Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing
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eLife assessment
This manuscript reports the response by cortical interneurons from mice expressing genetically defined fluorescent markers to sensory stimulation performed in awake animals without anesthesia. The data show in some cases distinct responses in specific neuron types. This manuscript contains unique information that will be valuable to other researchers in the field and influence future research in the field of cortical GABAergic neurons.
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Abstract
Neocortical neurons can increasingly be divided into well-defined classes, but their activity patterns during quantified behavior remain to be fully determined. Here, we obtained membrane potential recordings from various classes of excitatory and inhibitory neurons located across different cortical depths in the primary whisker somatosensory barrel cortex of awake head-restrained mice during quiet wakefulness, free whisking and active touch. Excitatory neurons, especially those located superficially, were hyperpolarized with low action potential firing rates relative to inhibitory neurons. Parvalbumin-expressing inhibitory neurons on average fired at the highest rates, responding strongly and rapidly to whisker touch. Vasoactive intestinal peptide-expressing inhibitory neurons were excited during whisking, but responded to active touch only after a delay. Somatostatin-expressing inhibitory neurons had the smallest membrane potential fluctuations and exhibited hyperpolarising responses at whisking onset for superficial, but not deep, neurons. Interestingly, rapid repetitive whisker touch evoked excitatory responses in somatostatin-expressing inhibitory neurons, but not when the intercontact interval was long. Our analyses suggest that distinct genetically-defined classes of neurons at different subpial depths have differential activity patterns depending upon behavioral state providing a basis for constraining future computational models of neocortical function.
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eLife assessment
This manuscript reports the response by cortical interneurons from mice expressing genetically defined fluorescent markers to sensory stimulation performed in awake animals without anesthesia. The data show in some cases distinct responses in specific neuron types. This manuscript contains unique information that will be valuable to other researchers in the field and influence future research in the field of cortical GABAergic neurons.
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Reviewer #1 (Public Review):
This manuscript attempts to disclose new insights into barrel cortex cell class-dependent and cell depth-dependent membrane potential (Vm) dynamics during active whisker sensing. The results highlight similarities but also specific differences between different types of cortical neurons. The approach used is very effective and direct: somatosensory stimulation is performed in awake animals without anesthesia, the neurons are recorded with intracellular whole cell patch clamp recording that can provide fast responses with high resolution, and the identification of various neuron types is achieved by using mice expressing genetically defined selective fluorescent markers. The results support the main conclusions. The work is an extension of previous, similar work performed by this group, However, most previous …
Reviewer #1 (Public Review):
This manuscript attempts to disclose new insights into barrel cortex cell class-dependent and cell depth-dependent membrane potential (Vm) dynamics during active whisker sensing. The results highlight similarities but also specific differences between different types of cortical neurons. The approach used is very effective and direct: somatosensory stimulation is performed in awake animals without anesthesia, the neurons are recorded with intracellular whole cell patch clamp recording that can provide fast responses with high resolution, and the identification of various neuron types is achieved by using mice expressing genetically defined selective fluorescent markers. The results support the main conclusions. The work is an extension of previous, similar work performed by this group, However, most previous Vm studies in the mouse barrel cortex during behavior have largely focused on superficial neurons located in the upper ~300 μm of the neocortex since these are more easily targeted through two-photon microscopy. In this study, the authors extend current knowledge by investigating Vm dynamics across a greater range of depths including two-photon targeted whole-cell recordings across the upper ~600 μm of the neocortex. I believe that this manuscript uses a demanding, but excellent approach that will be useful to other researchers in the field. The manuscript is likely to be influential.
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Reviewer #2 (Public Review):
This paper is a technical tour de force and provides interesting results. This group has indeed contributed to the understanding of membrane potential and firing dynamics of different cortical neuron subclasses during sensation in various previous papers. Yet, the paper falls short in providing a cohesive conclusion and interpretation of their results on pyramidal neurons, PV, SST, and VIP cells in response to free whisking and active touch at different cortical depths. The authors clearly claim that this manuscript aims to extend the current knowledge by investigating Vm dynamics of pyramidal neurons and various GABAergic subtypes across a greater range of cortical depths. The major shortcoming of this paper is indeed a lack of a clear conclusion or picture of how different cortical neuron types are engaged …
Reviewer #2 (Public Review):
This paper is a technical tour de force and provides interesting results. This group has indeed contributed to the understanding of membrane potential and firing dynamics of different cortical neuron subclasses during sensation in various previous papers. Yet, the paper falls short in providing a cohesive conclusion and interpretation of their results on pyramidal neurons, PV, SST, and VIP cells in response to free whisking and active touch at different cortical depths. The authors clearly claim that this manuscript aims to extend the current knowledge by investigating Vm dynamics of pyramidal neurons and various GABAergic subtypes across a greater range of cortical depths. The major shortcoming of this paper is indeed a lack of a clear conclusion or picture of how different cortical neuron types are engaged by different states. Overall, I struggle to find a novel message emerging from the present manuscript that hasn't already been described by the same lab. And this is a pity, as the experiments are of the highest quality and the data is definitely hard-won.
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Reviewer #3 (Public Review):
The manuscript by Kirtani et al. describes intracellular recordings from barrel cortex neurons identified under 2p microscopy in vivo during whisking. The major strengths of this work are that it is a technical feat and represents a unique dataset. It is a building block for future studies. The major weakness however is that it is a purely descriptive and observational study. There are no experimental manipulations, nor are there attempts to integrate the observations into a larger framework. As a result, there are no mechanistic or functional insights from this study. There is some speculation and discussion about how these results might fit into other studies of circuit connectivity or computational modeling, however, but this is relatively limited.
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