A role for low-frequency, rhythmic synaptic potentials in the synchronization of cat thalamocortical cells

1. Low-frequency, rhythmic synaptic potentials and their ability to evoke and modulate membrane potential oscillations in thalamocortical (TC) cells of the cat dorsal lateral geniculate nucleus (dLGN) were investigated using intracellular recordings in a brain slice preparation. Three types of rhythmic synaptic potentials were distinguished: EPSPs, IPSPs and 'complex synaptic potentials' consisting of an IPSP followed by an EPSP. 2. The frequency of all three types of synaptic potentials was insensitive to changes in the membrane potential. At potentials positive to -50 mV, the EPSPs and the complex potentials gave rise to action potentials, while between -65 and -80 mV all three types of synaptic potential evoked low-threshold Ca2+ potentials. TC cells which displayed rhythmic synaptic potentials were either cells that showed spontaneous pacemaker oscillation or cells that were brought to oscillate by the rhythmic EPSPs or depolarizing (i.e. reversed IPSPs. 3. The low-frequency (1.9 +/- 0.2 Hz), rhythmic EPSPs were observed in 23 (out of 192) cells, were abolished by tetrodotoxin (TTX; n = 4) and by the combined application of DL-2-amino-5-phosphonovaleric acid and 6-cyano-7-nitroquinoxaline-2,3-dione (n = 3), and were insensitive to bicuculline (n = 4). Paired intracellular recordings (n = 32) demonstrated the presence of simultaneously occurring EPSPs in a pair of cells situated 75 microns apart. 4. The low-frequency (2.2 +/- 0.3 Hz), rhythmic IPSPs were observed in 5 (out of 192) cells, were blocked by bicuculline (n = 3), and reversed in polarity at -65 mV. The low-frequency (1.3 +/- 0.3 Hz), rhythmic 'complex potentials' were observed in 5 (out of 192) cells and were abolished by TTX (n = 2). 5. Intracellular depolarizing current pulses delivered at different phases of the pacemaker oscillations revealed the existence of two different types of phase resetting. Furthermore, a current pulse of critical amplitude and duration applied at a specific phase of the cycle abolished the pacemaker oscillations. 6. These results indicate that the low-frequency, rhythmic synaptic potentials recorded in TC cells of the dLGN (i) originate from other TC cells that are in the pacemaker oscillating mode, (ii) are capable of driving other TC cells to oscillate rhythmically, or of modulating the frequency of pacemaker oscillations, and (iii) provide a means by which oscillatory activities of TC cells can be synchronized in the absence of sensory, cortical and reticular thalamic inputs.