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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.


Representation of neural ensemble responses by spike count vectors and spike pattern arrays.(A1) Neuronal ensemble activity in response to three trials of whisker D1 stimulation at low frequency. Blue and red dots mark the spike times of INH and EXC neurons, respectively. Cells were ordered along the y-axis according to their position on the shanks, i.e. belonging to the barrel-related columns C0 to D3 (see right side). The numbers at the left side (1 to 44) represent the ordering of the recorded neurons according to their horizontal location. Blue horizontal arrow (together with the black circle around its spike times) marks the INH neuron already presented in Figs 1 and 2A. (A2) Neuronal ensemble activity in response to three trials of whisker D2 stimulation (same as in A1). (B) Illustration of the method to quantify neural ensemble activity by spike count vectors and spike pattern arrays. Illustrative data are from trial #3 presented in panel A. In general, each trial is represented by a Nneurons spike count vector, or a Nneurons ⋅ Nbins spike pattern array. Afterwards the spike count vectors and spike pattern arrays are used to compute (1) the ensemble-based mutual information, and (2) the decoding performance obtained using linear discriminant analysis classifiers (see text).
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pcbi.1004121.g004: Representation of neural ensemble responses by spike count vectors and spike pattern arrays.(A1) Neuronal ensemble activity in response to three trials of whisker D1 stimulation at low frequency. Blue and red dots mark the spike times of INH and EXC neurons, respectively. Cells were ordered along the y-axis according to their position on the shanks, i.e. belonging to the barrel-related columns C0 to D3 (see right side). The numbers at the left side (1 to 44) represent the ordering of the recorded neurons according to their horizontal location. Blue horizontal arrow (together with the black circle around its spike times) marks the INH neuron already presented in Figs 1 and 2A. (A2) Neuronal ensemble activity in response to three trials of whisker D2 stimulation (same as in A1). (B) Illustration of the method to quantify neural ensemble activity by spike count vectors and spike pattern arrays. Illustrative data are from trial #3 presented in panel A. In general, each trial is represented by a Nneurons spike count vector, or a Nneurons ⋅ Nbins spike pattern array. Afterwards the spike count vectors and spike pattern arrays are used to compute (1) the ensemble-based mutual information, and (2) the decoding performance obtained using linear discriminant analysis classifiers (see text).

Mentions: Next we expanded our analyses to the neural ensemble level, thereby investigating how populations of neurons jointly represent the studied stimulus modalities, and whether different subgroups of neurons encoded the stimuli synergistically or redundantly. Despite the intrinsic trial-to-trial variability in the evoked population responses, a general propagation pattern could be observed across barrel-related columns (Fig 4A). At low frequency stimulation, neuronal activity started at the principal column ~7 to 10 ms after whisker stimulus, extending toward the first-order neighboring column ~5 ms afterwards [12].


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)

Representation of neural ensemble responses by spike count vectors and spike pattern arrays.(A1) Neuronal ensemble activity in response to three trials of whisker D1 stimulation at low frequency. Blue and red dots mark the spike times of INH and EXC neurons, respectively. Cells were ordered along the y-axis according to their position on the shanks, i.e. belonging to the barrel-related columns C0 to D3 (see right side). The numbers at the left side (1 to 44) represent the ordering of the recorded neurons according to their horizontal location. Blue horizontal arrow (together with the black circle around its spike times) marks the INH neuron already presented in Figs 1 and 2A. (A2) Neuronal ensemble activity in response to three trials of whisker D2 stimulation (same as in A1). (B) Illustration of the method to quantify neural ensemble activity by spike count vectors and spike pattern arrays. Illustrative data are from trial #3 presented in panel A. In general, each trial is represented by a Nneurons spike count vector, or a Nneurons ⋅ Nbins spike pattern array. Afterwards the spike count vectors and spike pattern arrays are used to compute (1) the ensemble-based mutual information, and (2) the decoding performance obtained using linear discriminant analysis classifiers (see text).
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4476555&req=5

pcbi.1004121.g004: Representation of neural ensemble responses by spike count vectors and spike pattern arrays.(A1) Neuronal ensemble activity in response to three trials of whisker D1 stimulation at low frequency. Blue and red dots mark the spike times of INH and EXC neurons, respectively. Cells were ordered along the y-axis according to their position on the shanks, i.e. belonging to the barrel-related columns C0 to D3 (see right side). The numbers at the left side (1 to 44) represent the ordering of the recorded neurons according to their horizontal location. Blue horizontal arrow (together with the black circle around its spike times) marks the INH neuron already presented in Figs 1 and 2A. (A2) Neuronal ensemble activity in response to three trials of whisker D2 stimulation (same as in A1). (B) Illustration of the method to quantify neural ensemble activity by spike count vectors and spike pattern arrays. Illustrative data are from trial #3 presented in panel A. In general, each trial is represented by a Nneurons spike count vector, or a Nneurons ⋅ Nbins spike pattern array. Afterwards the spike count vectors and spike pattern arrays are used to compute (1) the ensemble-based mutual information, and (2) the decoding performance obtained using linear discriminant analysis classifiers (see text).
Mentions: Next we expanded our analyses to the neural ensemble level, thereby investigating how populations of neurons jointly represent the studied stimulus modalities, and whether different subgroups of neurons encoded the stimuli synergistically or redundantly. Despite the intrinsic trial-to-trial variability in the evoked population responses, a general propagation pattern could be observed across barrel-related columns (Fig 4A). At low frequency stimulation, neuronal activity started at the principal column ~7 to 10 ms after whisker stimulus, extending toward the first-order neighboring column ~5 ms afterwards [12].

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.