RT Journal Article
SR Electronic
T1 Millisecond Timescale Disinhibition Mediates Fast Information Transmission through an Avian Basal Ganglia Loop
JF The Journal of Neuroscience
JO J. Neurosci.
FD Society for Neuroscience
SP 15420
OP 15433
DO 10.1523/JNEUROSCI.3060-09.2009
VO 29
IS 49
A1 Arthur Leblois
A1 Ágnes L. Bodor
A1 Abigail L. Person
A1 David J. Perkel
YR 2009
UL http://www.jneurosci.org/content/29/49/15420.abstract
AB 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.