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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.


Distribution of stimulus information in single neurons.(A) Time course of stimulus location information carried by the spikes counted in increasingly longer time windows for low frequency stimulation (<1 Hz). Data represent the mean values averaged across the specific neuronal subsets (symbols depicted at the legend, subset sizes displayed in panel B). (B) Stimulus location information using spike pattern parameters for optimal stimulus discrimination (see S2 and S5 Figs). Each bar represents mean±SEM values. Numbers inside bars represent amount of neurons in each subset. Otherwise same as in A. *P<0.05, **P<0.01. (C) Distribution of information at higher stimulation frequencies in different excitatory (EXC) cell groups (symbols represent layers as in A). Data represent the mean values of stimulus location information averaged across the tested stimulation frequencies. (D) Distribution of information in inhibitory (INH) cells (same as in C). (E) Time course of stimulus frequency information in INH and EXC cells (same as in A). (F) Stimulus frequency information using parameters for optimal discrimination (same as in B).
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pcbi.1004121.g003: Distribution of stimulus information in single neurons.(A) Time course of stimulus location information carried by the spikes counted in increasingly longer time windows for low frequency stimulation (<1 Hz). Data represent the mean values averaged across the specific neuronal subsets (symbols depicted at the legend, subset sizes displayed in panel B). (B) Stimulus location information using spike pattern parameters for optimal stimulus discrimination (see S2 and S5 Figs). Each bar represents mean±SEM values. Numbers inside bars represent amount of neurons in each subset. Otherwise same as in A. *P<0.05, **P<0.01. (C) Distribution of information at higher stimulation frequencies in different excitatory (EXC) cell groups (symbols represent layers as in A). Data represent the mean values of stimulus location information averaged across the tested stimulation frequencies. (D) Distribution of information in inhibitory (INH) cells (same as in C). (E) Time course of stimulus frequency information in INH and EXC cells (same as in A). (F) Stimulus frequency information using parameters for optimal discrimination (same as in B).

Mentions: At low stimulation frequencies (≤1 Hz), L4 EXC neurons also revealed a higher level of activity and shorter first-spike latencies in response to PW than to NW stimulation, but their evoked spike responses were less temporally precise than in L4 INH cells (Fig 2B1 & 2B2). Already at frequencies ≥2 Hz the number of evoked spikes for both PW and NW was close to background activity, which resulted in low values for stimulus location information (Fig 2B3). This property together with their lower spike timing precision made EXC neurons less suitable than INH ones for encoding stimulus frequency information (see values of representative neurons in Fig 2 caption, and for extended analyses Fig 3F). These results suggest that L4 INH neurons convey more information about the different stimulus modalities (location and frequency) than L4 EXC neurons, due to (1) their higher number of spikes per stimulus, (2) their higher precision, and (3) their lower adaptation at higher frequency stimulation [24].


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)

Distribution of stimulus information in single neurons.(A) Time course of stimulus location information carried by the spikes counted in increasingly longer time windows for low frequency stimulation (<1 Hz). Data represent the mean values averaged across the specific neuronal subsets (symbols depicted at the legend, subset sizes displayed in panel B). (B) Stimulus location information using spike pattern parameters for optimal stimulus discrimination (see S2 and S5 Figs). Each bar represents mean±SEM values. Numbers inside bars represent amount of neurons in each subset. Otherwise same as in A. *P<0.05, **P<0.01. (C) Distribution of information at higher stimulation frequencies in different excitatory (EXC) cell groups (symbols represent layers as in A). Data represent the mean values of stimulus location information averaged across the tested stimulation frequencies. (D) Distribution of information in inhibitory (INH) cells (same as in C). (E) Time course of stimulus frequency information in INH and EXC cells (same as in A). (F) Stimulus frequency information using parameters for optimal discrimination (same as in B).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4476555&req=5

pcbi.1004121.g003: Distribution of stimulus information in single neurons.(A) Time course of stimulus location information carried by the spikes counted in increasingly longer time windows for low frequency stimulation (<1 Hz). Data represent the mean values averaged across the specific neuronal subsets (symbols depicted at the legend, subset sizes displayed in panel B). (B) Stimulus location information using spike pattern parameters for optimal stimulus discrimination (see S2 and S5 Figs). Each bar represents mean±SEM values. Numbers inside bars represent amount of neurons in each subset. Otherwise same as in A. *P<0.05, **P<0.01. (C) Distribution of information at higher stimulation frequencies in different excitatory (EXC) cell groups (symbols represent layers as in A). Data represent the mean values of stimulus location information averaged across the tested stimulation frequencies. (D) Distribution of information in inhibitory (INH) cells (same as in C). (E) Time course of stimulus frequency information in INH and EXC cells (same as in A). (F) Stimulus frequency information using parameters for optimal discrimination (same as in B).
Mentions: At low stimulation frequencies (≤1 Hz), L4 EXC neurons also revealed a higher level of activity and shorter first-spike latencies in response to PW than to NW stimulation, but their evoked spike responses were less temporally precise than in L4 INH cells (Fig 2B1 & 2B2). Already at frequencies ≥2 Hz the number of evoked spikes for both PW and NW was close to background activity, which resulted in low values for stimulus location information (Fig 2B3). This property together with their lower spike timing precision made EXC neurons less suitable than INH ones for encoding stimulus frequency information (see values of representative neurons in Fig 2 caption, and for extended analyses Fig 3F). These results suggest that L4 INH neurons convey more information about the different stimulus modalities (location and frequency) than L4 EXC neurons, due to (1) their higher number of spikes per stimulus, (2) their higher precision, and (3) their lower adaptation at higher frequency stimulation [24].

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.