Induction of long-term potentiation leads to increased reliability of evoked neocortical spindles in vivo

Large amplitude electroencephalographic spindle waves (7-14 Hz) occur spontaneously in the neocortex during both sleep and awake immobility, and it has been proposed that synchronous neuronal activation during spindles may contribute to learning-related synaptic plasticity. Spindles can also be evoked in the sensorimotor cortex by electrical stimulation of cortical or thalamic inputs in the rat. To determine if strengthening cortical synapses can affect the initiation and maintenance of electrically evoked spindles, stimulation pulses were delivered at a range of intensities to the corpus callosum or ventrolateral thalamus in the awake rat before and after the induction of long-term potentiation (LTP) by tetanization of the corpus callosum. The morphology of evoked spindles was similar to that of naturally occurring spindles. Spindles were evoked less reliably during slow-wave sleep than during waking, and this was correlated with smaller synaptic responses during slow-wave sleep. Similar to previous findings, daily tetanization of the corpus callosum for 15 days decreased the early component and increased the late component of synaptic responses evoked by corpus callosum stimulation, but did not significantly affect synaptic responses evoked by thalamic stimulation. Similarly, LTP induction increased the reliability with which low-intensity corpus callosum stimulation evoked spindles, but increases in spindles evoked by thalamic stimulation were not significant. Synaptic potentiation and the increased reliability of spindles developed with a similar time-course over the 15-day LTP induction period. These results reflect strong correlations between the strength of cortical layer V activation and the initiation of spindles in the sensorimotor cortex, and support the idea that monosynaptic and polysynaptic horizontal collaterals of layer V neurons can play a significant role in the initiation of spindles.