Neocortical inhibitory interneuron subtypes display distinct responses to synchrony and rate of inputs

AbstractPopulations of neurons in the neocortex can carry information with both the synchrony and the rate of their spikes. However, it is unknown whether distinct subtypes of neurons in the cortical microcircuit are more sensitive to information carried by synchrony versus rate. Here, we address this question using patterned optical stimulation in slices of barrel cortex from transgenic mouse lines labelling distinct interneuron populations: fast-spiking parvalbumin-positive (PV+) and somatostatin-positive (SST+) interneurons. We use optical stimulation of channelrhodopsin-2 (ChR2) expressing excitatory neurons in layer 2/3 in order to encode a random 1-bit signal in either the synchrony or rate of activity in presynaptic cells. We then examine the mutual information between this 1-bit signal and the voltage and spiking responses in PV+ and SST+ interneurons. Generally, we find that both interneuron types carry more information than GFP negative (GFP-) control cells. More specifically, we find that for a synchrony encoding, PV+ interneurons carry more information in the first 5 milliseconds, while both interneuron subtypes carry more information than negative controls in their later response. We also find that for a rate encoding, SST+ interneurons carry more information than either PV+ or negative controls after several milliseconds. These data demonstrate that inhibitory interneuron subtypes in the neocortex have distinct responses to information carried by synchrony versus rates of spiking.

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Neocortical inhibitory interneuron subtypes are differentially attuned to synchrony- and rate-coded information

Communications Biology ◽

10.1038/s42003-021-02437-y ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Luke Y. Prince ◽

Matthew M. Tran ◽

Dorian Grey ◽

Lydia Saad ◽

Helen Chasiotis ◽

...

Keyword(s):

Mutual Information ◽

Somatosensory Cortex ◽

Inhibitory Interneuron ◽

Optical Stimulation ◽

Layer 2 ◽

Excitatory Neurons ◽

Fast Spiking ◽

Mouse Lines

AbstractNeurons can carry information with both the synchrony and rate of their spikes. However, it is unknown whether distinct subtypes of neurons are more sensitive to information carried by synchrony versus rate, or vice versa. Here, we address this question using patterned optical stimulation in slices of somatosensory cortex from mouse lines labelling fast-spiking (FS) and regular-spiking (RS) interneurons. We used optical stimulation in layer 2/3 to encode a 1-bit signal using either the synchrony or rate of activity. We then examined the mutual information between this signal and the interneuron responses. We found that for a synchrony encoding, FS interneurons carried more information in the first five milliseconds, while both interneuron subtypes carried more information than excitatory neurons in later responses. For a rate encoding, we found that RS interneurons carried more information after several milliseconds. These data demonstrate that distinct interneuron subtypes in the neocortex have distinct sensitivities to synchrony versus rate codes.

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Microcircuits of excitatory and inhibitory neurons in layer 2/3 of mouse barrel cortex

Journal of Neurophysiology ◽

10.1152/jn.00917.2011 ◽

2012 ◽

Vol 107 (11) ◽

pp. 3116-3134 ◽

Cited By ~ 112

Author(s):

Michael Avermann ◽

Christian Tomm ◽

Celine Mateo ◽

Wulfram Gerstner ◽

Carl C. H. Petersen

Keyword(s):

Barrel Cortex ◽

Gabaergic Neurons ◽

Network Activity ◽

Inhibitory Neurons ◽

Synaptic Connectivity ◽

Postsynaptic Potentials ◽

Optogenetic Stimulation ◽

Layer 2 ◽

Fast Spiking ◽

Whole Cell Recordings

Synaptic interactions between nearby excitatory and inhibitory neurons in the neocortex are thought to play fundamental roles in sensory processing. Here, we have combined optogenetic stimulation, whole cell recordings, and computational modeling to define key functional microcircuits within layer 2/3 of mouse primary somatosensory barrel cortex. In vitro optogenetic stimulation of excitatory layer 2/3 neurons expressing channelrhodopsin-2 evoked a rapid sequence of excitation followed by inhibition. Fast-spiking (FS) GABAergic neurons received large-amplitude, fast-rising depolarizing postsynaptic potentials, often driving action potentials. In contrast, the same optogenetic stimulus evoked small-amplitude, subthreshold postsynaptic potentials in excitatory and non-fast-spiking (NFS) GABAergic neurons. To understand the synaptic mechanisms underlying this network activity, we investigated unitary synaptic connectivity through multiple simultaneous whole cell recordings. FS GABAergic neurons received unitary excitatory postsynaptic potentials with higher probability, larger amplitudes, and faster kinetics compared with NFS GABAergic neurons and other excitatory neurons. Both FS and NFS GABAergic neurons evoked robust inhibition on postsynaptic layer 2/3 neurons. A simple computational model based on the experimentally determined electrophysiological properties of the different classes of layer 2/3 neurons and their unitary synaptic connectivity accounted for key aspects of the network activity evoked by optogenetic stimulation, including the strong recruitment of FS GABAergic neurons acting to suppress firing of excitatory neurons. We conclude that FS GABAergic neurons play an important role in neocortical microcircuit function through their strong local synaptic connectivity, which might contribute to driving sparse coding in excitatory layer 2/3 neurons of mouse barrel cortex in vivo.

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Similarity of Direction Tuning Among Responses to Stimulation of Different Whiskers in Neurons of Rat Barrel Cortex

Journal of Neurophysiology ◽

10.1152/jn.00113.2004 ◽

2005 ◽

Vol 94 (3) ◽

pp. 2004-2018 ◽

Cited By ~ 21

Author(s):

Hiroyuki Kida ◽

Satoshi Shimegi ◽

Hiromichi Sato

Keyword(s):

Barrel Cortex ◽

Direction Selectivity ◽

Specific Response ◽

Neuronal Responses ◽

Preferred Direction ◽

Fast Spiking ◽

Whisker Stimulation ◽

Direction Tuning ◽

Network Mechanism ◽

Stimulation Of

Cells in the rat barrel cortex exhibit stimulus-specific response properties. To understand the network mechanism of direction selectivity in response to facial whisker deflection, we examined direction selectivity of neuronal responses to single- and multiwhisker stimulations. In the case of regular-spiking units, i.e., putative excitatory cells, direction preferences were quite similar between responses to single-whisker stimulation of the principal and adjacent whiskers. In multiwhisker stimulation at short (≤5 ms) interstimulus intervals (ISIs), response facilitation was evoked only when the whiskers were deflected to the preferred direction of the response to the single whisker stimulation. These results suggest that there are neuronal networks among cells with different whisker preferences but with a common direction preference that could be the neuronal basis of the direction-selective facilitation of the response to multiwhisker stimulation. In contrast, multiwhisker stimulation at long (≥6 ms) ISIs caused non–direction-selective suppression of the response to the second stimulus. In the case of fast-spiking units, i.e., putative inhibitory cells, poor direction selectivity was exhibited. Thus stimulus direction is represented as the direction-selective responses to the single- and multiwhisker stimulations of putative excitatory cells rather than those of putative inhibitory cells.

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Cross-Whisker Adaptation of Neurons in Layer 2/3 of the Rat Barrel Cortex

Frontiers in Systems Neuroscience ◽

10.3389/fnsys.2021.646563 ◽

2021 ◽

Vol 15 ◽

Author(s):

Yonatan Katz ◽

Ilan Lampl

Keyword(s):

Cortical Neurons ◽

Barrel Cortex ◽

Receptive Fields ◽

Repetitive Stimulation ◽

Complex Environments ◽

Cortical Cells ◽

High Responsiveness ◽

Layer 2 ◽

Layer 4 ◽

Stimulation Of

Neurons in the barrel cortex respond preferentially to stimulation of one principal whisker and weakly to several adjacent whiskers. Such integration exists already in layer 4, the pivotal recipient layer of thalamic inputs. Previous studies show that cortical neurons gradually adapt to repeated whisker stimulations and that layer 4 neurons exhibit whisker specific adaptation and no apparent interactions with other whiskers. This study aimed to study the specificity of adaptation of layer 2/3 cortical cells. Towards this aim, we compared the synaptic response of neurons to either repetitive stimulation of one of two responsive whiskers or when repetitive stimulation of the two whiskers was interleaved. We found that in most layer 2/3 cells adaptation is whisker-specific. These findings indicate that despite the multi-whisker receptive fields in the cortex, the adaptation process for each whisker-pathway is mostly independent of other whiskers. A mechanism allowing high responsiveness in complex environments.

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Optical Stimulation of Thalamic Spindle Circuitry Sustains Electroencephalogram Patterns of General Anesthesia but not Duration of Loss of Consciousness

Neuroscience ◽

10.1016/j.neuroscience.2021.06.009 ◽

2021 ◽

Author(s):

Lia Mesbah-Oskui ◽

Patrick Gurges ◽

Wen-Ying Liu ◽

Richard L. Horner

Keyword(s):

General Anesthesia ◽

Loss Of Consciousness ◽

Optical Stimulation ◽

Stimulation Of

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Optical stimulation of semiconducting devices in the SEM

Microscopy of Semiconducting Materials, 1983 ◽

10.1201/9781003069614-60 ◽

2020 ◽

pp. 399-406

Author(s):

E F Maher ◽

P J Howard

Keyword(s):

Optical Stimulation ◽

Stimulation Of

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Mechanisms underlying the response of mouse cortical networks to optogenetic manipulation

eLife ◽

10.7554/elife.49967 ◽

2020 ◽

Vol 9 ◽

Cited By ~ 9

Author(s):

Alexandre Mahrach ◽

Guang Chen ◽

Nuo Li ◽

Carl van Vreeswijk ◽

David Hansel

Keyword(s):

Motor Cortex ◽

Numerical Simulations ◽

Barrel Cortex ◽

Population Models ◽

Gabaergic Interneurons ◽

Paradoxical Effect ◽

Form Complex ◽

Recurrent Excitation ◽

Layer 2

GABAergic interneurons can be subdivided into three subclasses: parvalbumin positive (PV), somatostatin positive (SOM) and serotonin positive neurons. With principal cells (PCs) they form complex networks. We examine PCs and PV responses in mouse anterior lateral motor cortex (ALM) and barrel cortex (S1) upon PV photostimulation in vivo. In ALM layer five and S1, the PV response is paradoxical: photoexcitation reduces their activity. This is not the case in ALM layer 2/3. We combine analytical calculations and numerical simulations to investigate how these results constrain the architecture. Two-population models cannot explain the results. Four-population networks with V1-like architecture account for the data in ALM layer 2/3 and layer 5. Our data in S1 can be explained if SOM neurons receive inputs only from PCs and PV neurons. In both four-population models, the paradoxical effect implies not too strong recurrent excitation. It is not evidence for stabilization by inhibition.

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