Abstract
The “non-specific” ventromedial thalamic nucleus (VM) has long been considered a candidate for mediating cortical arousal due to its diffuse, superficial projections, but direct evidence was lacking. Here, we show in mice that the activity of VM calbindin1-positive matrix cells is high in wake and REM sleep and low in NREM sleep, and increases before cortical activity at the sleep-to-wake transition. Optogenetic stimulation of VM cells rapidly awoke all mice from NREM sleep and consistently caused EEG activation during slow wave anesthesia, while arousal did not occur from REM sleep. Conversely, chemogenetic inhibition of VM decreased wake duration. Optogenetic activation of the “specific” ventral posteromedial nucleus (VPM) did not cause arousal from either NREM or REM sleep. Thus, matrix cells in VM produce arousal and broad cortical activation during NREM sleep and slow wave anesthesia in a way that accounts for the effects classically attributed to “non-specific” thalamic nuclei.
Highlights
The “non-specific” ventromedial thalamic nucleus (VM) has long been considered a candidate for mediating cortical arousal due to its diffuse, superficial projections, but direct evidence was lacking
In parietal cortex (−1.8 A/P), secondary somatosensory cortex (S2) showed the strongest innervation (Supplementary Fig. 2C). These results in mice are highly consistent with previous evidence in other species showing that VM is comprised of Calb1positive matrix cells that targets layer 1 (L1) of most cortical areas[17,21,22]
We have shown here that matrix cells concentrated in the “nonspecific” thalamic nucleus VM powerfully control cortical activity and promote arousal, whereas the stimulation of core cells in the “specific” thalamic nucleus ventral posteromedial nucleus (VPM) has none of these effects
Summary
The “non-specific” ventromedial thalamic nucleus (VM) has long been considered a candidate for mediating cortical arousal due to its diffuse, superficial projections, but direct evidence was lacking. Ascribing a specific function to various thalamic nuclei, has been difficult, with a few notable exceptions, such as the definite role of the reticular thalamic nucleus in the generation of sleep spindles[7,8,9] One reason for this difficulty is that classical lesion studies were either incomplete or too broad, involving passing fibers[10,11,12]. LS interneurons correspond to neurogliaform cells, are strongly electrically coupled to each other, and inhibit both layer 2/3 pyramidal cells and non-LS cells fibers[23,24] Because of their connectivity, VM cells are potentially in a good position to affect cortical activity strongly and diffusely. By recording and stimulating VM neurons, we provide direct evidence for their role in cortical activation and arousal
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