Thalamocortical circuits are involved in the transfer of sensory information to the cortex, as well as corticocortical communication. Information transfer through thalamocortical circuits is dynamically regulated by intrathalamic circuitry and external afferents (e.g. corticothalamic and brainstem inputs), but the degree to which synaptic plasticity occurs in the thalamus is not well characterized. I sought to investigate the role of activity-dependent synaptic plasticity in thalamic neurons. Electrophysiological recordings were obtained from thalamocortical relay neurons in the dorsal lateral geniculate nucleus (dLGN), ventrobasal nucleus (VB), and neurons in the thalamic reticular nucleus (TRN) using in vitro slice preparations. I first address the role of state-dependent synaptic plasticity by determining the influence of thalamic action potential firing modes on plasticity. Thalamic neurons ubiquitously fire in either burst or tonic firing modes, which are mediated by voltage-dependent T-type Ca2+ channels. Since the firing mode can change based on an organism’s behavioral state, findings regarding the role of plasticity with respect to burst and tonic firing will be valuable in determining how sensory information transfer is modulated. I show that thalamic relay neurons display short-term alterations in excitatory synaptic responses following postsynaptic pairing (i.e., burst or tonic firing) paired with corticothalamic activation. The magnitude and frequency of occurrence of short-term depression or facilitation differed depending on the firing state of the postsynaptic neuron. This plasticity was not observed when primary sensory afferents (retinogeniculate fibers) were stimulated, indicating the changes observed are restricted to corticothalamic inputs. TRN neurons, display depression following paired burst firing, which may affect the way in which the TRN mediates relay neuron activity in the thalamocortical circuit.When unpaired tetanic stimulation of corticothalamic afferents is applied, most thalamic neurons display short-term facilitation, irrespective of firing mode. I next elucidated the mechanism of activity-dependent short-term plasticity in thalamic relay neurons. I show that short-term facilitation is Ca2+-dependent and mediated by the adenylyl cyclase pathway. Adenylyl cyclase activation and cAMP production could lead to downstream modifications in ion channels. Blocking K+ currents and inhibiting hyperpolarization-activated cyclic-nucleotide modulated currents attenuated the tetanus-induced facilitation, indicating the dependence of K+ channels and the hyperpolarization-activated current (Ih) to this plasticity. I hypothesize that short-lasting alterations in these currents leads to the observed enhancement in neurotransmitter release and facilitation of the postsynaptic response following tetanic stimulation. Novel findings regarding synaptic plasticity in the thalamocortical circuit can have major implications on the role of cortical feedback on information transfer through the thalamus to the neocortex. Enhancing excitatory activity at corticothalamic synapses can influence the relay of sensory information to the cortex, increase thalamic throughput, and potentially impact the nature of sensory information.
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