Spatiotemporal Patterns of Spindle Oscillations in Cortex and Thalamus

TLDR

Spindle oscillations (7‑14 Hz) arise in thalamus and cortex during early sleep, driven by intrinsic neuronal properties, connectivity, and corticothalamic feedback that generate coherent spatiotemporal maps across widespread thalamic territories. The study investigates how spontaneous and evoked spindle oscillations are organized across cortex and thalamus, proposing that continuous corticothalamic input and divergent connectivity drive their coherence. Multisite field potential and unit recordings were performed in intact and decorticated animals to map spindle patterns. Spindle oscillations are synchronized over large cortical areas during natural sleep and barbiturate anesthesia; cortical coherence persists despite intracortical transection; in intact cortex, spontaneous spindles span widespread thalamic territories; without cortex, thalamic spindles are less organized but maintain local coherence; and low‑intensity cortical stimulation can trigger spindle propagation at 1–3 mm/s, with higher intensity inducing simultaneous onset across leads.

Abstract

Spindle oscillations (7-14 Hz) appear in the thalamus and cortex during early stages of sleep. They are generated by the combination of intrinsic properties and connectivity patterns of thalamic neurons and distributed to cortical territories by thalamocortical axons. The corticothalamic feedback is a major factor in producing coherent spatiotemporal maps of spindle oscillations in widespread thalamic territories. Here we have investigated the spatiotemporal patterns of spontaneously occurring and evoked spindles by means of multisite field potential and unit recordings in intact cortex and decorticated animals. We show that (1) spontaneous spindle oscillations are synchronized over large cortical areas during natural sleep and barbiturate anesthesia; (2) under barbiturate anesthesia, the cortical coherence is not disrupted by transection of intracortical synaptic linkages; (3) in intact cortex animals, spontaneously occurring barbiturate spindle sequences occur nearly simultaneously over widespread thalamic territories; (4) in the absence of cortex, the spontaneous spindle oscillations throughout the thalamus are less organized, but the local coherence (within 2-4 mm) is still maintained; and (5) spindling propagation is observed in intact cortex animals only when elicited by low intensity cortical stimulation, applied shortly before the initiation of a spontaneous spindle sequence; propagation velocities are between 1 and 3 mm/sec, measured in the anteroposterior axis of the thalamus; increasing the intensity of cortical stimulation triggers spindle oscillations, which start simultaneously in all leads. We propose that, in vivo, the coherence of spontaneous spindle oscillations in corticothalamic networks is attributable to the combined action of continuous background corticothalamic input initiating spindle sequences in several thalamic sites at the same time and divergent corticothalamic and intrathalamic connectivity.