Increased transneuronal excitation of the cat lateral geniculate nucleus after acute deafferentation

Single neurons and sum potentials were recorded from the cat optic tract (OT), the lateral geniculate nucleus (LGN) and the optic radiation (OR) before and after visual deafferentation obtained by locally restricted photocoagulation of the retina or by 'total' photocoagulation of the optic disc of 'monocular' cats. Immediately after deafferentation, the spontaneous activity of single LGN-neurons fell to a very low level (is much less than 0.1 impulses/sec). This nearly total depression of neuronal activity was followed by a slow but incomplete recovery of the spontaneous impulse rate which reached about 1-2 impulses/sec, 2-4 days after deafferentation. The 'normal' LGN neuron impulse rate was about 8-30 impulses/sec. After deafferentation the impulse pattern showed an increased occurrence of double discharges separated by very long intermittent intervals. The excitability of LGN principal cells activated by OT electrical stimuli increased immediately after deafferentation. Double and multiple discharges were then elicited by single optic tract stimuli. The deafferentation hyperexcitability was abolished temporarily by OT stimulus trains with a frequency range > 10 stimuli/sec, and returned to the prestimulus level within 0.5-1sec after the stimulus train was terminated. Antidromic conditioning stimuli did not influence the deafferentation hyperexcitability. The time course of the postdeafferentation hyperexcitability was separated into two parts: an immediate rise in excitability after deafferentation was followed by a further slow increase in excitability within the first 2 h after deafferentation. The hyperexcitability measurable at a single unit level was already maximal after locally restricted deafferentation and did not increase with the extension of the retinal lesion beyond 1-2 mm diameter, corresponding to 4-8 degrees in the visual field. Intracellular recordings after deafferentation displayed no significant increase in the amplitude of subthreshold EPSPs, but additional slow, aperiodic, depolarizing waves were found to modify the resting membrane potential. From the multiple discharge pattern elicited by single OT electrical stimuli, one can conjecture that the suprathreshold EPSPs, however, increased considerably in their amplitude. The evoked potentials (OR-waves r1, r2) elicited by electrical OT stimuli increased in amplitude and the small waves r3-r6 became more prominent after deafferentation. All postsynaptic r-waves reached their maximum values about 1.5 h after interruption of the optic nerve signal flow and did not change further within the following 28 h.