Cross-correlation analysis of a recurrent inhibitory circuit in the rat thalamus

Spontaneous activities of vibrissa-responding neurons in the rat ventrobasal complex (VB) and somatosensory part of the thalamic reticular nucleus (S-TR) were simultaneously recorded and subjected to cross-correlation analysis to investigate the functional organization of recurrent inhibitory action of the S-TR on VB neurons. Excitatory and/or inhibitory interactions were found between approximately 75% (25/34) of the pairs of S-TR and VB neurons with receptive fields (RFs) on the same vibrissa. In contrast, there was no significant interaction between 54 pairs of neurons having RFs on different vibrissae. Among the pairs of neurons with RFs on the same vibrissa, there were four types of correlations, which indicate the following connections: monosynaptic excitation from a VB to an S-TR neuron (7 pairs), monosynaptic inhibition from an S-TR to a VB neuron (10 pairs), reciprocal connection combining the above two types (7 pairs), and common excitation in addition to inhibition from an S-TR to a VB neuron (1 pair). Examples of divergence and convergence of connections between S-TR and VB neurons were demonstrated by testing one S-TR (VB) neuron with more than one VB (S-TR) neuron. Vibrissa-suppressed VB cells, which had exclusively inhibitory RFs, were included in eight pairs of the above samples. These VB cells were more likely to receive inhibitory inputs from S-TR neurons than other VB neurons. Cells with RFs on multiple vibrissae were included in the other 10 pairs. These multiple-vibrissa cells had no interaction with single-vibrissa cells but did with multiple-vibrissa cells. From the incidence of four types of correlation between S-TR and VB neurons with RFs on the same vibrissa, the following connection pattern is suggested: One S-TR neuron receives excitatory inputs from approximately 40% of the VB neurons with RFs on the same vibrissa and sends inhibitory outputs to approximately 55%. Since these two groups of VB neurons were overlapping, the S-TR neuron has reciprocal connections with approximately 20% of the VB neurons with RFs on the same vibrissa. The same estimate was applied to connectivity of one VB neuron. These results indicate that both inputs and outputs of S-TR neurons are precisely and topographically organized, although there is convergence to and divergence from a substantial number of VB neurons with RFs on the same vibrissa. It is proposed that the recurrent inhibitory circuit through the S-TR plays a role in improving discrimination of sensory information transmitted through the VB.