Elsevier

Neuroscience

Volume 76, Issue 1, 5 December 1996, Pages 11-24
Neuroscience

Synchronization of low-frequency rhythms in corticothalamic networks

https://doi.org/10.1016/S0306-4522(96)00393-4Get rights and content

Abstract

We have investigated the degree of synchronization between cortical, thalamic reticular and thalamocortical neurons of cats during low-frequency (<15 Hz) sleep-like oscillations, as they appear under anaesthesia. We have also studied the effects exerted by cortical stimulation on the synchronization among thalamic units. Parallel experiments [Steriade et al. (1996) J. Neurosci. 16, 392–417] in this laboratory have demonstrated the similarity between the slow oscillation (<1 Hz) under ketamine-xylazine anaesthesia and that occurring during the natural state of resting sleep. Spontaneous activity was recorded simultaneously, with independent microelectrodes, from groups of two to five physiologically identified neurons. The rhythmicity of spontaneous activity and the temporal relations between cellular discharges were statistically evaluated by auto- and crosscorrelation techniques. We have found no topography in the distribution of synchronization between thalamic reticular and thalamocortical cells. Only the slow, cortical-generated oscillation (<1 Hz) displayed a stable frequency and correlation among groups of cortical and thalamic cells. The other two sleep oscillations (thalamic-generated spindles at 7–14 Hz and clock-like delta at 1–4 Hz) fluctuated in frequency and the degree of correlation between neurons varied. Cortical volleys entrained and synchronized thalamic cells, and triggered synchronized spindling in the thalamus.

These results extend for large populations of cortical and thalamic neurons the phase relations found in intracellular recordings. [Contreras and Steriade (1995) J. Neurosci. 15, 604–622; Steriade and Contreras (1995) J. Neurosci. 15, 623–642]

Section snippets

Experimental animals

Experiments were performed on 39 adult cats. Of those, 12 were anaesthetized with urethane (1.8 g/kg, i.p.) and 27 with ketamine-xylazine (10–15 mg/kg and 2–3 mg/kg, i.m.). All wounds and pressure points were infiltrated with lidocaine. Additional doses of urethane (0.2–0.5 g/kg, i.p.), ketamine-xylazine (2–3 mg/kg; 0.4–0.6 mg/kg) or nitrous oxide were used at the earliest signs of diminished amplitude and/or increased frequency of EEG waves in order to maintain a picture of deep anaesthesia

Database and neuronal identification

Results are based on simultaneous extracellular recordings from 142 groups of cells making a total of 156 cortical cells from the pericruciate region, 318 RE cells from the rostral pole, rostrolateral and lateral regions (including the peri-VL and the peri-VP sectors), and 184 TC cells from the VL and the VP nucleus. Each group of simultaneously recorded cells had one to three cortical cells, two to five RE cells, and one to three TC cells. Several groups (n=51) consisted of neurons from both

Discussion

Our data show that: (i) high-amplitude, low-frequency oscillations are associated with highly coherent activities of cortical, RE and TC neurons; (ii) under urethane and ketamine-xylazine anaesthesia, cortical and RE cells mostly display spontaneous and synchronized slow oscillations between 0.3 and 0.9 Hz, while TC cells prevalently show clock-like delta oscillations at 1–4 Hz; and (iii) cortical stimulation is effective in entraining and synchronizing RE and TC cells within the frequency of

Conclusion

The only sleep oscillation in which the rhythmicity and phase between cells is kept relatively constant is the slow oscillation. The other two, thalamic-generated sleep oscillations (spindling and clock-like delta) display continuous variations in frequency and in relations between cells, rendering less homogeneous the population samples being recorded and therefore making it necessary to record from larger populations of neurons.

Acknowledgements

This work was supported by grant MT-3689 from the Medical Research Council of Canada. D.C. is a graduate student in this laboratory, partially supported by the Savoy Foundation. We thank P. Giguère and D. Drolet for technical assistance.

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