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

Prönneke, Alvar; Scheuer, Bianca; Wagener, Robin J.; Möck, Martin; Witte, Mirko; Staiger, Jochen F.

doi:10.1093/cercor/bhv202

Cited by 189 publications

(270 citation statements)

References 48 publications

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“…It is unlikely that the fast-spiking SCs reported in our study are identical to the small and nest basket cells reported in (23), because small and nest basket cells often display an adapting regularspiking firing pattern (unlike SCs) and were observed in neocortical L2/3 and L4 (unlike SCs) (23). In adult visual cortex, we found that L5 vasointestinal peptide (VIP-cre/Ai9 mice) (24) cells were very sparse, and the few we studied did not exhibit obvious bipolar morphology as previously reported in somatosensory cortex (25). Therefore, more work is needed to study the L5 VIP types.…”

supporting

confidence: 80%

Response to Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

Jiang

Shen

Sinz

et al. 2016

Science

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The critique of Barth et al. centers on three points: (i) the completeness of our study is overstated; (ii) the connectivity matrix we describe is biased by technical limitations of our brain-slicing and multipatching methods; and (iii) our cell classification scheme is arbitrary and we have simply renamed previously identified interneuron types. We address these criticisms in our Response. W e will address Barth et al.'s (1) three critiques of our Research Article (2) in turn.(i) The strength of our study is the number of connections tested (>11,000) in one species, cortical area, and age range, using the same experimental protocol. We agree that our study is not exhaustive, because it is focused on synaptic connectivity between interneurons in layers 1, 2/3, and 5, and we point this out in the abstract of the original paper. However, we do believe that no single study to date has presented a more complete wiring diagram of the adult neocortical microcircuit.(ii) Severed connections are a well-known limitation of slice recordings, which we discussed explicitly on p. 3 of the supplementary materials (SM) for (2). However, we do not agree that our study is substantially more susceptible to connection loss than previous patching studies, most of which also used 300-to 350-mm slices [we found fewer than half a dozen multipatching studies using 450-to 500-mm slices (3-5)]. Although cell depth is not reported in many of these studies, the depths at which we recorded (15 to 60 mm) seem typical (6). We patched cells at a wide range of intersomatic distances [see fig. S13A in (2)]; this range reflects the sparsity of labeled interneurons and is not a limitation of octuple patching.Like many previous studies, we used currentclamp mode to measure connectivity, which suffers less distance-dependent voltage attenuation compared with voltage clamp (7). Using potassium internal solution allowed us to characterize spiking properties and test bidirectional connectivity, whereas cesium-based internal solutions would prevent the patched neuron from firing. We discussed potential problems of voltage attenuation [SM for (2), p. 9], such as the underestimation of synaptic event amplitudes and potential nondetection of small synaptic events on the distal dendrites [e.g., connections from Martinotti cells onto layer 5 (L5) pyramidal neurons].To directly address Barth et al.'s concern that the connectivity matrix may be distorted due to slice cutting, we simulated the effect of slicing based on interneuron morphology (8) (Fig. 1A) [see also (6)] for the worst-case scenario where two neurons (pre-and postsynaptic) are both located 15-mm deep from the cutting surface. The resulting correction factor was similar across pairs of cell types (Fig. 1B), more or less scaling the entire connectivity matrix by a factor of 1.36 ± 0.10 (mean ± SD) (Fig. 1, C and D). Given these results and the fact that our connectivity principles mostly rely on the presence or absence of connectivity between specific types regardless of its magnitude, we believe ...

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supporting

confidence: 80%

Response to Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

Jiang

Shen

Sinz

et al. 2016

Science

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“…They imply, for instance, that, other than Martinotti cells, no other interneuron types were previously described in layer 5. This is at odds with publications reporting vasointestinal peptide (VIP) bipolar interneurons in layer 5 [e.g., (6) (7)]. The authors redefine and rename interneuron types resulting in claims of novel cell classes and improper acknowledgment of much of the literature.…”

mentioning

confidence: 96%

Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

Barth

Burkhalter

Callaway

et al. 2016

Science

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, aac9462) describe detailed experiments that substantially add to the knowledge of cortical microcircuitry and are unique in the number of connections reported and the quality of interneuron reconstruction. The work appeals to experts and laypersons because of the notion that it unveils new principles and provides a complete description of cortical circuits. We provide a counterbalance to the authors' claims to give those less familiar with the minutiae of cortical circuits a better sense of the contributions and the limitations of this study.

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“…This does not seem to be the case in the adult isocortex, where the Cre-driven labeling of the PV+, SST+, and VIP+ cells colocalizes in >95% cells with the expression of the respective reporter proteins (Pfeffer et al, 2013; Pronneke et al, 2015; Taniguchi et al, 2011). Similarly, subcortical PV-Cre and VIP-Cre labeling agrees well with available data for the respective mRNA and protein marker expression in the adult brain, while several thalamic and hypothalamic SST-Cre-positive areas do not appear to express SST in the adult brain, suggesting that these cell populations are indeed marked due to a transient developmental SST expression (see Anatomical Description in the STAR method).…”

Section: Discussionmentioning

confidence: 93%

“…Previous immunohistochemical studies characterized the relative laminar distribution of major interneuron cell types in the somatosensory and visual cortex (Gonchar et al, 2007; Pfeffer et al, 2013; Pronneke et al, 2015; Rudy et al, 2011; Xu et al, 2010), and our data showed that this pattern is indeed repeated across the entire isocortex: the PV+ and SST+ interneurons are most abundant in the layers 4–5 (PV+) and layers 4–6 (SST+), while the VIP+ interneurons show high density in the layers 1–4, with a peak in the layer 2/3 (Figure 3; see also Figure S5 for distribution based on distance from the brain surface).…”

Section: Resultsmentioning

confidence: 99%

Brain-wide Maps Reveal Stereotyped Cell-Type-Based Cortical Architecture and Subcortical Sexual Dimorphism

Kim

Yang

Pradhan

et al. 2017

Cell

343

530

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SUMMARY The stereotyped features of neuronal circuits are those most likely to explain the remarkable capacity of the brain to process information and govern behaviors, yet it has not been possible to comprehensively quantify neuronal distributions across animals or genders due to the size and complexity of the mammalian brain. Here we apply our quantitative brain-wide (qBrain) mapping platform to document the stereotyped distributions of mainly inhibitory cell types. We discover an unexpected cortical organizing principle: sensory-motor areas are dominated by output-modulating parvalbumin-positive interneurons, whereas association, including frontal, areas are dominated by input-modulating somatostatin-positive interneurons. Furthermore, we identify local cell type distributions with more cells in the female brain in seven out of eight sexually dimorphic subcortical areas, in contrast to the overall larger brains in males. The qBrain resource can be further mined to link stereotyped aspects of neuronal distributions to known and unknown functions of diverse brain regions.

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

Cited by 189 publications

References 48 publications

Response to Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

Response to Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

Comment on “Principles of connectivity among morphologically defined cell types in adult neocortex”

Brain-wide Maps Reveal Stereotyped Cell-Type-Based Cortical Architecture and Subcortical Sexual Dimorphism

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