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Giant Synapse in Thalamic Relay Cells

Urra Quiroz, Francisco José

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The thalamus processes and relays sensory information from the periphery to the cortex and from the cortex to other areas of the cortex. A trisynaptic pathway connects the whiskers with the somatosensory cortex. The principal nucleus of the trigeminal nerve (Pr5) in the brainstem receives sensory information from the whiskers and sends them to the ventral posteromedial nucleus of the thalamus (VPM), which in turn projects to the somatosensory cortex. The synaptic transmission between Pr5 and relay cells of the VPM is mediated by giant synapses, however, this transmission is poorly characterized. In this study we labeled trigeminothalamic (Pr5-VPM) giant terminals by stereotaxic delivery of adeno-associated virus particles (AAV) encoding synaptophysin-EGFP into the Pr5 nucleus of rats. Pr5-VPM giant terminals were identified in the VPM and directly stimulated with a double-barrel electrode after establishing whole-cell patch-clamp recordings from the postsynaptic relay neuron. This allowed us to study synaptic transmission in identified Pr5-VPM giant synapses for the first time . We found that stimulation of single terminals generates large postsynaptic responses, with a low probability of release, short-term depression and a fast recovery after a train of stimuli. Moreover, a single synaptic input shows a synaptic transfer function capable of generating a voltage-dependent postsynaptic spike response. Different currents modulate the spike response of relay cells. IA correspond to fast outward potassium currents generated by Kv1, Kv3 and/or Kv4 potassium channel subunits. We showed that IA currents in VPM relay cells are in part generated by Kv4.3 channels. Blockade of Kv4.3 channels decreased the amplitude response of relay cells to stimulation of Pr5-VPM synapses. In silico models can be used to explore the firing mechanisms of relay cells. We generated a model that considers the morphology of relay cells, the input location of large terminals and the electrophysiological information of Pr5-VPM synapses. The in silico model predicts stimulation of more than one terminal changes the spike response of the relay cell, increasing the number of spikes. The model also predicts the effects of decreasing IA or IT, the low threshold calcium current, in the relay cell response. Layer 5B (L5B) pyramidal neurons of the somatosensory cortex connect via relay neurons from the posteromedial nucleus (POm) to neurons of higher order somatosensory cortex. The synaptic transmission between L5B pyramidal neurons and POm relay cells is mediated by L5B-POm synapses. To place the properties of this synapse in the context of behavioral abilities developing during the first two months of postnatal life, it is required to know the synaptic maturation changes. We used the same approach as for the Pr5-VPM synapses project but we injected the AVV particles in the L5B and we recorded the responses in POm relay cells from mice at different ages. The frequency of spontaneous activity decreased over time, however, L5B-POm synapses did not show differences in EPSC evoked responses. Nevertheless, stimulation of single large terminals could generate spike responses in animals older than 4 to 5 weeks old. We described the properties of first order (Pr5-VPM) and higher order (L5B-POm) driver synapses involved in the whisker system of rodents. Stimulation of both synapses generated large amplitude responses and a strong depression. In addition, stimulation of single synapses in mature animals did generate spikes responses. Comparison of both giant synapses shows that both have remarkably similar properties, suggesting that both synaptic circuits, despite their different functions, employ similar information processing strategies. Sensory information reaches the cortex by the thalamus. The thalamus does not just work as the major relay center to the cortex, but it also processes the sensory information to be sent to the cortex depending on the level of attention of the organism. This work shows that the relay function of first order and higher order nuclei appears at the level of single synapses. In addition, the information processing function of the thalamus is also seen in a voltage-dependent transfer function of single synapses. The main task of the thalamus, to process and relay information, appears at the level of single relay cell synapses.

Item Type: Dissertation
Supervisor: Frings, Prof. Dr. Stephan
Place of Publication: Heidleberg
Date of thesis defense: 27 February 2014
Date Deposited: 17 Mar 2014 07:55
Date: 2014
Faculties / Institutes: The Faculty of Bio Sciences > Dean's Office of the Faculty of Bio Sciences
Subjects: 570 Life sciences
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