Burst firing mediated by a low-threshold spike (LTS) is the hallmark of many thalamic neurons. However, postburst afterhyperpolarizations (AHPs) are relatively uncommon in thalamus. We now report data from patch-clamp recordings in rat brain slice preparations that reveal an LTS-induced slow AHP (sAHP) in thalamic paraventricular (PVT) and other midline neurons, but not in ventrobasal or reticular thalamic neurons. The LTS-induced sAHP lasts 8.9 ± 0.4 s and has a novel pharmacology, with resistance to tetrodotoxin and cadmium and reduction by Ni2+ or nominally zero extracellular calcium concentration, which also attenuate both the LTS and sAHP. The sAHP is inhibited by 10 mM intracellular EGTA or by equimolar replacement of extracellular Ca2+ with Sr2+, consistent with select activation of LVA T-type Ca2+ channels and subsequent Ca2+ influx. In control media, the sAHP reverses near EK+, shifting to −78 mV in 10.1 mM [K+]o and is reduced by Ba2+ or tetraethylammonium. Although these data are consistent with opening of Ca2+-activated K+ channels, this sAHP lacks sensitivity to specific Ca2+-activated K+ channel blockers apamin, iberiotoxin, charybdotoxin, and UCL-2077. The LTS-induced sAHP is suppressed by a β-adrenoceptor agonist isoproterenol, a serotonin 5-HT7 receptor agonist 5-CT, a neuropeptide orexin-A, and by stimulation of the cAMP/protein kinase A pathway with 8-Br-cAMP and forskolin. The data suggest that PVT and certain midline thalamic neurons possess an LTS-induced sAHP that is pharmacologically distinct and may be important for information transfer in thalamic–limbic circuitry during states of attentiveness and motivation.
