Diversity and Connectivity of Layer 5 Somatostatin-Expressing Interneurons in the Mouse Barrel Cortex

• Published in: The Journal of neuroscience 2018-02, Vol.38 (7), p.1622-1633
• Main Authors: Nigro, Maximiliano José, Hashikawa-Yamasaki, Yoshiko, Rudy, Bernardo
• Format: Article
• Language: English
• Subjects: Activity patterns; Animals; Correlation analysis; Cortex (barrel); Cortex (somatosensory); Dendrites; Dendrites - physiology; Dendrites - ultrastructure; Dendritic structure; Electrophysiological Phenomena - physiology; Female; Firing pattern; In Vitro Techniques; Information processing; Interneurons; Interneurons - physiology; Interneurons - ultrastructure; Male; Mice; Molecular properties; Morphology; Neural Inhibition - physiology; Neural networks; Neural Pathways - cytology; Neural Pathways - physiology; Neural Pathways - ultrastructure; Neurons; Neurons - physiology; Neurons - ultrastructure; Pyramidal cells; Pyramidal Cells - physiology; Pyramidal Cells - ultrastructure; Rodents; Sensory integration; Shape recognition; Somatosensory Cortex - cytology; Somatosensory Cortex - physiology; Somatostatin; Somatostatin - biosynthesis; Somatostatin - genetics; Spiking; T shape; γ-Aminobutyric acid
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.2415-17.2017

Inhibitory interneurons represent 10-15% of the neurons in the somatosensory cortex, and their activity powerfully shapes sensory processing. Three major groups of GABAergic interneurons have been defined according to developmental, molecular, morphological, electrophysiological, and synaptic features. Dendritic-targeting somatostatin-expressing interneurons (SST-INs) have been shown to display diverse morphological, electrophysiological, and molecular properties and activity patterns However, the correlation between these properties and SST-IN subtype is unclear. In this study, we aimed to correlate the morphological diversity of layer 5 (L5) SST-INs with their electrophysiological and molecular diversity in mice of either sex. Our morphological analysis demonstrated the existence of three subtypes of L5 SST-INs with distinct electrophysiological properties: T-shaped Martinotti cells innervate L1, and are low-threshold spiking; fanning-out Martinotti cells innervate L2/3 and the lower half of L1, and show adapting firing patterns; non-Martinotti cells innervate L4, and show a quasi-fast spiking firing pattern. We estimated the proportion of each subtype in L5 and found that T-shaped Martinotti, fanning-out Martinotti, and Non-Martinotti cells represent ∼10, ∼50, and ∼40% of L5 SST-INs, respectively. Last, we examined the connectivity between the three SST-IN subtypes and L5 pyramidal cells (PCs). We found that L5 T-shaped Martinotti cells inhibit the L1 apical tuft of nearby PCs; L5 fanning-out Martinotti cells also inhibit nearby PCs but they target the dendrite mainly in L2/3. On the other hand, non-Martinotti cells inhibit the dendrites of L4 neurons while avoiding L5 PCs. Our data suggest that morphologically distinct SST-INs gate different excitatory inputs in the barrel cortex. Morphologically diverse layer 5 SST-INs show different patterns of activity in behaving animals. However, little is known about the abundance and connectivity of each morphological type and the correlation between morphological subtype and spiking properties. We demonstrate a correlation between the morphological and electrophysiological diversity of layer 5 SST-INs. Based on these findings we built a classifier to infer the abundance of each morphological subtype. Last, using paired recordings combined with morphological analysis, we investigated the connectivity of each morphological subtype. Our data suggest that, by targeting different cell types and cellular compartments