Membrane Potential Dynamics of GABAergic Neurons in the Barrel Cortex of Behaving Mice

• Published in: Neuron (Cambridge, Mass.) Mass.), 2010-02, Vol.65 (3), p.422-435
• Main Authors: Gentet, Luc J., Avermann, Michael, Matyas, Ferenc, Staiger, Jochen F., Petersen, Carl C.H.
• Format: Article
• Language: English
• Subjects: Action Potentials - genetics; Animals; Behavior; Brain; Fourier transforms; gamma-Aminobutyric Acid - metabolism; Glutamate Decarboxylase - genetics; Green Fluorescent Proteins - genetics; Interneurons - physiology; Membrane Potentials - genetics; Membrane Potentials - physiology; Mice; Mice, Inbred C57BL; Mice, Transgenic; Microscopy; Models, Neurological; Movement - physiology; Neural Inhibition - physiology; Neurons; Nonlinear Dynamics; Patch-Clamp Techniques - methods; Somatosensory Cortex - cytology; Statistics as Topic; SYSNEURO; Vibrissae - innervation; Wakefulness
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2010.01.006

Computations in cortical circuits are mediated by synaptic interactions between excitatory and inhibitory neurons, and yet we know little about their activity in awake animals. Here, through single and dual whole-cell recordings combined with two-photon microscopy in the barrel cortex of behaving mice, we directly compare the synaptically driven membrane potential dynamics of inhibitory and excitatory layer 2/3 neurons. We find that inhibitory neurons depolarize synchronously with excitatory neurons, but they are much more active with differential contributions of two classes of inhibitory neurons during different brain states. Fast-spiking GABAergic neurons dominate during quiet wakefulness, but during active wakefulness Non-fast-spiking GABAergic neurons depolarize, firing action potentials at increased rates. Sparse uncorrelated action potential firing in excitatory neurons is driven by fast, large, and cell-specific depolarization. In contrast, inhibitory neurons fire correlated action potentials at much higher frequencies driven by slower, smaller, and broadly synchronized depolarization. [Display omitted] ► Two-photon targeted whole-cell recordings of GABAergic neurons in awake mice ► GABAergic neurons fire action potentials at higher rates than excitatory neurons ► Highly correlated membrane potential dynamics in GABAergic and excitatory neurons ► Behavior differentially modulates fast-spiking versus non-fast-spiking GABAergic neurons