Abstract
Sleep-wake behaviors are important for survival and highly conserved among animal species. A growing body of evidence indicates that the midbrain dopaminergic system is associated with sleep-wake regulation in mammals. Songbirds exhibit mammalian-like sleep structures, and neurons in the midbrain ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) possess physiological properties similar to those in mammals. However, it remains uncertain whether the neurons in the songbird VTA/SNc are associated with sleep-wake regulation. Here, we show that VTA/SNc neurons in zebra finches exhibit arousal state-dependent alterations in spontaneous neural activity. By recording extracellular single-unit activity from anesthetized or freely behaving zebra finches, we found that VTA/SNc neurons exhibited increased firing rates during wakefulness, and the same population of neurons displayed reduced firing rates during anesthesia and slow-wave sleep. These results suggest that the songbird VTA/SNc is associated with the regulation of sleep and wakefulness along with other arousal regulatory systems. These findings raise the possibility that fundamental neural mechanisms of sleep-wake behaviors are evolutionarily conserved between birds and mammals.
Highlights
Midbrain dopaminergic neurons in the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) play an important role in a wide variety of behaviors such as learning, motivation, and movement (Berke, 2018)
We found that VTA/SNc neurons in zebra finches exhibit arousal state-dependent alterations in neural activity
In both isoflurane-induced anesthesia and natural sleepawake transitions, most VTA/SNc neurons showed increased spontaneous firing rates during wakefulness and a reduction in firing rates during slow-wave sleep. These results suggest that VTA/SNc neurons may play a role in regulating sleepwake transitions
Summary
Midbrain dopaminergic neurons in the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) play an important role in a wide variety of behaviors such as learning, motivation, and movement (Berke, 2018). The relationship between VTA/SNc and sleep-wakefulness has been relatively overlooked. In vivo electrophysiological studies in rats (Miller et al, 1983) and cats (Trulson and Preussler, 1984) showed that dopaminergic neurons in the VTA/SNc have similar firing rates during sleep and wakefulness, while a later study revealed enhanced burst firing during REM sleep (Dahan et al, 2007). Non-dopaminergic neurons in the VTA/SNc showed increased firing rates during wakefulness and REM sleep (Miller et al, 1983; Lee et al, 2001). A growing body of evidence supports the notion that VTA dopaminergic and non-dopaminergic neurons regulate sleep-wake behaviors in rodents. VTA dopaminergic neurons exhibit higher calcium activity during wakefulness and REM sleep than during non-REM sleep (Eban-Rothschild et al, 2016), and activation of dopaminergic neurons by optogenetics or
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