Intracellular and extracellular in vivo recording of different response modes for relay cells of the cat's lateral geniculate nucleus

Prior studies of thalamic neurons have demonstrated that they exhibit at least two response modes: a relay mode and a burst mode. During the relay mode, sensory information is faithfully relayed to cortex; during the burst mode, which is caused by a voltagedependent Ca2+ conductance, this relay of sensory information is interrupted. We began in vivo studies of these response modes in neurons from the lateral geniculate nucleus of anesthetized, paralyzed cats. Each of the 9 X and 10 Y cells we recorded intracellularly displayed voltage-dependent, low threshold spikes that were presumably the Ca2+ spikes described from in vitro recording. These spikes were triangular in waveform and typically had 2–7 fast action potentials (interspike intervals of 1.2–4 ms) riding its crest. Furthermore, the cell's membrane had to be hyperpolarized to de-inactivate the low threshold spike before a depolarization could then activate it. We could activate these low threshold spikes in Y cells from EPSPs, whether spontaneous or evoked from activation of the optic chiasm. However, in only one of the X cells could we activate low threshold spikes from chiasm shock; in the remainder, we could activate low threshold spikes only via depolarizing current pulses, possibly because the EPSPs of these X cells were too small to activate these spikes. We also used extracellular recording to study spontaneous activity and responses to chiasm shock from 114 geniculate neurons and, as a control, 57 optic tract axons. We concentrated on periods of bursty responsiveness signifying the burst mode. We define a burst as 2–7 action potentials with interspike intervals 100 ms; from our intracellular recording, we know that such bursts signify low threshold spikes. We found that, during extracellular recording, 20 of the 39 X cells and each of the 75 Y cells displayed evidence of the burst response mode, although burst periods were rare in X cells. Electrical activation of the optic chiasm greatly enhanced the burstiness of Y cells for periods of 500 ms or more. We also electrically stimulated the parabrachial region of the midbrain, which provides a mostly cholinergic innervation to the lateral geniculate nucleus. Although parabrachial activation by itself had no detectable effect on Y cell response modes, prior parabrachial activation prevented the enhanced burstiness caused by chiasm stimulation. This parabrachial effect lasted for roughly 500 ms after stimulation. Neither chiasm nor parabrachial stimulation, singly or in combination, had a noticeable effect on the bursting activity of X cells. Finally, none of the extracellularly recorded retinogeniculate axons (23 X and 34 Y) showed any evidence of burst responses. This supports the conclusion that the burst responses we found for geniculate neurons represent an emergent property of the lateral geniculate nucleus, and this burstiness reflects an interruption of retinogeniculate transmission. We conclude that geniculate X and Y cells do indeed show evidence during extracellular recording of maintaining two very different response modes and that, under our recording conditions, Y cells are much more prone to burst activity than are X cells.