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Phasic Activation of Lateral Geniculate and Perigeniculate Thalamic Neurons During Sleep with Ponto-Geniculo-Occipital Waves

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Phasic Activation of Lateral Geniculate and Perigeniculate Thalamic Neurons During Sleep with Ponto-Geniculo-Occipital Waves The Journal of Neuroscience, July 1989, g(7): 2215-2229 Phasic Activation of Lateral Geniculate and Perigeniculate Thalamic Neurons During Sleep with Ponto-Geniculo-Occipital Waves M. Steriade, D. Pare, D. Bouhassira, M. DeschQnes, and G. Oakson Laboratoire de Neurophysiologie, Facultk de Mkdecine, Universitb Laval, Qukbec, Canada GlK 7P4 Ponto-geniculo-occipital (PGO) waves are spiky field poten- The ponto-geniculo-occipital (PGO) waves are a cardinal sign tials generated in cholinergic nuclei of the dorsolateral of the rapid-eye-movement (REM) sleep. A series of experi- mesopontine tegmentum just prior to and during rapid-eye- mental evidence, including stimulation, lesions, reversible cool- movement (REM) sleep and transferred toward thalamic nu- ing, and recordings of cellular activities, have established that clei. These events are commonly regarded as physiological PGO waves are generated in the rostra1 pons and are transferred correlates of oneiric behavior. We have examined the PGO- to the thalamus by neurons located in and around the peribra- related discharges of physiologically identified neurons lo- chial (PB) area of the pedunculopontine nucleus (for recent re- cated in the dorsal lateral geniculate (LG) nucleus and peri- views, see Sakai, 1985; Hobson and Steriade, 1986; Callaway geniculate (PG) sector of the reticular thalamic complex in et al., 1987). Immunohistochemical studies have revealed that chronically implanted, naturally sleeping cats. PGO focal a large proportion of PB cells are cholinergic (Jones and Beaudet, waves and associated unit discharges were simultaneously 1987; Vincent and Reiner, 1987), and retrograde tracing studies recorded by the same microelectrode. PGO waves herald combined with choline acetyltransferase (ChAT) immunohis- the other signs of REM sleep (EEG desynchronization and tochemistry have demonstrated the existence of a cholinergic musdular atonia), appearing 30-90 set before REM sleep projection from the brain-stem PB area to the lateral geniculate over the EEG-synchronized activity of slow-wave sleep (pre- (LG) and perigeniculate (PG) thalamic nuclei of cat (DeLima REM epoch). (1) Most PG neurons discharged bursts of ac- and Singer, 1987; Smith et al., 1988). These investigations have tion potentials in relation to PGO waves during both pre-REM also established that, quantitatively, the cholinergic projection and REM sleep. (2) The PGO-related activity of LG neurons is by far the most important ascending system of the brain-stem was quite different. During the pre-REM stage, PGO waves core. correlated with a short (7-15 msec), high-frequency (300- PGO waves are commonly regarded as the physiological cor- 500 Hz) spike burst of LG neurons, followed by a long (0.2- relate of dreaming during REM sleep. In animals, PGO waves 0.4 set) train of single spikes, whereas during REM sleep, recorded from the LG nucleus are lateralized according to the the PGO-related activity lacked the initial burst and con- direction of eye movements (Nelson et al., 1983). This char- sisted of a spike train that only slightly exceeded the toni- acteristic is shared by human parieto-occipital potentials re- cally increased background firing of LG cells. The stereo- corded during REM sleep (McCarley et al., 1983b). The re- typed characteristics of the PGO-related spike bursts during lation between eye movement direction and gaze direction in the pre-REM epoch suggest that they are the extracellular dream imagery has been reported by Dement and Kleitman reflection of a low-threshold spike deinactivated by the tonic (1957) and was recently confirmed with statistical methods membrane hyperpolarization of LG cells associated with the (Herman et al., 1984). EEG-synchronized sleep state. Such bursts are inactivated Despite the importance of PGO waves as probable indicators during the tonic depolarization of LG cells that occurs in of internally generated brain activation processes during dream REM sleep. The synchronous spike bursts discharged by LG mentation, little is known about the neuronal events that are cells in relation with the PGO waves of the pre-REM epoch associated with these spiky field potentials in the thalamus and probably underlie the much larger amplitude of the PGO cerebral cortex during natural sleep. Bizzi (1966) reported that waves of the pre-REM epoch as compared with those of the most LG neurons discharge spike trains of about 100 msec REM-sleep state. Since LG neurons have relatively low spon- beginning at the peak of the PGO focal wave, whereas 12% of taneous firing rates during the EEG-synchronized pre-REM LG cells exhibit a transitory arrest of firing during PGO waves. epoch, the PGO-related activity of this transitional stage leads Similarly, Sakakura (1968) observed that the increased firing of to a higher signal-to-noise ratio in the visual thalamocortical LG relay cells occurs in association with the slow deflection that channel than during REM sleep. We suggest that the PGO- follows the peak of PGO field potentials. related activity during the pre-REM epoch is related to vivid The results of those early investigations left open a series of imagery during this stage of sleep. fundamental issues. (1) First, it is known that PGO waves herald REM sleep by about 0.5-1.5 min. They appear during the state of sleep with Received Aug. 22, 1988; revised Dec. 5, 1988; accepted Dec. 6, 1988. EEG synchronization well before the EEG desynchronization This work was supported by the Medical Research Council of Canada. D.P. is that accompanies the fully developed REM sleep (Fig. 1). In an MRC fellow. D.B. was a visiting investigator from INSERM (Paris). We thank what follows, we will use the term pre-REM when referring to P. Gig&e and D. Drolet for technical assistance. this period of slow-wave sleep with PGO waves. Intracellular Copyright 0 1989 Society for Neuroscience 0270-6474/89/072215-15$02.00/O recordings in chronically implanted animals have shown that 2216 Steriade et al. l PGO Waves in Geniculate Thalamic Complex EEG EMG .. EMG Figure 1. Electrographic criteria of sleep states. I-3, Contiguous epochs. The 4 ink-written traces represent elec- trical activity of the LG nucleus re- corded by a coaxial electrode, ocular movements (EOG), EEG waves from the surface of the anterior suprasylvian gyrus, and electromyographic activity (EMG). Arrow in I indicates start of the pre-REM epoch, beginning with the first EEG PGO wave. First arrow in 2 points to EEG desynchronization, while second arrow indicates complete muscular atonia during REM sleep. EMG 5s LG neurons are hyperpolarized during EEG-synchronized sleep, of recurrent inhibition acting upon LG thalamocortical cells. It whereas they are tonically depolarized during REM sleep with has recently been shown that the effects of brain-stem reticular EEG desynchronization (Hirsch et al., 1983). The EEG-syn- stimulation and ACh application are strikingly different upon chronized and EEG-desynchronized behavioral states are as- LG and PG or RE neurons. In particular, ACh induces a se- sociated with opposite modes of background discharges and quence of depolarizing responses in most LG neurons of cat cellular responsiveness in thalamic neurons (Steriade and studied in vitro (McCormick and Prince, 1987a, b), whereas the Deschenes, 1984). In particular, waking and REM sleep are response of RE cells to ACh is a powerful hyperpolarization accompanied by stabilized membrane potential and tonic firing, with increased K conductance (McCormick and Prince, 1986, whereas EEG-synchronized sleep is associated with long-lasting 1987b). Since ACh is involved in the thalamic response to the hyperpolarizations and high-frequency bursts related to spindle PGO volley (see above), the question arises as to the possibly oscillations. The basis of sleep bursts is a low-threshold Ca spike differential effects exerted by the brain-stem executive elements (LTS) deinactivated by membrane hyperpolarization that gives on LG and PG neurons. rise to high-frequency Na action potentials (see Steriade and In this paper, we attempt to answer these questions by re- Llinbs, 1988). What are the LG-cell responses to the brain stem- cording the PGO-related activities of physiologically identified generated PGO volley during 2 behavioral states (EEG-syn- LG and PG neurons in naturally sleeping cats. chronized pre-REM stage and EEG-desynchronized REM sleep) associated with different levels of resting membrane potential Materials and Methods in thalamic neurons? Preparation, stimulation, and recording. Adult catswere used. The chronic implantation was performed under sodium pentobarbital anesthesia (35 (2) Second, what is the ratio between the PGO signal and the mg/kg). During recording sessions, the head was rigidly held in a ster- background discharge in the visual channel during the pre-REM eotaxic position without pain or pressure (Steriade and Glenn, 1982). period of PEG-synchronized sleep and during REM sleep? This Recording leads consisted of monopolar electrodes over the surface of question may give clues as to the vivid imagery during these 2 the anterior suprasylvian cortex to record EEG rhythms, silver ball epochs of the sleep cycle. electrodes for ocular movements (EOG), and electrodes for neck muscle potentials (EMG). Bipolar stimulating electrodes were inserted into the (3) At the time of earlier investigations on LG unitary activ- optic chiasm (OX). A coaxial recording electrode was implanted in the ities related to PGO waves, it was not known that the PG sector LG nucleus, contralaterally to the LG-PG complex explored by mi- of the reticular thalamic (RE) nuclear complex is the main source croelectrodes. The positions of OX stimulating and LG recording elec- The Journal of Neuroscience, July 1989, 9(7) 2217 2ms ’ I 2ms Number C of cells :::::::::i:::: lo- :::::::::::::: /j//j/j/j/j/j/ ::::::i::::::: l-l 0 _..iiix:::::::: LG PG Figure 2. Physiological identification of LG and PG neurons. A and B. TVD- ical OX-evoked responses in LG and PG neurons, respectively.
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