Electrical Coupling within Thalamocortical Networks Cumulatively Reduces Cortical Correlation to Sensory Inputs

Thalamocortical (TC) cells relay sensory information to the cortex as well as driving their own feedback inhibition through collateral excitation of the thalamic reticular nucleus (TRN). Inhibitory TRN cells are extensively coupled through electrical synapses. While electrical synapses are most often noted for synchronizing rhythmic forms of neuronal activity, their modulation of transient neuronal signals is less understood. Here we sought to characterize how electrical synapses embedded within a network of TRN neurons regulate the processing of ongoing sensory inputs during relay from thalamus to cortex. We constructed a thalamocortical network consisting of reciprocally connected Hodgkin-Huxley-style TC and TRN cells and one cortical output cell summing the TC activity. TRN cells were each electrically coupled to two neighboring cells, forming a ring topology. TC cells received synaptic inputs in sequence, with inputs separated by 10-50 ms, allowing us to assess the functional radius of an electrical synapse by comparing the cumulative effects of each additional TRN electrical synapse on responses within the network. Electrical synapse strength altered both TRN and TC spike response rates and latencies with each additional electrical synapse. Coupling within TRN modulated cortical integration of TC inputs by unexpectedly increasing response rates, duration, and reducing spike correlation to the input sequence that was presented to the TC layer. Thus, embedded TRN electrical synapses exert powerful influence on thalamocortical relay, highlighting the multisynaptic influences of electrically coupled cells on more complex and realistic networks of the brain.