Dendrodendritic and Axoaxonic Synapses in the Thalamic Reticular Nucleus of the Adult Rat

Abstract

Currently, it is believed that cell-cell communications occur in the thalamic reticular nucleus (RT) during thalamocortical operations, but the anatomical substrate underlying these intrinsic interactions has not been characterized fully in the rat yet. To further our knowledge on this issue, we stained juxtacellularly rat RT neurons with biocytin or Neurobiotin and examined their intrinsic axon collaterals and "axon-like processes" at both light and electron microscopic levels. Of 111 tracer-filled RT cells for which the axon could be followed from its origin up to the thalamus, 12 displayed short-range, poorly ramifying varicose local axon collaterals, which remained undistinguishable from parent distal dendrites, raising the question as to whether their varicosities were presynaptic terminals. Correlated light and electron microscopic observations of the proximal part of these intrinsic varicose axonal segments revealed that their varicosities and intervaricose segments were, in fact, postsynaptic structures contacted by a large number of boutons that, for the most, formed asymmetric synapses and were nonimmunoreactive for GABA. Similarly, the so-called "axon-like processes" stemming from the soma or dendrites also were identified as postsynaptic structures. Two unexpected observations were made in the course of this analysis. First, the hillock and initial segment of some RT axons were found to receive asymmetric synaptic inputs from GABA-negative terminals. Second, examination of serial ultrathin sections of dendritic bundles cut in their longitudinal plane revealed the existence of several short symmetric dendrodendritic synapses and numerous puncta adhaerentia between component dendrites. In conclusion, dendrodendritic junctions might be a prominent anatomical substrate underlying interneuronal communications in the RT of the adult rat. Furthermore, excitatory axoaxonic synapses on the axon hillock, initial segment, and local axon collaterals might represent a powerful synaptic drive for synchronizing the firing of RT neurons. Future studies are essential to verify whether excitatory axoaxonic synapses with the axon hillock are a general feature in the RT.