Physiological characteristics of anterior thalamic nuclei, a group devoid of inputs from reticular thalamic nucleus

D. Pare, M. Steriade, M. Deschenes and G. Oakson This study tested the hypothesis that neurons of thalamic nuclei, which are normally devoid of inputs from the reticular thalamic nucleus, do not display spindle oscillations and related rhythmic spike bursts. This proposal derived from our recent studies indicating that the reticular nucleus is the generator of spindling rhythmicity. We used retrograde tracing methods, intracellular recordings in barbiturized cats, and extracellular recordings of single neurons and field potentials in anteroventral (AV), anteromedial (AM), ventroanterior (VA), ventrolateral (VL), and central lateral (CL) thalamic nuclei in cats with rostral brain stem transections (cerveau isole preparations), before and after administration of barbiturates. The observation that AV and AM nuclei do not receive inputs from the reticular nucleus was confirmed by using injections of horseradish peroxidase conjugated to wheat germ agglutinin confined within the limits of anterior nuclei. Such injections led to massive retrograde labeling in mammillary nuclei and layer VI of the retrosplenial cortex but left free of labeling the neurons of the reticular thalamic nucleus. Intracellular recordings showed that AV-AM neurons discharge tonically in response to a depolarizing current applied at rest, whereas they give rise to a slow spike that underlies a burst of fast action potentials when the membrane is hyperpolarized by 5-12 mV. Despite the fact that they share similar properties with other thalamic neurons, intracellularly recorded AV-AM neurons do not exhibit spindle waves under barbiturate anesthesia, whereas VA-VL, CL, and other thalamocortical neurons that receive afferents from the reticular nucleus commonly display such oscillations. With extracellular recordings performed simultaneously in CL and AV or AM nuclei of the unanesthetized cerveau isole preparation, focal spindle oscillations and related rhythmic high-frequency spike bursts of single CL cells contrasted with absence of spindles and spike bursts in AV or AM neurons. Spindling could be induced in AV-AM nuclei only after administration of barbiturates at doses exceeding 3 mg/kg, and it appeared approximately 35-40 s after the barbiturate effect was detected in the simultaneously recorded CL nucleus. Moreover, the spike bursts that were elicited in AV-AM neurons after barbiturate administration were not temporally related with focal spindles. Since spindle oscillations did not appe