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Characterizing VIP Neurons in the Barrel Cortex of VIPcre/tdTomato Mice Reveals Layer-Specific Differences.

ABSTRACT: Neocortical GABAergic interneurons have a profound impact on cortical circuitry and its information processing capacity. Distinct subgroups of inhibitory interneurons can be distinguished by molecular markers, such as parvalbumin, somatostatin, and vasoactive intestinal polypeptide (VIP). Among these, VIP-expressing interneurons sparked a substantial interest since these neurons seem to operate disinhibitory circuit motifs found in all major neocortical areas. Several of these recent studies used transgenic Vip-ires-cre mice to specifically target the population of VIP-expressing interneurons. This makes it necessary to elucidate in detail the sensitivity and specificity of Cre expression for VIP neurons in these animals. Thus, we quantitatively compared endogenous tdTomato with Vip fluorescence in situ hybridization and αVIP immunohistochemistry in the barrel cortex of VIPcre/tdTomato mice in a layer-specific manner. We show that VIPcre/tdTomato mice are highly sensitive and specific for the entire population of VIP-expressing neurons. In the barrel cortex, approximately 13% of all GABAergic neurons are VIP expressing. Most VIP neurons are found in layer II/III (∼60%), whereas approximately 40% are found in the other layers of the barrel cortex. Layer II/III VIP neurons are significantly different from VIP neurons in layers IV-VI in several morphological and membrane properties, which suggest layer-dependent differences in functionality.

SUBMITTER: Pronneke A

PROVIDER: S-EPMC4635925 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The recurrent network composed of excitatory and inhibitory neurons is fundamental to neocortical function. Inhibitory neurons in the mammalian neocortex are molecularly diverse, and individual cell types play unique functional roles in the neocortical microcircuit. Recently, vasoactive intestinal polypeptide-positive (VIP+) neurons, comprising a subclass of inhibitory neurons, have attracted particular attention because they can disinhibit pyramidal cells through inhibition of other types of inhibitory neurons, such as parvalbumin- (PV+) and somatostatin-positive (SOM+) inhibitory neurons, promoting sensory information processing. Although VIP+ neurons have been reported to receive synaptic inputs from PV+ and SOM+ inhibitory neurons as well as from cortical and thalamic excitatory neurons, the somatodendritic localization of these synaptic inputs has yet to be elucidated at subcellular spatial resolution. In the present study, we visualized the somatodendritic membranes of layer (L) 2/3 VIP+ neurons by injecting a newly developed adeno-associated virus (AAV) vector into the barrel cortex of VIP-Cre knock-in mice, and we determined the extensive ramification of VIP+ neuron dendrites in the vertical orientation. After immunohistochemical labeling of presynaptic boutons and postsynaptic structures, confocal laser scanning microscopy revealed that the synaptic contacts were unevenly distributed throughout the perisomatic (<100 μm from the somata) and distal-dendritic compartments (≥100 μm) of VIP+ neurons. Both corticocortical and thalamocortical excitatory neurons preferentially targeted the distal-dendritic compartment of VIP+ neurons. On the other hand, SOM+ and PV+ inhibitory neurons preferentially targeted the distal-dendritic and perisomatic compartments of VIP+ neurons, respectively. Notably, VIP+ neurons had few reciprocal connections. These observations suggest different inhibitory effects of SOM+ and PV+ neuronal inputs on VIP+ neuron activity; inhibitory inputs from SOM+ neurons likely modulate excitatory inputs locally in dendrites, while PV+ neurons could efficiently interfere with action potential generation through innervation of the perisomatic domain of VIP+ neurons. The present study, which shows a precise configuration of site-specific inputs, provides a structural basis for the integration mechanism of synaptic inputs to VIP+ neurons.

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Characterizing VIP Neurons in the Barrel Cortex of VIPcre/tdTomato Mice Reveals Layer-Specific Differences.

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