Millisecond timescale disinhibition mediates fast information transmission through an avian basal ganglia loop.
Journal of Neuroscience. 2009-12-09; 29(49): 15420-15433
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1. J Neurosci. 2009 Dec 9;29(49):15420-33. doi: 10.1523/JNEUROSCI.3060-09.2009.
Millisecond timescale disinhibition mediates fast information transmission
through an avian basal ganglia loop.
Leblois A(1), Bodor AL, Person AL, Perkel DJ.
(1)Department of Otolaryngology, University of Washington, Seattle, Washington
Avian song learning shares striking similarities with human speech acquisition
and requires a basal ganglia (BG)-thalamo-cortical circuit. Information
processing and transmission speed in the BG is thought to be limited by synaptic
architecture of two serial inhibitory connections. Propagation speed may be
critical in the avian BG circuit given the temporally precise control of
musculature during vocalization. We used electrical stimulation of the cortical
inputs to the BG to study, with fine time resolution, the functional connectivity
within this network. We found that neurons in thalamic and cortical nuclei that
are not directly connected with the stimulated area can respond to the
stimulation with extremely short latencies. Through pharmacological
manipulations, we trace this property back to the BG and show that the cortical
stimulation triggers fast disinhibition of the thalamic neurons. Surprisingly,
feedforward inhibition mediated by striatal inhibitory neurons onto BG output
neurons sometimes precedes the monosynaptic excitatory drive from cortical
afferents. The fast feedforward inhibition lengthens a single interspike interval
in BG output neurons by just a few milliseconds. This short delay is sufficient
to drive a strong, brief increase in firing probability in the target thalamic
neurons, evoking short-latency responses. By blocking glutamate receptors in
vivo, we show that thalamic responses do not appear to rely on excitatory drive,
and we show in a theoretical model that they could be mediated by postinhibitory
rebound properties. Such fast signaling through disinhibition and rebound may be
a crucial specialization for learning of rapid and temporally precise motor acts
such as vocal communication.
PMID: 20007467 [Indexed for MEDLINE]