Abstract
Neocortico-thalamo-cortical loops represent a common, yet poorly understood, circuit employing giant synapses also referred to as “class I”, giant, or driver synapses. Here, we characterize a giant synapse formed by projection neurons of the paleocortical piriform cortex (PIR) onto neurons of the mediodorsal thalamus (MD). Three-dimensional (3D) ultrastructure of labeled PIR-MD terminals, obtained by using serial-section scanning electron microscopy (EM) combined with photooxidation-based detection of labeled terminals, revealed a large terminal engulfing multiple postsynaptic dendritic excrescences. The terminal contained multiple synaptic contacts, a high density of synaptic vesicles and several central mitochondria. Using targeted stimulations of single identified PIR-MD terminals in combination with patch-clamp recordings from the connected MD neuron, we found large postsynaptic currents with fast kinetics and strong short-term depression, yet fast recovery upon repetitive stimulation. We conclude that the phylogenetically old paleocortex already developed giant synaptic connections exhibiting similar functional properties as connections formed by giant neocortico-thalamic projections.
Highlights
Cortico-thalamo-cortical loops operating giant synaptic connections between cortex and thalamus are a characteristic feature of primary sensory cortices and have been described for associative cortices (Sherman and Guillery, 2006, 2011)
We address the question if these, in the phylogenetical context, first giant synaptic connections between piriform cortex (PIR) and mediodorsal thalamus (MD) share similar features with giant synapses formed by neocortical areas
Subsequent to the expression period of 12–37 days, expression of the reporter protein was found in the somata of PIR neurons (Figure 1B) and their terminations in the MD (Figure 1C)
Summary
Cortico-thalamo-cortical loops operating giant synaptic connections between cortex and thalamus are a characteristic feature of primary sensory cortices and have been described for associative cortices (Sherman and Guillery, 2006, 2011). While their systemic function remains elusive, these giant synapses have been first reported in electron microscopic studies (Hoogland et al, 1991; Kuroda and Price, 1991). This connection could be relevant for higher cortical processing of olfactory information (Slotnick and Risser, 1990; Kuroda and Price, 1991; Plailly et al, 2008), yet, the role of PIR-MD giant synapses in the olfactory circuit is currently not understood (reviewed in Courtiol and Wilson, 2015).
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