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

D. Pare, M. Steriade, M. Deschenes, G. Oakson

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21 Scopus citations


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 ~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 appear intracellularly in AV-AM neurons, the possibility was envisaged that barbiturate-induced spindles were the passive reflection of field potentials actively generated in neighboring thalamic nuclei. We lesioned the AV-AM nuclei with a local H2O2 microinjection and we monitored, before and after injection, both the field potential evoked synaptically by stimulating the mammillary nuclei and the spindle oscillations precipitated by a short-acting barbiturate. The synaptic response was completely obliterated after H2O2 injection, whereas spindling persisted in AV-AM nuclei with the same characteristics as before the injection. These data support the assumption that the extracellular spindles were due to field effects. We conclude that the synaptic connections from the reticular thalamic nucleus are indispensable for the occurrence of spindling in thalamocortical systems. The role of synaptic networks specialized in the genesis of different rhythms is emphasized by the variety observed among the rhythmicity generated by different networks despite great similarities in the intrinsic properties of their constituent elements. The AV-AM thalamic neurons have intrinsic properties similar to other thalamocortical cells. At variance with other thalamic neurons, however, AV-AM cells do not exhibit spindle oscillations because they are not interposed within circuits involving the reticular thalamic nucleus, the pacemaker of spindle rhythmicity.

Original languageEnglish (US)
Pages (from-to)1669-1685
Number of pages17
JournalJournal of neurophysiology
Issue number6
StatePublished - 1987
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology


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