Abstract
The pulvinar nucleus of the tree shrew receives both topographic (specific) and nontopographic (diffuse) projections from superior colliculus (SC), which form distinct synaptic arrangements. We characterized the physiological properties of these synapses and describe two distinct types of excitatory postsynaptic potentials (EPSPs) that correlate with structural properties of the specific and diffuse terminals. Synapses formed by specific terminals were found to be significantly longer than those formed by diffuse terminals. Stimulation of these two terminal types elicited two types of EPSPs that differed in their latency and threshold amplitudes. In addition, in response to repetitive stimulation (0.5–20 Hz) one type of EPSP displayed frequency-dependent depression whereas the amplitudes of the second type of EPSP were not changed by repetitive stimulation of up to 20Hz. To relate these features to vesicle release, we compared the synapsin content of terminals in the pulvinar nucleus and the dorsal lateral geniculate (dLGN) by combining immunohistochemical staining for synapsin I or II with staining for the type 1 or type 2 vesicular glutamate transporters (markers for corticothalamic and tectothalamic/retinogeniculate terminals, respectively). We found that retinogeniculate terminals do not contain either synapsin I or synapsin II, corticothalamic terminals in the dLGN and pulvinar contain synapsin I, but not synapsin II, whereas tectopulvinar terminals contain both synapsin I and synapsin II. Finally, both types of EPSPs showed a graded increase in amplitude with increasing stimulation intensity, suggesting convergence; this was confirmed using a combination of anterograde tract tracing and immunocytochemisty. We suggest that the convergent synaptic arrangements, as well as the unique synapsin content of tectopulvinar terminals, allow them to relay a dynamic range of visual signals from the SC.
Highlights
Three main types of glutamatergic terminals have been identified in the visual dorsal thalamus of rodents, carnivores, primates, and tree shrews
Diffuse and specific excitatory postsynaptic potentials (EPSPs) Based on differences in their convergence patterns, we suggest that the slower latency, smaller amplitude EPSPs represent activation of diffuse tectopulvinar projections, while the faster, larger amplitude EPSPs represent activation of specific tectopulvinar projections
This suggestion is based on comparisons to our previous study of EPSPs elicited by stimulation of tectothalamic axons in the rat
Summary
Three main types of glutamatergic terminals have been identified in the visual dorsal thalamus of rodents, carnivores, primates, and tree shrews. The role of tectothalamic RM profiles is less clear, but they appear to form a third functional class of terminals [21,22]; it has been suggested that the collective activities of multiple convergent RM inputs are critical for the formation of the receptive field properties of postsynaptic neurons. RS profiles make single synaptic contacts [16,17,24] and their stimulation elicits smaller amplitude EPSPs that facilitate with high frequency stimulation [23,25,28,29,30] These features have been linked to the distribution of synapsin I and synapsin II, proteins that tether a reserve pool of synaptic vesicles [31,32,33,34,35]. These proteins are found in corticogeniculate (RS) terminals but not retinogeniculate (RL) terminals, and in synapsin I/II knockout mice the short-term plasticity of corticogeniculate EPSPs is altered, while retinogeniculate EPSPs are unchanged [36]
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