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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 single neural responses by spike counts and spike patterns.(A) Schematic illustration of experimental setup for selective mechanical stimulation of single whiskers and simultaneous VSD imaging or multi-electrode recordings in four barrel-related columns. (B) Illustration of the 8x16 channels probe showing shank and site spacing, position of the barrels C0 to D3, and the location of the cortical layers relative to the electrode sites. (C) Activity of an inhibitory neuron located at L4 of the barrel D1 in response to principal whisker (PW, upper part) and neighboring whisker (NW, lower part) deflections. Five illustrative trials are plotted for each condition. From the original raster plots (left side), spike counts in a 50 ms time window (middle) and spike pattern vectors of 5 ms bin size (right side) were computed to represent the activity in each single trial. (D) Discrimination capacity of the two selected response representations (spike counts and patterns). Left side, distribution of spike counts after PW vs. NW stimulation (200 trials each). Right side, distribution of spike patterns. Note that the overlap of the two distributions is lower for spike patterns than spike counts, thus accounting for higher values of mutual information (Im).
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pcbi.1004121.g001: Representation of single neural responses by spike counts and spike patterns.(A) Schematic illustration of experimental setup for selective mechanical stimulation of single whiskers and simultaneous VSD imaging or multi-electrode recordings in four barrel-related columns. (B) Illustration of the 8x16 channels probe showing shank and site spacing, position of the barrels C0 to D3, and the location of the cortical layers relative to the electrode sites. (C) Activity of an inhibitory neuron located at L4 of the barrel D1 in response to principal whisker (PW, upper part) and neighboring whisker (NW, lower part) deflections. Five illustrative trials are plotted for each condition. From the original raster plots (left side), spike counts in a 50 ms time window (middle) and spike pattern vectors of 5 ms bin size (right side) were computed to represent the activity in each single trial. (D) Discrimination capacity of the two selected response representations (spike counts and patterns). Left side, distribution of spike counts after PW vs. NW stimulation (200 trials each). Right side, distribution of spike patterns. Note that the overlap of the two distributions is lower for spike patterns than spike counts, thus accounting for higher values of mutual information (Im).

Mentions: Ensembles of well-isolated neurons were recorded with 16- or 128-channel electrode arrays in the barrel cortex of anesthetized adult Wistar rats in vivo. A systematic approach was used in order to allocate the isolated neurons to specific modules of the barrel cortex anatomy [12]. First, barrel-related columns were located by voltage sensitive dye (VSD) imaging upon single-whisker stimulation, which determined the insertion points of the electrode arrays. Local field potential (LFP) responses to stimulation of up to four neighboring single whiskers exhibited a barrel- and layer-specific activation pattern, thus allowing us to allocate the individual recording channels to their respective columns and layers (Fig 1A and 1B). Single neurons were further sorted using a ‘virtual tetrode’ approach, and assigned to the corresponding recording channel containing the maximum negative waveform amplitude (see Methods for further details). Note that no cross-contamination was present among neurons recorded within the same or closely neighboring electrode sites, thus discarding the possibility that the same neural event was assigned to different units (S1 Fig).


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 single neural responses by spike counts and spike patterns.(A) Schematic illustration of experimental setup for selective mechanical stimulation of single whiskers and simultaneous VSD imaging or multi-electrode recordings in four barrel-related columns. (B) Illustration of the 8x16 channels probe showing shank and site spacing, position of the barrels C0 to D3, and the location of the cortical layers relative to the electrode sites. (C) Activity of an inhibitory neuron located at L4 of the barrel D1 in response to principal whisker (PW, upper part) and neighboring whisker (NW, lower part) deflections. Five illustrative trials are plotted for each condition. From the original raster plots (left side), spike counts in a 50 ms time window (middle) and spike pattern vectors of 5 ms bin size (right side) were computed to represent the activity in each single trial. (D) Discrimination capacity of the two selected response representations (spike counts and patterns). Left side, distribution of spike counts after PW vs. NW stimulation (200 trials each). Right side, distribution of spike patterns. Note that the overlap of the two distributions is lower for spike patterns than spike counts, thus accounting for higher values of mutual information (Im).
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Related In: Results  -  Collection

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

pcbi.1004121.g001: Representation of single neural responses by spike counts and spike patterns.(A) Schematic illustration of experimental setup for selective mechanical stimulation of single whiskers and simultaneous VSD imaging or multi-electrode recordings in four barrel-related columns. (B) Illustration of the 8x16 channels probe showing shank and site spacing, position of the barrels C0 to D3, and the location of the cortical layers relative to the electrode sites. (C) Activity of an inhibitory neuron located at L4 of the barrel D1 in response to principal whisker (PW, upper part) and neighboring whisker (NW, lower part) deflections. Five illustrative trials are plotted for each condition. From the original raster plots (left side), spike counts in a 50 ms time window (middle) and spike pattern vectors of 5 ms bin size (right side) were computed to represent the activity in each single trial. (D) Discrimination capacity of the two selected response representations (spike counts and patterns). Left side, distribution of spike counts after PW vs. NW stimulation (200 trials each). Right side, distribution of spike patterns. Note that the overlap of the two distributions is lower for spike patterns than spike counts, thus accounting for higher values of mutual information (Im).
Mentions: Ensembles of well-isolated neurons were recorded with 16- or 128-channel electrode arrays in the barrel cortex of anesthetized adult Wistar rats in vivo. A systematic approach was used in order to allocate the isolated neurons to specific modules of the barrel cortex anatomy [12]. First, barrel-related columns were located by voltage sensitive dye (VSD) imaging upon single-whisker stimulation, which determined the insertion points of the electrode arrays. Local field potential (LFP) responses to stimulation of up to four neighboring single whiskers exhibited a barrel- and layer-specific activation pattern, thus allowing us to allocate the individual recording channels to their respective columns and layers (Fig 1A and 1B). Single neurons were further sorted using a ‘virtual tetrode’ approach, and assigned to the corresponding recording channel containing the maximum negative waveform amplitude (see Methods for further details). Note that no cross-contamination was present among neurons recorded within the same or closely neighboring electrode sites, thus discarding the possibility that the same neural event was assigned to different units (S1 Fig).

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.