conveying an equal amount of ensemble information (1.69±0.18 bits). Groups of INH neurons contained significantly less information redundancy (-0.51±0.2 bits) than comparable groups of best EXC neurons (-0.79±0.27 bits) (n = 16 datasets from 8 animals, paired signed-rank test, p<0.05) (Fig 8A1). Since best EXC neurons carried stimulus frequency information more redundantly, a slightly higher number of neurons were needed in the best EXC groups (6.8±1.3) to reach similar levels of ensemble-based information than in the INH groups (5.6±0.56) (n = 16 datasets, paired signed-rank test, p = 0.27) (Fig 8A2). This result suggests that the property of INH neurons encoding stimuli more efficiently than EXC neurons is not specific to one stimulus modality (location), but rather a general phenomenon.


High Stimulus-Related Information in Barrel Cortex Inhibitory Interneurons.

Reyes-Puerta V, Kim S, Sun JJ, Imbrosci B, Kilb W, Luhmann HJ - PLoS Comput. Biol. (2015)

More efficient encoding of stimulus frequency by INH neuronal ensembles.(A1) Comparison of information redundancy present in groups of INH neurons to that in equally informative groups of best EXC neurons. Each line represents the corresponding values of an individual dataset, including the stimulation blocks at all tested frequencies for a specific whisker and animal (n = 16 datasets from 8 animals). Circles and error bars denote mean±SD. *P<0.05. (A2) Number of neurons constituting the groups of INH and best EXC cells. Bars and error bars denote mean±SEM. (A3) Level of stimulus-independent noise correlations averaged across datasets. (B) Impact of trial-shuffling on decoding performance of the liner discriminant analysis decoders (same as in Fig 7A). ***P<0.001. (C) For each neuronal group, comparison of the relative increase obtained in decoding performance after trial-shuffling to the decrease in the variability of the ensemble activity level averaged across trials. Crosses represent mean±SD of the computed values for each neuronal group.
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getmorefigures.php?uid=PMC4476555&req=5

pcbi.1004121.g008: More efficient encoding of stimulus frequency by INH neuronal ensembles.(A1) Comparison of information redundancy present in groups of INH neurons to that in equally informative groups of best EXC neurons. Each line represents the corresponding values of an individual dataset, including the stimulation blocks at all tested frequencies for a specific whisker and animal (n = 16 datasets from 8 animals). Circles and error bars denote mean±SD. *P<0.05. (A2) Number of neurons constituting the groups of INH and best EXC cells. Bars and error bars denote mean±SEM. (A3) Level of stimulus-independent noise correlations averaged across datasets. (B) Impact of trial-shuffling on decoding performance of the liner discriminant analysis decoders (same as in Fig 7A). ***P<0.001. (C) For each neuronal group, comparison of the relative increase obtained in decoding performance after trial-shuffling to the decrease in the variability of the ensemble activity level averaged across trials. Crosses represent mean±SD of the computed values for each neuronal group.
Mentions: We further computed the amount of redundancy related to stimulus frequency information. As previously, we compared groups of INH (n = 5.6±0.56) and EXC (n = 6.8±1.3) neurons selected in descending order and conveying an equal amount of ensemble information (1.69±0.18 bits). Groups of INH neurons contained significantly less information redundancy (-0.51±0.2 bits) than comparable groups of best EXC neurons (-0.79±0.27 bits) (n = 16 datasets from 8 animals, paired signed-rank test, p<0.05) (Fig 8A1). Since best EXC neurons carried stimulus frequency information more redundantly, a slightly higher number of neurons were needed in the best EXC groups (6.8±1.3) to reach similar levels of ensemble-based information than in the INH groups (5.6±0.56) (n = 16 datasets, paired signed-rank test, p = 0.27) (Fig 8A2). This result suggests that the property of INH neurons encoding stimuli more efficiently than EXC neurons is not specific to one stimulus modality (location), but rather a general phenomenon.

Bottom Line: We also demonstrate that ensembles of INH cells jointly provide as much information about such stimuli as comparable ensembles containing the ~20% most informative EXC neurons, however presenting less information redundancy - a result which was consistent when applying both theoretical information measurements and linear discriminant analysis classifiers.These results suggest that a consortium of INH neurons dominates the information conveyed to the neocortical network, thereby efficiently processing incoming sensory activity.This conclusion extends our view on the role of the inhibitory system to orchestrate cortical activity.

View Article: PubMed Central - PubMed

Affiliation: Institute of Physiology, University Medical Center of the Johannes Gutenberg University, Mainz, Germany.

ABSTRACT
The manner in which populations of inhibitory (INH) and excitatory (EXC) neocortical neurons collectively encode stimulus-related information is a fundamental, yet still unresolved question. Here we address this question by simultaneously recording with large-scale multi-electrode arrays (of up to 128 channels) the activity of cell ensembles (of up to 74 neurons) distributed along all layers of 3-4 neighboring cortical columns in the anesthetized adult rat somatosensory barrel cortex in vivo. Using two different whisker stimulus modalities (location and frequency) we show that individual INH neurons--classified as such according to their distinct extracellular spike waveforms--discriminate better between restricted sets of stimuli (≤6 stimulus classes) than EXC neurons in granular and infra-granular layers. We also demonstrate that ensembles of INH cells jointly provide as much information about such stimuli as comparable ensembles containing the ~20% most informative EXC neurons, however presenting less information redundancy - a result which was consistent when applying both theoretical information measurements and linear discriminant analysis classifiers. These results suggest that a consortium of INH neurons dominates the information conveyed to the neocortical network, thereby efficiently processing incoming sensory activity. This conclusion extends our view on the role of the inhibitory system to orchestrate cortical activity.

No MeSH data available.