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The stimulus-evoked response of a cortical neuron depends on both details of the afferent signal and the momentary state of the larger network in which it is embedded. Consequently, identical sensory stimuli evoke highly variable responses. Using simultaneous recordings of thalamic barreloid and/or cortical barrel neurons in the rat whisker-to-barrel pathway, we determined the extent to which the responses of pairs of cells covary on a trial-by-trial basis. In the thalamus and cortical layer IV, a substantial component of trial-to-trial variability is independent of the specific parameters of the stimulus, probed here using deflection angle. These stimulus-nonspecific effects resulted in greater-than-chance similarities in trial-averaged angular tuning among simultaneously recorded pairs of barrel neurons. Such effects were not observed among simultaneously recorded thalamic and cortical barrel neurons, suggesting strong intracortical mechanisms of synchronization. Sensory adaptation produced by prior whisker deflections reduced response magnitudes and enhanced the joint angular tuning of simultaneously recorded neurons. Adaptation also decorrelated stimulus-evoked responses, rendering trial-by-trial responses of neuron pairs less similar to each other. Adaptation-induced decorrelation coupled with sharpened joint tuning could enhance the saliency of cells within thalamus or cortex that continue to fire synchronously during ongoing tactile stimulation associated with active touch.

Stimulus-Specific and Stimulus-Nonspecific Firing Synchrony and Its Modulation by Sensory Adaptation in the Whisker-to-Barrel Pathway