Diverse sources of GABAergic inhibition are a major feature of cortical networks,
but distinct inhibitory input systems have not been systematically characterized in
the thalamus. Here, we contrasted the properties of two independent GABAergic pathways
in the posterior thalamic nucleus of rat, one input from the reticular thalamic nucleus
(nRT), and one "extrareticular" input from the anterior pretectal nucleus (APT). The
vast majority of nRT-thalamic terminals formed single synapses per postsynaptic target
and innervated thin distal dendrites of relay cells. In contrast, single APT-thalamic
terminals formed synaptic contacts exclusively via multiple, closely spaced synapses
on thick relay cell dendrites. Quantal analysis demonstrated that the two inputs displayed
comparable quantal amplitudes, release probabilities, and multiple release sites.
The morphological and physiological data together indicated multiple, single-site
contacts for nRT and multisite contacts for APT axons. The contrasting synaptic arrangements
of the two pathways were paralleled by different short-term plasticities. The multisite
APT-thalamic pathway showed larger charge transfer during 50-100 Hz stimulation compared
with the nRT pathway and a greater persistent inhibition accruing during stimulation
trains. Our results demonstrate that the two inhibitory systems are morpho-functionally
distinct and suggest and that multisite GABAergic terminals are tailored for maintained
synaptic inhibition even at high presynaptic firing rates. These data explain the
efficacy of extrareticular inhibition in timing relay cell activity in sensory and
motor thalamic nuclei. Finally, based on the classic nomenclature and the difference
between reticular and extrareticular terminals, we define a novel, multisite GABAergic
terminal type (F3) in the thalamus.
