Abstract
Cortical state modulates the background activity of cortical neurons, and their evoked response to sensory stimulation. Multiple mechanisms are involved in switching between cortical states including various neuromodulatory systems. Locus Coeruleus (LC) is one of the major neuromodulatory nuclei in the brainstem with widespread projections throughout the brain and modulates the activity of cells and networks. Here, we quantified the link between the LC spontaneous activity, cortical state and sensory processing in the rat vibrissal somatosensory “barrel” cortex (BC). We simultaneously recorded unit activity from LC and BC along with prefrontal electroencephalogram (EEG) while presenting brief whisker deflections under urethane anesthesia. The ratio of low to high frequency components of EEG (referred to as the L/H ratio) was employed to identify cortical state. We found that the spontaneous activity of LC units exhibited a negative correlation with the L/H ratio. Cross-correlation analysis revealed that changes in LC firing preceded changes in the cortical state: the correlation of the LC firing profile with the L/H ratio was maximal at an average lag of −1.2 s. We further quantified BC neuronal responses to whisker stimulation during the synchronized and desynchronized states. In the desynchronized state, BC neurons showed lower stimulus detection threshold, higher response fidelity, and shorter response latency. The most prominent change was observed in the late phase of BC evoked activity (100–400 ms post stimulus onset): almost every BC unit exhibited a greater late response during the desynchronized state. Categorization of the BC evoked responses based on LC activity (into high and low LC discharge rates) resulted in highly similar response profiles compared to categorization based on the cortical state (low and high L/H ratios). These findings provide evidence for the involvement of the LC neuromodulatory system in desynchronization of cortical state and the consequent enhancement of sensory coding efficiency.
Highlights
In order to adapt to various environmental and behavioral demands, the brain switches between multiple modes of processing
We quantified the link between cortical state, spontaneous Locus Coeruleus (LC) activity, and sensory processing in the rat barrel” cortex (BC)
We demonstrated that spontaneous fluctuations in LC firing rate preceded changes in the cortical state by an average of 1.2 s
Summary
In order to adapt to various environmental and behavioral demands, the brain switches between multiple modes of processing. The synchronized state is associated with slow-wave sleep and quiet waking whereas the desynchronized state is associated with active waking and rapid eye movement (REM) sleep (Steriade et al, 1993; Poulet and Petersen, 2008; Lee and Dan, 2012; McCormick et al, 2015). Both states are observed during anesthesia in rodents and primates (Murakami et al, 2005; Clement et al, 2008; Cheong et al, 2011; Bermudez Contreras et al, 2013; Pachitariu et al, 2015). Multiple mechanisms are suggested to be involved in the switches between the cortical states including thalamic input (Hirata and Castro-Alamancos, 2010; Poulet et al, 2012), motor cortex feedback (Zagha et al, 2013) and the neuromodulatory systems (Lee and Dan, 2012; Sara and Bouret, 2012; Eggermann et al, 2014; Zagha and McCormick, 2014)
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