Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems

M. Steriade, Subimal Datta, D. Paré, G. Oakson, R. Curró Dossi

Research output: Contribution to journalArticle

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Abstract

This study was performed to examine the hypothesis that thalamic-projecting neurons of mesopontine cholinergic nuclei display activity patterns that are compatible with their role in inducing and maintaining activation processes in thalamocortical systems during the states of waking (W) and rapid-eye-movement (REM) sleep associated with desynchronization of the electroencephalogram (EEG). A sample of 780 neurons located in the peribrachial (PB) area of the pedunculopontine tegmental nucleus and in the laterodorsal tegmental (LDT) nucleus were recorded extracellularly in unanesthetized, chronically implanted cats. Of those neurons, 82 were antidromically invaded from medial, intralaminar, and lateral thalamic nuclei; 570 were orthodromically driven at short latencies from various thalamic sites; and 45 of the latter elements are also part of the 82 cell group, as they were activated both antidromically and synaptically from the thalamus. There were no statistically significant differences between firing rates in the PB and LDT neuronal samples. Rate analyses in 2 distinct groups of PB/LDT neurons, with fast (> 10 Hz) and slow (<2 Hz) discharge rates in W, indicated that (1) the fast-discharging cell group had higher firing rates in W and REM sleep compared to EEG-synchronized sleep (S), the differences between all states being significant (p < 0.0005); (2) the slow-discharging cell group increased firing rates from W to S and further to REM sleep, with significant difference between W and S (p < 0.01), as well as between W or S and REM sleep (p < 0.0005). Interspike interval histograms of PB and LDT neurons showed that 75% of them have tonic firing patterns, with virtually no high-frequency spike bursts in any state of the wake-sleep cycle. We found 22 PB cells that discharged rhythmic spike trains with recurring periods of 0.8-1 sec. Autocorrelograms revealed that this oscillatory behavior disappeared when their firing rate increased during REM sleep. Dynamic analyses of sequential firing rates throughout the waking-sleep cycle showed that none of the full-blown states of vigilance is associated with a uniform level of spontaneous firing rate. Signs of decreased discharge frequencies of mesopontine neurons appeared toward the end of quiet W, preceding by about 10-20 sec the most precocious signs of EEG synchronization heralding the sleep onset. During transition from S to W, rates of spontaneous discharges increased 20 sec before the onset of EEG desynchronization. Similarly, a group analysis of PB/LDT cells showed precursor changes of increased discharge rates during transition from S to REM sleep, 1 min in advance of EEG desynchronization (p < 0.05). The enhanced level of spontaneous discharge during W and REM sleep was paralleled by an increase in neuronal excitability. Indeed, the probability of antidromic responses increased by 30-80% during REM sleep, and the probability of synaptically evoked discharges increased by 40-85% from S to either W or REM sleep. We conclude that neurons in thalamic-projecting mesopontine cholinergic nuclei are good candidates for preparing and maintaining the tonic activation processes in thalamocortical systems during W and REM sleep associated with EEG desynchronization. In our view, this action is accomplished by direct depolarization of thalamocortical neurons and by the inhibition of the thalamic generator of synchronized spindle oscillations.

Original languageEnglish (US)
Pages (from-to)2541-2559
Number of pages19
JournalJournal of Neuroscience
Volume10
Issue number8
StatePublished - Dec 1 1990
Externally publishedYes

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Cholinergic Agents
Brain Stem
Sleep
REM Sleep
Electroencephalography
Neurons
Pedunculopontine Tegmental Nucleus
Intralaminar Thalamic Nuclei
Lateral Thalamic Nuclei
Mediodorsal Thalamic Nucleus
Cholinergic Neurons
Thalamus
Cats

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. / Steriade, M.; Datta, Subimal; Paré, D.; Oakson, G.; Curró Dossi, R.

In: Journal of Neuroscience, Vol. 10, No. 8, 01.12.1990, p. 2541-2559.

Research output: Contribution to journalArticle

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abstract = "This study was performed to examine the hypothesis that thalamic-projecting neurons of mesopontine cholinergic nuclei display activity patterns that are compatible with their role in inducing and maintaining activation processes in thalamocortical systems during the states of waking (W) and rapid-eye-movement (REM) sleep associated with desynchronization of the electroencephalogram (EEG). A sample of 780 neurons located in the peribrachial (PB) area of the pedunculopontine tegmental nucleus and in the laterodorsal tegmental (LDT) nucleus were recorded extracellularly in unanesthetized, chronically implanted cats. Of those neurons, 82 were antidromically invaded from medial, intralaminar, and lateral thalamic nuclei; 570 were orthodromically driven at short latencies from various thalamic sites; and 45 of the latter elements are also part of the 82 cell group, as they were activated both antidromically and synaptically from the thalamus. There were no statistically significant differences between firing rates in the PB and LDT neuronal samples. Rate analyses in 2 distinct groups of PB/LDT neurons, with fast (> 10 Hz) and slow (<2 Hz) discharge rates in W, indicated that (1) the fast-discharging cell group had higher firing rates in W and REM sleep compared to EEG-synchronized sleep (S), the differences between all states being significant (p < 0.0005); (2) the slow-discharging cell group increased firing rates from W to S and further to REM sleep, with significant difference between W and S (p < 0.01), as well as between W or S and REM sleep (p < 0.0005). Interspike interval histograms of PB and LDT neurons showed that 75{\%} of them have tonic firing patterns, with virtually no high-frequency spike bursts in any state of the wake-sleep cycle. We found 22 PB cells that discharged rhythmic spike trains with recurring periods of 0.8-1 sec. Autocorrelograms revealed that this oscillatory behavior disappeared when their firing rate increased during REM sleep. Dynamic analyses of sequential firing rates throughout the waking-sleep cycle showed that none of the full-blown states of vigilance is associated with a uniform level of spontaneous firing rate. Signs of decreased discharge frequencies of mesopontine neurons appeared toward the end of quiet W, preceding by about 10-20 sec the most precocious signs of EEG synchronization heralding the sleep onset. During transition from S to W, rates of spontaneous discharges increased 20 sec before the onset of EEG desynchronization. Similarly, a group analysis of PB/LDT cells showed precursor changes of increased discharge rates during transition from S to REM sleep, 1 min in advance of EEG desynchronization (p < 0.05). The enhanced level of spontaneous discharge during W and REM sleep was paralleled by an increase in neuronal excitability. Indeed, the probability of antidromic responses increased by 30-80{\%} during REM sleep, and the probability of synaptically evoked discharges increased by 40-85{\%} from S to either W or REM sleep. We conclude that neurons in thalamic-projecting mesopontine cholinergic nuclei are good candidates for preparing and maintaining the tonic activation processes in thalamocortical systems during W and REM sleep associated with EEG desynchronization. In our view, this action is accomplished by direct depolarization of thalamocortical neurons and by the inhibition of the thalamic generator of synchronized spindle oscillations.",
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T1 - Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems

AU - Steriade, M.

AU - Datta, Subimal

AU - Paré, D.

AU - Oakson, G.

AU - Curró Dossi, R.

PY - 1990/12/1

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N2 - This study was performed to examine the hypothesis that thalamic-projecting neurons of mesopontine cholinergic nuclei display activity patterns that are compatible with their role in inducing and maintaining activation processes in thalamocortical systems during the states of waking (W) and rapid-eye-movement (REM) sleep associated with desynchronization of the electroencephalogram (EEG). A sample of 780 neurons located in the peribrachial (PB) area of the pedunculopontine tegmental nucleus and in the laterodorsal tegmental (LDT) nucleus were recorded extracellularly in unanesthetized, chronically implanted cats. Of those neurons, 82 were antidromically invaded from medial, intralaminar, and lateral thalamic nuclei; 570 were orthodromically driven at short latencies from various thalamic sites; and 45 of the latter elements are also part of the 82 cell group, as they were activated both antidromically and synaptically from the thalamus. There were no statistically significant differences between firing rates in the PB and LDT neuronal samples. Rate analyses in 2 distinct groups of PB/LDT neurons, with fast (> 10 Hz) and slow (<2 Hz) discharge rates in W, indicated that (1) the fast-discharging cell group had higher firing rates in W and REM sleep compared to EEG-synchronized sleep (S), the differences between all states being significant (p < 0.0005); (2) the slow-discharging cell group increased firing rates from W to S and further to REM sleep, with significant difference between W and S (p < 0.01), as well as between W or S and REM sleep (p < 0.0005). Interspike interval histograms of PB and LDT neurons showed that 75% of them have tonic firing patterns, with virtually no high-frequency spike bursts in any state of the wake-sleep cycle. We found 22 PB cells that discharged rhythmic spike trains with recurring periods of 0.8-1 sec. Autocorrelograms revealed that this oscillatory behavior disappeared when their firing rate increased during REM sleep. Dynamic analyses of sequential firing rates throughout the waking-sleep cycle showed that none of the full-blown states of vigilance is associated with a uniform level of spontaneous firing rate. Signs of decreased discharge frequencies of mesopontine neurons appeared toward the end of quiet W, preceding by about 10-20 sec the most precocious signs of EEG synchronization heralding the sleep onset. During transition from S to W, rates of spontaneous discharges increased 20 sec before the onset of EEG desynchronization. Similarly, a group analysis of PB/LDT cells showed precursor changes of increased discharge rates during transition from S to REM sleep, 1 min in advance of EEG desynchronization (p < 0.05). The enhanced level of spontaneous discharge during W and REM sleep was paralleled by an increase in neuronal excitability. Indeed, the probability of antidromic responses increased by 30-80% during REM sleep, and the probability of synaptically evoked discharges increased by 40-85% from S to either W or REM sleep. We conclude that neurons in thalamic-projecting mesopontine cholinergic nuclei are good candidates for preparing and maintaining the tonic activation processes in thalamocortical systems during W and REM sleep associated with EEG desynchronization. In our view, this action is accomplished by direct depolarization of thalamocortical neurons and by the inhibition of the thalamic generator of synchronized spindle oscillations.

AB - This study was performed to examine the hypothesis that thalamic-projecting neurons of mesopontine cholinergic nuclei display activity patterns that are compatible with their role in inducing and maintaining activation processes in thalamocortical systems during the states of waking (W) and rapid-eye-movement (REM) sleep associated with desynchronization of the electroencephalogram (EEG). A sample of 780 neurons located in the peribrachial (PB) area of the pedunculopontine tegmental nucleus and in the laterodorsal tegmental (LDT) nucleus were recorded extracellularly in unanesthetized, chronically implanted cats. Of those neurons, 82 were antidromically invaded from medial, intralaminar, and lateral thalamic nuclei; 570 were orthodromically driven at short latencies from various thalamic sites; and 45 of the latter elements are also part of the 82 cell group, as they were activated both antidromically and synaptically from the thalamus. There were no statistically significant differences between firing rates in the PB and LDT neuronal samples. Rate analyses in 2 distinct groups of PB/LDT neurons, with fast (> 10 Hz) and slow (<2 Hz) discharge rates in W, indicated that (1) the fast-discharging cell group had higher firing rates in W and REM sleep compared to EEG-synchronized sleep (S), the differences between all states being significant (p < 0.0005); (2) the slow-discharging cell group increased firing rates from W to S and further to REM sleep, with significant difference between W and S (p < 0.01), as well as between W or S and REM sleep (p < 0.0005). Interspike interval histograms of PB and LDT neurons showed that 75% of them have tonic firing patterns, with virtually no high-frequency spike bursts in any state of the wake-sleep cycle. We found 22 PB cells that discharged rhythmic spike trains with recurring periods of 0.8-1 sec. Autocorrelograms revealed that this oscillatory behavior disappeared when their firing rate increased during REM sleep. Dynamic analyses of sequential firing rates throughout the waking-sleep cycle showed that none of the full-blown states of vigilance is associated with a uniform level of spontaneous firing rate. Signs of decreased discharge frequencies of mesopontine neurons appeared toward the end of quiet W, preceding by about 10-20 sec the most precocious signs of EEG synchronization heralding the sleep onset. During transition from S to W, rates of spontaneous discharges increased 20 sec before the onset of EEG desynchronization. Similarly, a group analysis of PB/LDT cells showed precursor changes of increased discharge rates during transition from S to REM sleep, 1 min in advance of EEG desynchronization (p < 0.05). The enhanced level of spontaneous discharge during W and REM sleep was paralleled by an increase in neuronal excitability. Indeed, the probability of antidromic responses increased by 30-80% during REM sleep, and the probability of synaptically evoked discharges increased by 40-85% from S to either W or REM sleep. We conclude that neurons in thalamic-projecting mesopontine cholinergic nuclei are good candidates for preparing and maintaining the tonic activation processes in thalamocortical systems during W and REM sleep associated with EEG desynchronization. In our view, this action is accomplished by direct depolarization of thalamocortical neurons and by the inhibition of the thalamic generator of synchronized spindle oscillations.

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