Segregation of nociceptive and non-nociceptive networks in the squirrel monkey somatosensory thalamus

The somatosensory thalamus (here we examine neurons in the caudal cutaneous portion of ventral posterior lateral nucleus, VPL) is composed of a somatotopic arrangement of anteroposteriorly oriented rods. Each rod is a collection of neurons with homogeneous properties that relay sensory information to specific cortical columns. We developed a multi-electrode recording technique, using fixed-geometry four-tip electrodes that allow simultaneous recordings from small populations of neurons (4-11), in a ~150 X 150 X 150 μm³ volume of brain tissue (i.e., the approximate diameter of rods) and study of their spatiotemporal interactions. Due to the fixed geometry of the four-tip electrodes, the relative locations of these neurons can be determined, and due to the simultaneity of the recordings, their spike-timing coordination can be calculated. With this method, we demonstrate the existence of two distinct functional networks: nociceptive and non- nociceptive networks. The population dynamics of these two types of networks are different: cross-correlations in each type of network were different in direction and strength, were a function of the distance between neurons, had an opponent organization for nociceptive networks and a non-opponent organization for non-nociceptive networks, and rapidly changed under different stimulus conditions independent of changes in firing rates. A simple neural network model mimicked these physiological findings, demonstrating the necessity of inhibitory interneurons and different amounts of afferent input synchronization. Based on these results, we conclude that the somatosensory thalamus is composed of two modules, nociceptive and non- nociceptive rods, and that the response dynamics differences between these modules are due to spatiotemporal differences of their afferent inputs.