In vivo induction of striatal long-term potentiation by low-frequency stimulation of the cerebral cortex.

Both long-term depression and long-term potentiation have been described at corticostriatal synapses. These long-lasting changes in synaptic strength were classically induced by high-frequency (100 Hz) electrical stimulations of cortical afferents. The purpose of the present study was to test the ability of corticostriatal connections to express use-dependent modifications after cortical stimulation applied at the frequency of synchronization of corticostriatal inputs observed in our in vivo preparation, i.e. the barbiturate-anesthetized rat. For this study we used an identified monosynaptic corticostriatal pathway, between the orofacial motor cortex and its target region in the striatum. Intracellular recording of striatal output neurons showed spontaneous large-amplitude oscillation-like depolarizations exhibiting a strong periodicity with a narrow frequency band at 5 Hz. Using the focal electroencephalogram of the cortical region projecting to the recorded cells, we found that membrane potential oscillations in striatal neurons were in phase with episodes of spontaneous cortical spindle waves. To determine directly the pattern of activity of corticostriatal neurons, we performed intracellular recordings of electrophysiologically identified corticostriatal neurons simultaneously with the corresponding surface electroencephalogram. We found that corticostriatal cells (n = 7) exhibited periods of spontaneous 5-Hz discharges in phase with the cortical spindle waves. Therefore, we have tested the effect of repetitive cortical stimulations at this low frequency (5 Hz, 500-1000 pulses) on the corticostriatal synaptic efficacy. In 62% of cases (eight of 13 neurons tested), this conditioning was able to produce long-term potentiation in the corticostriatal synaptic efficacy. The mean increase of excitatory postsynaptic potential amplitude ranged from 13.3% to 172% (mean = 67.3%, n = 8). These results provide additional support for physiological long-term potentiation at corticostriatal connections. Furthermore, this study demonstrates that corticostriatal long-term potentiation can be induced by synchronization at low frequency of cortical afferents. Our data support the concept that the striatal output neuron may operate as a coincidence detector of converging cortical information.