Functional implications of burst firing and single spike activity in lateral geniculate relay neurons

Abstract

Guinea-pig thalamocortical relay neurons can intrinsically generate action potentials in two distinct patterns: as high frequency bursts or as relatively independent single spikes. The burst firing mode is due to the presence of a low threshold Ca2+ current and imposes a marked non-linear transformation on depolarizing or hyperpolarizing inputs. In the burst firing mode, thalamic neurons respond to increasing frequencies of depolarizing inputs with progressively fewer action potentials such that they fail to respond to inputs arriving at rates greater than approximately 15 Hz. In this manner, the amplitude of the burst discharge relays little information concerning the characteristics of phasic excitatory postsynaptic potentials which may trigger them, but rather is determined by the membrane potential preceding the burst and the time interval since the last burst. In contrast to the behavior of neurons in the burst firing mode, the pattern of action potentials generated after depolarization into the single spike mode is a more faithful representation of the characteristics of incoming excitatory postsynaptic potentials or depolarizing inputs. The pattern of action potentials generated in the single spike mode is determined by the intensity, duration, and frequency of incoming excitatory inputs even when they arrive at rates in excess of 100 Hz. These, and other properties, allow thalamic neurons to possess two distinct states of neuronal activity: an oscillatory mode in which rhythmic bursts of action potentials are generated and in which responsiveness to stimulation of peripheral receptive fields is greatly reduced, and a transfer mode in which action potentials are generated in relative independence of one another and in which the ability to respond to barrages of phasic excitatory inputs is greatly enhanced. The presence of the rhythmic burst firing mode may therefore facilitate the filtering of sensory information during periods of drowsiness, inattentiveness, and slow wave sleep.