Abstract
The cellular and synaptic mechanisms driving cell-type-specific function during various cortical network activities and behaviors are poorly understood. Here, we targeted whole-cell recordings to two classes of inhibitory GABAergic neurons in layer 2/3 of the barrel cortex of awake head-restrained mice and correlated spontaneous membrane potential dynamics with cortical state and whisking behavior. Using optogenetic stimulation of single layer 2/3 excitatory neurons we measured unitary excitatory postsynaptic potentials (uEPSPs) across states. During active states, characterized by whisking and reduced low-frequency activity in the local field potential, parvalbumin-expressing neurons depolarized and, albeit in a small number of recordings, received uEPSPs with increased amplitude. In contrast, somatostatin-expressing neurons hyperpolarized and reduced firing rates during active states without consistent change in uEPSP amplitude. These results further our understanding of neocortical inhibitory neuron function in awake mice and are consistent with the hypothesis that distinct genetically-defined cell classes have different state-dependent patterns of activity.
Highlights
We identified periods of high and low local field potential (LFP) power in the 1–5 Hz frequency band, as the amplitude of low frequency activity is known to correlate with various levels of arousal and to be modulated by movement (Steriade, 2000; Gervasoni et al, 2004; Crochet and Petersen, 2006; McGinley et al, 2015)
Cortical states with high 1–5 Hz LFP power largely occurred during non-whisking periods, whereas whisking periods were dominated by low 1–5 Hz LFP power (Figure 2—figure supplement 2)
We distinguished the two predominant non-overlapping states: Quiet periods defined as epochs with high 1–5 Hz LFP power without whisker movement, and Active periods defined as epochs with low 1–5 Hz LFP power accompanied by whisker movement
Summary
In cortical excitatory neurons, reduced low-frequency neocortical EEG or local field potential (LFP) activity, such as that observed during active behaviors, consistently correlates with a decrease in membrane potential (Vm) variance through a reduction in the amplitude of low-frequency Vm fluctuations, accompanied, on average, by Vm depolarization (Steriade et al, 2001; Timofeev et al, 2001; Crochet and Petersen, 2006; Poulet and Petersen, 2008; Yamashita et al, 2013; Bennett et al, 2013; Polack et al, 2013; Schneider et al, 2014; Reimer et al, 2014; Zhao et al, 2016). In layer 2/3 (L2/3) mouse primary somatosensory whisker barrel cortex (wS1), fast-spiking inhibitory neurons were found to decrease AP firing during whisking with little change in mean Vm but decreased Vm variance (Gentet et al, 2010). Parvalbumin-expressing (PV) neurons in L2/3 mouse visual cortex exhibited Vm depolarization accompanied by an increase in AP firing during locomotion (Polack et al, 2013). Disparities exist amongst somatostatin-expressing (Sst) neurons, which are inhibited during whisking in L2/3 of wS1 (Gentet et al, 2012; Lee et al, 2013; Munoz et al, 2017), and either excited or inhibited by locomotion in L2/3 visual cortex (Polack et al, 2013; Reimer et al, 2014).
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