Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats

Abstract

1. The patterns and synchronization of low-frequency, sleeplike rhythms (slow, spindle and delta oscillations) were compared in the intact-cortex and decorticated hemispheres of cats under ketamine-xylazine anesthesia. Intracellular recordings were performed in intact and decorticated hemispheres from 58 rostrolateral thalamic reticular (RE) neurons and from 164 thalamocortical (TC) neurons in the ventrolateral (VL) nucleus. In the decorticated hemisphere, dual intracellular recordings were performed from five RE-VL cell couples and from 12 TC cell couples within the VL nucleus. In addition, field potentials were simultaneously recorded from the neocortex (electroencephalogram) and ipsilateral thalamus [electrothalamogram (EThG)] of the intact (right) hemisphere, while EThG was recorded from the VL nucleus of the decorticated (left) hemisphere. 2. The slow oscillation (< 1 Hz) was absent in all 72 VL cells and in 23 of 25 RE cells from the decorticated hemisphere, as well as in the EThG recorded from the VL nucleus in the decorticated hemisphere, whereas it was simultaneously present in the cortex and thalamus of the intact hemisphere. The remaining two RE neurons (8%) in the decorticated hemisphere oscillated in close time relation with the slow oscillation in the cortex and thalamus of the opposite hemisphere; averaged activities showed that the onset of depolarization in RE cell followed 12 ms after the sharp depth-negative (depolarizing) component in the contralateral cortex. We view this result as the electrophysiological correlate of a disynaptic excitatory pathway consisting of crossed cortical projections, first relayed in contralateral dorsal thalamic nuclei. 3. The patterns of thalamic spindles (7-14 Hz) differed between the two hemispheres. Whereas the decorticated hemisphere displayed prolonged, waxing and waning spindles, the spindles in the intact-cortex hemisphere were short and exclusively waning and followed the depth-negative component of cortical slow oscillation. This result indicates that the synchronized corticothalamic drive associated with the slow oscillation fully entrains thalamic circuits from the onset of spindles, thus preventing further waxing. Similar differences between waxing and waning and waning spindles were obtained by stimulating with different intensities the thalamus in the decorticated hemisphere. 4. Simultaneous intracellular recordings from two VL cells or from RE and VL cells showed nearly simultaneous spindle sequences in the decorticated hemisphere. 5. The hyperpolarization-activated intrinsic delta oscillation (1-4 Hz) of TC cells was asynchronous in the decorticated hemisphere. 6. These results strengthen the idea that the slow oscillation is cortical in origin; demonstrate a full, short-range, intrathalamic synchrony of spindles in the absence of cortex; and indicate that the pattern of spindles, a sleep rhythm that is conventionally regarded as purely thalamic, is shaped by the corticothalamic feedback.

Interaction between neocortical and hippocampal networks via slow oscillations

“…The DOWN state is associated with a positive polarity local field potential (LFP) in infragranular layers. Rhythmical shifts between DOWN and UP states have also been described in striatal (Wilson et al, 1990;Stern et al, 1997) and thalamic (Steriade et al, 1993b;Timofeev and Steriade, 1996;Hughes et al, 2002) neurons. Similar dynamics have been described in vitro in the presence of near normal Ca 2+ /high K + /low Mg 2+ , either spontaneously or in response to electrical stimulation of the cortex (Shu et al, 2003;Steriade et al, 1993b;Sanchez-Vives and McCormick, 2000), and during application of either mGluR agonists or muscarinic agonists (Beierlein et al, 2000).…”

“…Although the thalamic circuit is sufficient to generate spindles (Morison and Bassett, 1945;Deschenes et al, 1984;Timofeev and Steriade, 1996), in the intact brain the cortico-thalamic feedback has an important coordinating role. The thalamus is organized locally and does not have the means to produce global synchrony (McCormick and Bal, 1997).…”

Thalamocortical synchronization during induction and emergence from propofol-induced unconsciousness

“…The role of the thalamus in generating slow and δ oscillations observed during nonrapid eye movement sleep and some states of anesthesiainduced altered consciousness has been a topic of much debate (21). Recordings in deafferented cortex show that slow oscillations can occur in the absence of thalamic connections (22). Yet basic functional anatomic and neurophysiological reasoning suggests that the thalamus is likely a significant participant in slow and δ oscillations (23,24).…”

“…Electroencephalogram (EEG) recordings in humans during gradual induction of unconsciousness with propofol show the appearance of frontal β oscillations (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) at the onset of sedation, followed by the appearance of coherent frontal α (8-12 Hz) oscillations (7)(8)(9)(10) and widespread slow (0.1-1 Hz) and δ (1-4 Hz) oscillations (7,11,12) when subjects no longer respond to sensory stimuli. Biophysical models of neuronal dynamics have shown that whereas α and β oscillations can be generated by propofol's actions in cortex alone (13), coherent α oscillations require the participation of both thalamus and cortex (14).…”

Cortical locations of maximal spindle activity: magnetoencephalography (MEG) study

“…Thus, both the cortex and thalamus are important for the generation of spindles as demonstrated by studies of thalamectomy and experiments using decorticate cats (Amzica and Steriade, 1995;Timofeev and Steriade, 1996). It was shown that the slow oscillation is reflected in the thalamus by thalamic reticular and thalamocortical cells that produce sleep spindles (Amzica and Steriade, 1995).…”