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The processing of somatosensory information in the mammalian brain involves the transmission of neural activity from the skin to the neocortex by way of parallel pathways that ascend through a hierarchical sequence of neural structures (1). Like those in other sensory systems, these ascending pathways are far outnumbered by corticofugal descending projections (2), which can act at multiple subcortical levels to modify the processing of sensory information (3). These connections define a recurrent network that is theoretically capable of generating complex emergent dynamic patterns of neural activity, manifested by synchronous oscillations or even chaotic behavior (4), that could be computationally useful (5). The existence of this network raises the question of whether large-scale coordinated activity of neural ensembles involving multiple levels of a sensory system (that is, brainstem, thalamus, and cortex) can play a fundamental role in the coding of sensory information. To address this issue, we simultaneously recorded up to 48 single neurons, distributed across up to five distinct processing relays of the trigeminal somatosensory system, in freely behaving rats (6). The rat trigeminal system is a multilevel, recurrently interconnected neuronal network, specialized for processing complex patterns of tactile stimuli generated by the repetitive contacts of facial whiskers with surrounding objects. Rats rely on rhythmic movements of their facial whiskers, much as humans rely on coordinated movements of their fingertips, to discriminate object shape and texture (7). Although the properties of single neurons belonging to this sensory system have been well studied under anesthetized conditions (8), little is known about information processing at the neural ensemble level during exploratory tactile behaviors.
The results described here are based on the long-term behavior of 424 single neurons chronically recorded in 11 animals. Sampled structures included the trigeminal ganglion (Vg, 17 cells), the principal (PrV, 52 cells) and spinal (SpV, 39 cells) trigeminal brainstem nuclei, the ventral posterior medial (VPM, 186 cells) and posterior medial (POm, 19 cells) nuclei of the thalamus, the primary somatosensory (SI, 95 cells) cortex, and the primary motor (MI, 32 cells) cortex. Pairwise cross correlation analysis was initially used to characterize the coordinated activity of simultaneously recorded neurons across the trigeminal system. Cross correlograms averaged around the spiking of a single representative VPM neuron (Fig. 1A) in each animal demonstrated the existence...