In the mammalian cerebral cortex the diversity of interneuronal subtypes underlies
a division of labour subserving distinct modes of inhibitory control. A unique mode
of inhibitory control may be provided by inhibitory neurons that specifically suppress
the firing of other inhibitory neurons. Such disinhibition could lead to the selective
amplification of local processing and serve the important computational functions
of gating and gain modulation. Although several interneuron populations are known
to target other interneurons to varying degrees, little is known about interneurons
specializing in disinhibition and their in vivo function. Here we show that a class
of interneurons that express vasoactive intestinal polypeptide (VIP) mediates disinhibitory
control in multiple areas of neocortex and is recruited by reinforcement signals.
By combining optogenetic activation with single-cell recordings, we examined the functional
role of VIP interneurons in awake mice, and investigated the underlying circuit mechanisms
in vitro in auditory and medial prefrontal cortices. We identified a basic disinhibitory
circuit module in which activation of VIP interneurons transiently suppresses primarily
somatostatin- and a fraction of parvalbumin-expressing inhibitory interneurons that
specialize in the control of the input and output of principal cells, respectively.
During the performance of an auditory discrimination task, reinforcement signals (reward
and punishment) strongly and uniformly activated VIP neurons in auditory cortex, and
in turn VIP recruitment increased the gain of a functional subpopulation of principal
neurons. These results reveal a specific cell type and microcircuit underlying disinhibitory
control in cortex and demonstrate that it is activated under specific behavioural
conditions.
