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). The GABAergic cells of the TRN are extensively coupled through electrical synapses. While electrical synapses are most often noted for their roles in synchronizing rhythmic forms of neuronal activity, they are also positioned to modulate responses to transient information flow across and throughout the brain, although this effect is seldom explored. Here we sought to understand how electrical synapses embedded within a network of TRN neurons regulate the processing of ongoing sensory inputs during relay from thalamus to cortex. We used Hodgkin-Huxley point models to construct a network of a 9 TC and 9 TRN cells, with one cortical output neuron summing the TC activity. Each pair of TC and TRN cells was reciprocally coupled by chemical synapses. TRN cells were each electrically coupled to two neighboring cells, forming a ring topology. TC cells received synaptic inputs in sequence, with intervals between inputs varying from 10 to 50 ms across simulations. This architecture and sequence of inputs allowed us to assess the functional radius of an electrical synapse by comparing the cumulative effects of each additional TRN electrical synapse on the responses of the TRN and TC cells and the cortical output. Effects of electrical synapses on TRN cell activity were strongest for smaller intervals between inputs, and cumulative with additional synapses. In contrast, effects in TC neurons were strongest for larger intervals between inputs and also increased with coupling strength. 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, in a cumulative manner. These results highlight the multi-synaptic influences of electrically coupled cells and reinforce that they should be included in more complex and realistic networks of the brain.