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Repetitive synaptic potentials responsible for inhibition of spinal cord motoneurons during active sleep
EXPERIMENTAL
NEUROLOGY
78,47 l-476 (1982)
RESEARCH
NOTE
Repetitive Synaptic Potentials Responsible for Inhibition Spinal Cord Motoneurons during Active Sleep FRANCISCO R. MORALES AND MICHAEL
of
H. CHASE’
Department of Physiology, School of Medicine, University of California, Los Angeles, California 90024 Received May 19, I982 High-gain intracellular recordings of spinal cord motoneurons were obtained in the chronically prepared cat during wakefulness, quiet sleep, and active sleep. Discrete hyperpokuizing postsynaptic potentials were found to occur repetitively throughout active sleep in conjunction with the presence of somatomotor atonia. These potentials were most prominent in the transition period from quiet to active sleep as well as during episodes of rapid eye movements during active sleep. Their polarity was reversed after the intracellular injection of chloride ions. We propose that these are inhibitory potentials which are responsible for or contribute significantly to the postsynaptic inhibition of spinal cord motoneurons during active sleep.
It recently has been shown that alpha motoneurons of the spinal cord are hyperpolarized and their excitability is depressed during active sleep (AS) compared with quiet sleep (QS) or wakefulness (W) (8, 12, 13). In addition, the somadendritic invasion of antidromically induced action potentials is impaired and there is a decrease in motoneuron input resistance (8, 13). These data indicate that motoneurons are subjected to continuous inhibitory synaptic input during the atonia accompanying AS. The present report describes the putative basis for this input, which consists of discrete inhibitory postsynaptic potentials (IPSPs) that impinge on spinal cord motoneurons repetitively throughout AS. Abbreviations: AS, QS-active, quiet sleep; W-wakefulness; IPSP-inhibitory postsynaptic potential. ’ This research was supported by a grant from the National Science Foundation (BNS 7912897). 471 0014-4886/82/l
10471-06$02.00/O
Copyright 0 1982 by Academic Press, Inc. Ail rights of reproduction in any form resewed.
472
MORALES
AND
CHASE
Experiments were conducted on six chronically prepared cats that were undrugged, unanesthetized, and respiring normally. Each animal was implanted with permanent head and lumbar restraining devices and peripheral nerve stimulating electrodes. Recording electrodes for EEG, EQG, and EMG were placed to monitor the states of sleep and wakefulness. These surgical and implantation techniques have been described in detail ( 14). Single-barrel glass micropipettes with tip resistances of 8 to 10 Mn were used for intracellular recording. The microelectrodes were filled with different electrolyte solutions according to the particular experimental objective: 2 M potassium citrate (K-citrate) was used to examine the waveform of inhibitory potentials (7); 3 M potassium chloride (KCl) was utilized when the iontophoretic injection of chloride ions was undertaken to determine the inhibitory nature of the potentials (7). In the latter case, anodal currents of 5 to 10 nA (1 min duration) were delivered during W, QS, and AS. Intracellular DC records (at high amplification-200X) were stored on magnetic tape (high frequency cutoff at 5 kHz) after eliminating, with an automatic offset circuit, the large DC shift produced by the membrane potential (4). The data were filmed with a Grass camera at a film speed of 250 to 500 mm/s. Selected portions of the recordings were digitized with a Nicolet Explorer III digital oscilloscope (20 to 50 &address) (Fig. 2). Synaptic potentials were identified on the basis of their waveform and polarity (1, 3, 6, 9, 11). Records were obtained from 65 motoneurons with K-citrate-filled microelectrodes and from 15 motoneurons with KCl-filled electrodes. The motoneurons (in the spinal segment L7) were identified by the presence of an antidromic action potential induced by peripheral stimulation of the sciatic, tibial, or common peroneal nerves (14). The amplitude of the antidromic spikes (255 mV), the resting membrane potential (255 mV), and the duration of recording (210 min) complied with standards that have been established for intracellular recording from lumbar motoneurons in the chronically prepared cat during W, QS, and AS (14). To examine synaptic activity when it was not contaminated by action potentials, analyses were carried out on those motoneurons that did not present tonic discharge during either W or QS. Discrete hyperpolarizing potentials occurred during AS (Figs. 1 and 2). These potentials emerged from the background activity during the transition from QS to AS. There was great variation in the amplitude of these hyperpolarizing potentials, not only within a given cell, but also when they were compared across cells (Fig. 1). Large potentials of approximately 2 to 3 mV were observed (Fig. 2A); however, potentials as small as 200 PV could also be differentiated.
MOTONEURON
D
WAKEFULNESS m
E
OUIET
INHIBITION
DURING
ACTIVE
SLEEP
473
SLEEP
FIG. 1. Intracellular recordings, obtained with K-citrate-filled microelectrodes, from two different motoneurons during wakefulness, quiet sleep, and active sleep. Traces A, B and D, E reveal background activity during wakefulness and quiet sleep. During active sleep (C, F) there appeared relatively large amplitude hyperpolarizing potentials. Examples of these potentials are shown in an expanded format in Cl-3 and Fl-3. The variety of different amplitudes is evident when the potentials C l-3 are compared to potentials in Fl-3. (Amplitude calibrations are different for each cell.) Both records are from tibial motoneurons. Antidromic action potentials: A, 68 mV; B, 82 mV.
Although these potentials were present throughout the entire period of AS, their occurrence was greatest during the transition from QS to AS and whenever intense clusters of rapid eye movements were present. In both instances, summation of these potentials was clearly observed. In certain episodes of rapid eye movements depolarizing potentials were also present (5). Discrete hyperpolarizing potentials that did not present an inflexion in their rising phase (Fig. 2A) were examined to determine their shape parameters. Due to the high frequency of synaptic bombardment, the half-width was determined only for those potentials that exhibited a decay phase that was not interrupted by succeeding potentials (for example, see potential 1 in Fig. 2A). A detailed analysis of these potentials was carried out in five cells with action and membrane potentials exceeding 70 mV. To avoid the
MORALES
AND CHASE
FIG. 2. Representative recordings from two different motoneurons during quiet sleep and active sleep utilizing microelectrodes filled with two different electrolyte solutions. A-K-citrate electrode. During active sleep, hyperpolarizing potentials were easily distinguishable. Potentials labeled 1-3 are shown in an expanded format. Their 10 to 90% amplitude rise-times, measured from the digitized record, were 1.4, I .6, and 1 ms, respectively. B- K-chloride electrode. Recordings were maintained for 6 min during quiet sleep without any retention current. A hyperpolarizing current of 10 nA was passed for 45 s during quiet sleep approximately 1 min before the animal entered into active sleep. The quiet sleep recording of the membrane potential was obtained after current injection had ceased. The active sleep record of the membrane potential revealed the advent of high-frequency depolarizing potentials. Bl-3 are potentials shown in greater detail; their 10 to 90% rise-times were 0.95, 1.05, and 1 ms, respectively. Depolarizing potentials like these were never observed while recording with K-citrate electrodes; they are interpreted as being reversed inhibitory potentials (7, 13). Calibration signals are identical for the two cells. Both records are from sciatic motoneurons. Antidromic action potentials: A, 72 mV, B, 75 mV.
ambiguities inherent in estimating the shape parameters of the smaller potentials, for each cell 50 consecutive potentials with an amplitude of 1 f 0.15 mV were analyzed. Their mean 10 to 90% rise-time was 0.89 f 0.04
MOTONEURON
INHIBITION
DURING
ACTIVE
SLEEP
475
ms (SE) and their half-width duration was 2.58 ms (+O. 13). Based upon their amplitude, as well as their rise-time and half-width duration, we conclude that these were compound potentials resulting from short-duration bursts of highly synchronized input. The polarity of the hyperpolarizing potentials could be reversed by the injection of chloride ions (Fig. 2B). This result indicates that these hyperpolarizing potentials are true inhibitory postsynaptic potentials (IPSPS). The general waveform and polarity of these potentials, as well as their sensitivity to chloride ions, are comparable to other IPSPs such as those mediating Ia reciprocal inhibition (7, 10). The occurrence of these potentials during AS, which coincides with episodes of postsynaptic inhibition of motoneurons ( 13), indicate that they are likely to underlie or be responsible for this inhibitory process. Synaptic potentials of this nature have not been reported. In fact, Glenn and Dement claimed that neither discrete IPSPs nor EPSPs could be resolved during active sleep from intracellular records of spinal cord motoneurons (8). This claim is not supported by our results. In their work, however, “synaptic noise” was examined after the recorded membrane potential had been subjected to high-pass filtering, full-wave rectification, and integration. Under those circumstances, they found that the majority of motoneurons exhibited a decrease in “synaptic noise” during AS compared with QS, even though this decrease was not statistically significant. Clearly, as shown in Figs. 1 and 2, there is an increase in synaptic inhibitory activity during AS. During the transition from QS to AS, however, they noticed a transient increase in “noise” during the period when we observed a high frequency of occurrence of discrete inhibitory synaptic potentials. For brain stem motoneurons of the trigeminal system, Nakamura et al. (15) determined that postsynaptic inhibition was present during AS and hypothesized that it was directed toward distal dendritic compartments because they found a reduction in intrasomatically recorded synaptic activity during this state. On the other hand, most of the potentials that we described in the present report, on the basis of their large amplitude, fast rise-time, and brief half-width are likely to have their origin in the motoneuron soma or proximal dendrites. Others may be situated at a greater distance from the impaling microelectrode, because some of the inhibitory potentials that we recorded were relatively resistant to polarity reversal by the iontophoretic injection of chloride ions (2, 10). Thus, there may be a difference in the modulation of motor activity during AS between the brain stem and spinal cord. It is clear, however, that for spinal cord motoneurons, somatic or proximal dendritic inhibitory potentials appear to contribute decisively to the process of motoneuron inhibition that occurs during the atonia of active sleep.
476
MORALES
AND CHASE
REFERENCES 1. BLANKENSHIP, J. E., AND M. KUNO. 1968. Analysis of spontaneous subthreshold activity in spinal motoneurons of the cat. J. Neurophysiol. 31: 195-209. 2. BURKE, R. E., L. FEDINA, AND A. LUNDBERG. 1971. Spatial synaptic distribution of recurrent and group Ia inhibitory systems in cat spinal motoneurons. J. Physiol. (London) 214: 305-326. 3. BURKE, R. E., AND P. G. NELSON. 1966. Synaptic activity in motoneurons during natural stimulation of muscle spindles. Science 151: 1088-109 1. 4. CHASE, M. H., S. H. CHANDLER, AND Y. NAKAMURA. 1980. Intracellular determination of membrane potential of trigeminal. motoneurons during sleep and wakemlness. J. Neurophysiol. 44: 349-358. 5. CHASE, M. H., AND F. MORALES. 1979. Subthreshold membrane activity in spinal cord motoneurons during active sleep. Sot. Neurosci. Abstr. 5: 365. 6. COLOMO, F., AND S. D. ERULKAR. 1968. Miniature synaptic potentials of frog spinal neurons in the presence of tetrodotoxin. J. Physiol. (London) 199: 205-222. 7. COOMBS, J. S., J. C. ECCLES,AND P. FATT. 1955. The specific ionic conductances and the ionic movements across the motoneurons membrane that produce the inhibitory postsynaptic potential. J. Physiol. (London) 130: 326-373. 8. GLENN, L. L., AND W. L. DEMENT. 1981. Membrane potential, synaptic activity and excitability of hind-limb motoneurons during wakefulness and sleep. J. Neurophysiol. 46: 839-854. 9.
10. 11. 12. 13. 14. 15.
HUBBARD, V. I., D. STENHOUSE, AND R. A. ECCLES. 1967. Origin of synaptic noise. Science 21: 330-331. JANKOWSKA, E., AND W. J. ROBERTS. 1972. Synaptic actions of single interneurones mediating reciprocal Ia inhibition of motoneurones. J. Physiol. (London) 222: 623-642. KATZ, B., AND R. MILEDI. 1963. A study of spontaneous miniature potentials in spinal motoneurones. J. Physiol. (London) 168: 389-422. MORALES, F. R., AND M. H. CHASE. 1978. Intracellular recording of lumbar motoneuron membrane potential during sleep and wakefulness. Exp. Neural. 62: 821-827. MORALES, F. R., AND M. H. CHASE. 1981. Postsynaptic control of lumbar motoneuron excitability during active sleep in the chronic cat. Brain Rex 225: 279-295. MORALES, F. R., AND M. H. CHASE. 1981. Intracellular recording from spinal cord motoneurons in the chronic cat. Physiol. Behav. 27: 355-362. NAKAMURA, Y., L. J. GOLDBERG, S. H. CHANDLER, AND M. H. CHASE. 1978. Intracellular analysis of trigeminal motoneuron activity during sleep in the cat. Science 199: 204207.
NEUROLOGY
78,47 l-476 (1982)
RESEARCH
NOTE
Repetitive Synaptic Potentials Responsible for Inhibition Spinal Cord Motoneurons during Active Sleep FRANCISCO R. MORALES AND MICHAEL
of
H. CHASE’
Department of Physiology, School of Medicine, University of California, Los Angeles, California 90024 Received May 19, I982 High-gain intracellular recordings of spinal cord motoneurons were obtained in the chronically prepared cat during wakefulness, quiet sleep, and active sleep. Discrete hyperpokuizing postsynaptic potentials were found to occur repetitively throughout active sleep in conjunction with the presence of somatomotor atonia. These potentials were most prominent in the transition period from quiet to active sleep as well as during episodes of rapid eye movements during active sleep. Their polarity was reversed after the intracellular injection of chloride ions. We propose that these are inhibitory potentials which are responsible for or contribute significantly to the postsynaptic inhibition of spinal cord motoneurons during active sleep.
It recently has been shown that alpha motoneurons of the spinal cord are hyperpolarized and their excitability is depressed during active sleep (AS) compared with quiet sleep (QS) or wakefulness (W) (8, 12, 13). In addition, the somadendritic invasion of antidromically induced action potentials is impaired and there is a decrease in motoneuron input resistance (8, 13). These data indicate that motoneurons are subjected to continuous inhibitory synaptic input during the atonia accompanying AS. The present report describes the putative basis for this input, which consists of discrete inhibitory postsynaptic potentials (IPSPs) that impinge on spinal cord motoneurons repetitively throughout AS. Abbreviations: AS, QS-active, quiet sleep; W-wakefulness; IPSP-inhibitory postsynaptic potential. ’ This research was supported by a grant from the National Science Foundation (BNS 7912897). 471 0014-4886/82/l
10471-06$02.00/O
Copyright 0 1982 by Academic Press, Inc. Ail rights of reproduction in any form resewed.
472
MORALES
AND
CHASE
Experiments were conducted on six chronically prepared cats that were undrugged, unanesthetized, and respiring normally. Each animal was implanted with permanent head and lumbar restraining devices and peripheral nerve stimulating electrodes. Recording electrodes for EEG, EQG, and EMG were placed to monitor the states of sleep and wakefulness. These surgical and implantation techniques have been described in detail ( 14). Single-barrel glass micropipettes with tip resistances of 8 to 10 Mn were used for intracellular recording. The microelectrodes were filled with different electrolyte solutions according to the particular experimental objective: 2 M potassium citrate (K-citrate) was used to examine the waveform of inhibitory potentials (7); 3 M potassium chloride (KCl) was utilized when the iontophoretic injection of chloride ions was undertaken to determine the inhibitory nature of the potentials (7). In the latter case, anodal currents of 5 to 10 nA (1 min duration) were delivered during W, QS, and AS. Intracellular DC records (at high amplification-200X) were stored on magnetic tape (high frequency cutoff at 5 kHz) after eliminating, with an automatic offset circuit, the large DC shift produced by the membrane potential (4). The data were filmed with a Grass camera at a film speed of 250 to 500 mm/s. Selected portions of the recordings were digitized with a Nicolet Explorer III digital oscilloscope (20 to 50 &address) (Fig. 2). Synaptic potentials were identified on the basis of their waveform and polarity (1, 3, 6, 9, 11). Records were obtained from 65 motoneurons with K-citrate-filled microelectrodes and from 15 motoneurons with KCl-filled electrodes. The motoneurons (in the spinal segment L7) were identified by the presence of an antidromic action potential induced by peripheral stimulation of the sciatic, tibial, or common peroneal nerves (14). The amplitude of the antidromic spikes (255 mV), the resting membrane potential (255 mV), and the duration of recording (210 min) complied with standards that have been established for intracellular recording from lumbar motoneurons in the chronically prepared cat during W, QS, and AS (14). To examine synaptic activity when it was not contaminated by action potentials, analyses were carried out on those motoneurons that did not present tonic discharge during either W or QS. Discrete hyperpolarizing potentials occurred during AS (Figs. 1 and 2). These potentials emerged from the background activity during the transition from QS to AS. There was great variation in the amplitude of these hyperpolarizing potentials, not only within a given cell, but also when they were compared across cells (Fig. 1). Large potentials of approximately 2 to 3 mV were observed (Fig. 2A); however, potentials as small as 200 PV could also be differentiated.
MOTONEURON
D
WAKEFULNESS m
E
OUIET
INHIBITION
DURING
ACTIVE
SLEEP
473
SLEEP
FIG. 1. Intracellular recordings, obtained with K-citrate-filled microelectrodes, from two different motoneurons during wakefulness, quiet sleep, and active sleep. Traces A, B and D, E reveal background activity during wakefulness and quiet sleep. During active sleep (C, F) there appeared relatively large amplitude hyperpolarizing potentials. Examples of these potentials are shown in an expanded format in Cl-3 and Fl-3. The variety of different amplitudes is evident when the potentials C l-3 are compared to potentials in Fl-3. (Amplitude calibrations are different for each cell.) Both records are from tibial motoneurons. Antidromic action potentials: A, 68 mV; B, 82 mV.
Although these potentials were present throughout the entire period of AS, their occurrence was greatest during the transition from QS to AS and whenever intense clusters of rapid eye movements were present. In both instances, summation of these potentials was clearly observed. In certain episodes of rapid eye movements depolarizing potentials were also present (5). Discrete hyperpolarizing potentials that did not present an inflexion in their rising phase (Fig. 2A) were examined to determine their shape parameters. Due to the high frequency of synaptic bombardment, the half-width was determined only for those potentials that exhibited a decay phase that was not interrupted by succeeding potentials (for example, see potential 1 in Fig. 2A). A detailed analysis of these potentials was carried out in five cells with action and membrane potentials exceeding 70 mV. To avoid the
MORALES
AND CHASE
FIG. 2. Representative recordings from two different motoneurons during quiet sleep and active sleep utilizing microelectrodes filled with two different electrolyte solutions. A-K-citrate electrode. During active sleep, hyperpolarizing potentials were easily distinguishable. Potentials labeled 1-3 are shown in an expanded format. Their 10 to 90% amplitude rise-times, measured from the digitized record, were 1.4, I .6, and 1 ms, respectively. B- K-chloride electrode. Recordings were maintained for 6 min during quiet sleep without any retention current. A hyperpolarizing current of 10 nA was passed for 45 s during quiet sleep approximately 1 min before the animal entered into active sleep. The quiet sleep recording of the membrane potential was obtained after current injection had ceased. The active sleep record of the membrane potential revealed the advent of high-frequency depolarizing potentials. Bl-3 are potentials shown in greater detail; their 10 to 90% rise-times were 0.95, 1.05, and 1 ms, respectively. Depolarizing potentials like these were never observed while recording with K-citrate electrodes; they are interpreted as being reversed inhibitory potentials (7, 13). Calibration signals are identical for the two cells. Both records are from sciatic motoneurons. Antidromic action potentials: A, 72 mV, B, 75 mV.
ambiguities inherent in estimating the shape parameters of the smaller potentials, for each cell 50 consecutive potentials with an amplitude of 1 f 0.15 mV were analyzed. Their mean 10 to 90% rise-time was 0.89 f 0.04
MOTONEURON
INHIBITION
DURING
ACTIVE
SLEEP
475
ms (SE) and their half-width duration was 2.58 ms (+O. 13). Based upon their amplitude, as well as their rise-time and half-width duration, we conclude that these were compound potentials resulting from short-duration bursts of highly synchronized input. The polarity of the hyperpolarizing potentials could be reversed by the injection of chloride ions (Fig. 2B). This result indicates that these hyperpolarizing potentials are true inhibitory postsynaptic potentials (IPSPS). The general waveform and polarity of these potentials, as well as their sensitivity to chloride ions, are comparable to other IPSPs such as those mediating Ia reciprocal inhibition (7, 10). The occurrence of these potentials during AS, which coincides with episodes of postsynaptic inhibition of motoneurons ( 13), indicate that they are likely to underlie or be responsible for this inhibitory process. Synaptic potentials of this nature have not been reported. In fact, Glenn and Dement claimed that neither discrete IPSPs nor EPSPs could be resolved during active sleep from intracellular records of spinal cord motoneurons (8). This claim is not supported by our results. In their work, however, “synaptic noise” was examined after the recorded membrane potential had been subjected to high-pass filtering, full-wave rectification, and integration. Under those circumstances, they found that the majority of motoneurons exhibited a decrease in “synaptic noise” during AS compared with QS, even though this decrease was not statistically significant. Clearly, as shown in Figs. 1 and 2, there is an increase in synaptic inhibitory activity during AS. During the transition from QS to AS, however, they noticed a transient increase in “noise” during the period when we observed a high frequency of occurrence of discrete inhibitory synaptic potentials. For brain stem motoneurons of the trigeminal system, Nakamura et al. (15) determined that postsynaptic inhibition was present during AS and hypothesized that it was directed toward distal dendritic compartments because they found a reduction in intrasomatically recorded synaptic activity during this state. On the other hand, most of the potentials that we described in the present report, on the basis of their large amplitude, fast rise-time, and brief half-width are likely to have their origin in the motoneuron soma or proximal dendrites. Others may be situated at a greater distance from the impaling microelectrode, because some of the inhibitory potentials that we recorded were relatively resistant to polarity reversal by the iontophoretic injection of chloride ions (2, 10). Thus, there may be a difference in the modulation of motor activity during AS between the brain stem and spinal cord. It is clear, however, that for spinal cord motoneurons, somatic or proximal dendritic inhibitory potentials appear to contribute decisively to the process of motoneuron inhibition that occurs during the atonia of active sleep.
476
MORALES
AND CHASE
REFERENCES 1. BLANKENSHIP, J. E., AND M. KUNO. 1968. Analysis of spontaneous subthreshold activity in spinal motoneurons of the cat. J. Neurophysiol. 31: 195-209. 2. BURKE, R. E., L. FEDINA, AND A. LUNDBERG. 1971. Spatial synaptic distribution of recurrent and group Ia inhibitory systems in cat spinal motoneurons. J. Physiol. (London) 214: 305-326. 3. BURKE, R. E., AND P. G. NELSON. 1966. Synaptic activity in motoneurons during natural stimulation of muscle spindles. Science 151: 1088-109 1. 4. CHASE, M. H., S. H. CHANDLER, AND Y. NAKAMURA. 1980. Intracellular determination of membrane potential of trigeminal. motoneurons during sleep and wakemlness. J. Neurophysiol. 44: 349-358. 5. CHASE, M. H., AND F. MORALES. 1979. Subthreshold membrane activity in spinal cord motoneurons during active sleep. Sot. Neurosci. Abstr. 5: 365. 6. COLOMO, F., AND S. D. ERULKAR. 1968. Miniature synaptic potentials of frog spinal neurons in the presence of tetrodotoxin. J. Physiol. (London) 199: 205-222. 7. COOMBS, J. S., J. C. ECCLES,AND P. FATT. 1955. The specific ionic conductances and the ionic movements across the motoneurons membrane that produce the inhibitory postsynaptic potential. J. Physiol. (London) 130: 326-373. 8. GLENN, L. L., AND W. L. DEMENT. 1981. Membrane potential, synaptic activity and excitability of hind-limb motoneurons during wakefulness and sleep. J. Neurophysiol. 46: 839-854. 9.
10. 11. 12. 13. 14. 15.
HUBBARD, V. I., D. STENHOUSE, AND R. A. ECCLES. 1967. Origin of synaptic noise. Science 21: 330-331. JANKOWSKA, E., AND W. J. ROBERTS. 1972. Synaptic actions of single interneurones mediating reciprocal Ia inhibition of motoneurones. J. Physiol. (London) 222: 623-642. KATZ, B., AND R. MILEDI. 1963. A study of spontaneous miniature potentials in spinal motoneurones. J. Physiol. (London) 168: 389-422. MORALES, F. R., AND M. H. CHASE. 1978. Intracellular recording of lumbar motoneuron membrane potential during sleep and wakefulness. Exp. Neural. 62: 821-827. MORALES, F. R., AND M. H. CHASE. 1981. Postsynaptic control of lumbar motoneuron excitability during active sleep in the chronic cat. Brain Rex 225: 279-295. MORALES, F. R., AND M. H. CHASE. 1981. Intracellular recording from spinal cord motoneurons in the chronic cat. Physiol. Behav. 27: 355-362. NAKAMURA, Y., L. J. GOLDBERG, S. H. CHANDLER, AND M. H. CHASE. 1978. Intracellular analysis of trigeminal motoneuron activity during sleep in the cat. Science 199: 204207.