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Hippocampal and cortical EEG activity in rats with transected hypothalamus
Brain Research Bulletin, Vol. 27, pp. 637440.
0 Pergamon Press
plc,
0361-9230191 $3.00 + .OO
1991. Printed in the U.S.A.
Hippocampal and Cortical EEG Activity in Rats With Transected Hypothalamus L. GLIN,’
B. ZERNICK12 AND C. GOTTESMANN3
Laboratoire de Psychophysiologie, Faculte’ des Sciences, Universite’ de Nice, Part Valrose, 06034, Nice cedex, France Received
1 December
1989
GLIN, L., B. ZERNlCIU AND C. GOTTBSMANN. Hippocampal and corrical EEG acriviry in rats wirh rransecred hyporhalamus. BRAIN RBS BULL 27(5) 637440, 1991.-The brain was transected in eight rats: the transection passed through the posterior pole of the superior colliculi and ended down at midhypothalamic level. The EEG activity in the dorsal hippocampus and cortex showed continuously slow, high amplitude waves. Thus the posterior hypothalamus is critical for the previously described hippocampal theta rhythm found in rats transected at the posthypothalamic level.
Hippocampal theta rhythm
Hypothalamic transection
Posterior hypothalamus
Rat
taxically calibrated holder at an angle 45” backwards from the vertical plane in rats 1, 2 and 6-8 and at an angle of 50” in rats 3-5. The transection plane was aimed to pass the basi-horizontal plane A8-All, depending on the size of the rat. The spatula was inserted in the midline, just behind the sinus, pushing it slightly forward. Then it was slightly withdrawn, turned laterally and inserted again. The same procedure was repeated at the other side and the spatula was withdrawn. Just after the transection the ether anesthesia was discontinued. Other methodological details for brain stem transections can be found elsewhere (20). The cortical EEG activity was recorded mono- and bipolarly from the frontal cortex by means of silver ball electrodes of about 1 mm diameter placed on the dura. The reference electrode was screwed to the skull in front of the olfactory bulb at the midline. The EEG activity of the right dorsal hippocampus CA, area (A 3.4; L 2.6; +2.3) was recorded with a multipolar twisted electrode made of insulated (except at the tip) stainless steel wires of 100 pm. In rats 3, 6 and 7 the position of the electrode was changed vertically 1.5 mm with 0.5~mm steps in the later period of recording. The recording started 1 h after the transection (about 9 a.m.) and lasted about 6 h, but in rats 1 and 2 about 24 h. The recording samples were taken every 20 mitt for about 5 min, but at night break (10 p.m.-6 a.m.) in rats 1 and 2. The rectal temperature of the preparations was maintained at 37°C. After the transection the rats were given subcutaneously 2 ml of 5% glucose solution. Rats 1 and 2 were given glucose four times. Level of transections and deep electrode location were conformed on 20-p paraffin sections stained by Nissl and KliiverBarrera techniques. Dorsally, the transection passed the posterior pole of the superior colliculus in rats l-4 and was just behind it
IN the intact animal the hippocampal theta activity depends on the activating influences from the brain stem [(10,17), for review see (2)]. However, long-lasting episodes of continuous theta activity are present in rat (8) and cat (9) intercollicular cerveau isole preparations. Moreover, we have recently found that theta activity is abundant in the majority of precollicular rats: in some preparations the theta rhythm occupied above 50% of recording time and could be induced or its frequency increased by electrical stimulation of the medial posterior hypothalamus (7). These results suggest that in the intact animal the hippocampal theta activity is reduced by some brain stem influences [see (5)], presumably issued from the medial raphe nucleus (13). Moreover, one can suppose that in the precollicullar rat the disinhibited posterior hypothalamus is responsible for the presence of theta rhythm (7). This hypothesis is tested in the present study. METHOD
Reliable information was obtained from eight male Wistar rats. They were identified with numbers according to the level of transection: it was most rostral in rats 1 and 2 and most caudal in rats 7 and 8. Rats weighed about 250 g but rats 6 and 7 about 350 g. Rats 1 and 2 were anesthetized with thiopental sodium (Pentothal, 60 mg/kg, IP) and rats 3-8 were deeply anesthetized with ether. They were placed into the stereotaxic apparatus according to Konig and Klippel coordinates (11). The bone over the cerebellum was removed and the dura cut. The transection was performed with a blunt, flat, thin spatula. The width of its tip was 4.5 mm. The spatula was guided by a plate attached to a stereo-
‘On leave of absence from Dtpartement de Biologie et Physiologie, Faculte des Sciences, Universite d’Abidjan, 22 BP 582 Abidjan, C&e d’Ivoire. ‘On leave of absence from Department of Neurophysiology, Nencki Institute of Experimental Biology, Pasteura 3, 01093 Warsaw, Poland. sRequests for reprints should be addressed to C. Gottesmann, Laboratoire de Psychophysiologie, Faculte des Sciences, Pam Valrose, 06034 Nice cedex, France.
637
C&IN, ZERNlCKI
AND GOlTESMANN
Right
Left
FIG. 1. Transections in rats 7 and 8 (shown with broken solid lines) according to the atlas of KGnig and Klippel (11). Abbreviations: CA, commissura anterior; CC, crus cerebri; CO, chiasma opticum; F, columna fomicis; FMT, fasciculus mamillothaiamicus; FR, fascicuius retroflexus; ha, nucleus anterior hypothalami; hdv, nucleus dorsomedialis hypothaiami, pars vent&is; hl, nucleus later&s hypothalami; LM, lemiscus media&; mml, nucleus mamillaris medialis, pars lateralis; pal, nucleus preopticus lateralis. SN. substantia nigra: TO tractus opticus.
639
THETA ACTIVITY AND HYPOTHALAMUS
RAT 7 FCxA HFCr
RAT 8
FIG. 2. The EEG activity in the frontal cortex and dorsal hippocampus in rats 7 and 8. In rat 7 is seen cortical typical synchronized EEG activity without any theta rhythm in the hippocampus (95 min after transection). In rat 8 theta activity in the hippocampus is accompanied by slow-wave, high amplitude EEG activity in the cortex (90 min after transection). Calibration: 100 )LV, 1 s.
in rats 5-8. Ventrally, it was just behind the chiasma in rats l-4 and at the level of the infundibulum in rats 5-8. The transection was complete in rats 1, 2 and 6. In rats 5 and 7 it was complete, except in the left thalamus. In rat 3 the transection was not complete laterally on the right, in rat 4 on the left, and in rat 8 on both sides (Fig. 1). In all cases the medial hypothalamus was bilaterally cut. The tip of the deep electrode was always in the hippocampus. RESULTS
In all rats both hippocampal and cortical EEG records showed continuous, slow-wave, high amplitude activity (Fig. 2). In the hippocampus this pattern was never interrupted by theta rhythm in rats 1, 2 and 4. In rats 3 and 7 a few l-s episodes of theta appeared. In rats 5 and 6 there were several episodes of theta, each of a few seconds duration; the theta did not exceed 1% of the recording time. In contrast, in rat 8 (with incomplete transection laterally) the continuous theta rhythm took about 30% of the recording time; its mean frequency being 4 c/s (Fig. 2). During theta rhythm the cortical EEG activity remained unchanged (Fig. 2). However, in rats 3 and 4 theta rhythm appeared during an episode of EEG flattening lasting about 20 s. In the cortical EEG activity the spindles were never observed in rats l-5. In rats 6 and 8, abortive spindles occasionally appeared. In rat 7 the abortive spindles with some EEG desynchronization in the intermediate lulls took about 30% of the recording
time. These spindles could be due to preservation lamic reticular nucleus (16).
of tbe tba-
DISCUSSION
Just prior to paradoxical sleep (PS) the rat (3) and cat (6) show a short-lasting intermediate electrophysiological stage characterized by high amplitude cortical spindles (index of deep slow-wave sleep) and low frequency hippocampal theta rhythm (index of central activation). This unusual pattern association is massively extended at the expense of PS by low doses of barbiturates (3). We hypothetized a long time ago that this theta rhythm has to appear through a disinhibitory process and that it corresponds to a state of the cerveau isole preparation (4). In confirmation, we found that the intercollicularly transected rat (8) and cat (6) show for hours high amplitude cortical spindles and continuous or almost continuous low frequency theta rhythm. This result shows that in front of the intercollicular level there is a theta rhythm trigger, able to induce monotonous theta rhythm. In the following study we found that precollicular transections can be followed by a large amount of theta rhythm (7). Since medio-posterior hypothalamic stimulation induced or modulated this theta rhythm, we hypothetized that this structure is a trigger zone of the theta activity of the precollicularly transected preparation (7). Our present results show that rats transected at the midhypothalamic level do not virtually show any theta rhythm. The few
640
GLIN, ZERNICKI AND GOTTESMANN
seconds episodes of theta rhythm could be of hippocampal origin [as theta rhythm recorded in slice preparations, (12)] or could be generated in the entorhinal cortex (1) which is related to hippocampus CA, area by several synaptic pathways (19). In contrast, abundant theta rhythm was found in rat 8 with the uncomplete transection laterally. Consequently, the structures triggering the theta rhythm would be situated in the posterior hypothalamus, as postulated by Wilson et al. (18). However, our results suggest that this trigger zone could be rather diffuse as suggested by Robinson and Whishaw (15). Altogether the results suggest that since during sleep the medial raphe nucleus [which inhibits theta rhythm appearance, (13)] is silent or almost silent just prior to PS (14) the low frequency theta rhythm of the intermediate stage of sleep occurs through a disinhibition of the hypothalamic trigger. Since during PS the medial raphe nucleus remains silent, the theta rhythm would be also mainly of hypothalamic origin during this sleep stage. Only the slight ionic Increase of frequency o&-ring dking-PS anh
the stronger transient
increase occurring during the phasic motor activities (particularly during rapid eye movements) could be of lower brain stem origin. The only lower brain stem influences. mainly from the pontine level, are probably not strong enough to generate the high frequency synchronized theta rhythm of PS. In fact, the electrolytic lesion of the posterior hypothalamus decreases the frequency of theta rhythm during PS (15). However, the electrolytic lesion destroys both the cells and ascending fibers. It would be interesting to destroy selectively the hypothetic hypothalamic trigger cells by ibotenic acid to study the characteristics of theta rhythm during sleep. ACKNOWLEDGEMENTS
This study was partially supported by a grant from PACA Regional Council. We thank Dr. A. Kosmal for help in histological analysis of data and Dr. G. Gandolfo for his help at the very beginning of this research.
REFERENCES 1. Alonso, A.; Garcia-Austt, E. Neuronal sources of theta rhythm in the entorhinal cortex of the rat. II. Phase relations between unit discharges and theta field potentials. Exp. Brain Res. 67502-509; 1987. 2. Bland, B. H. The physiology and pharmacology of hippocampal formation theta rhythms. Prog. Neurobiol. 26:1-54; 1986. 3. Gottesmann, D. Donnees sur l’activitk corticale au tours du sommeil profond chez le rat. C. R. Sot. Biol. (Paris) 158:1829-1834: 1964. 4. Gottesmann, C. Recherche sur la psychophysiologie du sommeil chez le rat. Paris: Presses du Palais-Royal; 1967. 5. Gottesmann, C. What the cerveau isolC preparation tells us nowadays about sleep-wake mechanisms? Neurosci. Biobehav. Rev. 12: 39-48; 1988. 6. Gottesmann, C.; Gandolfo, B.; Zemicki, B. Intermediate stage of sleep in the cat. J. Physiol. (Paris) 79:365-372; 1984. 7. Gottesmann, C.; Gandolfo, G.; Zemicki, B. Hippocampal theta activity in the acute precollicular rat. Brain Res. Bull. 22:959-962; 1989. 8. Gottesmann, C.; User, P.; Gioanni, H. Sleep: a physiological cerveau is016 stage? Waking Sleep 4:1-7; 1980. 9. Gottesmann, C.; Zemicki, B.; Gandolfo, G. Hippocampal theta activity in the acute cerveau is016 cat. Acta Neurobiol. Exp. (Warsz.) 41:251-255; 1981. 10. Green, J. D.; Arduini, A. Hippocampal electrical activity in arousal. J. Neurophysiol. 17:532-557; 1954. 11. Kiinig; J.F.R.; Klippel, R. A. The rat brain. A stereotaxic atlas. Baltimore: Williams and Wilkins Co.; 1963.
12. Konopacki, J.; Maciver, M. B.; Bland, B. H.; Roth, S. H. Theta in hippocampal slices: Relation to synaptic responses of dentate neurons. Brain Res. Bull. 18:25-27; 1987. 13. Maru, E.; Takahashi, L. K.; Iwahara, S. Effects of median raphe nucleus lesions on hippocampal EEG in the freely moving rat. Brain Res. 163:223-234; 1979. 14. Rasmussen, K.; Heym, J.; Jacobs, B. L. Activity of serotonin-containing neurons on nucleus centralis superior of freely moving cats. Exp. Neurol. 83:302-317; 1984. 15. Robinson, T. E.; Whishaw, I. Q. Effects of posterior hypothalamic lesions on voluntary behavior and hippocampal electroencephalograms in the rat. J. Comp. Physiol. Psychol. 86:768-786; 1974. 16. Steriade, M.; Domich, L.; Oakson, G.; Deschsnes, M. The deafferented reticular thalamic nucleus generates spindle rhythmicity. J. Neurophysiol. 57:2&l-273; 1987. 17. Vertes, R. P. An analysis of ascending brain stem systems involved in hippocampal synchronization and desynchronization. J. Neurophysiol. 46:1140-1159; 1981. 18. Wilson, C. L.; Motter, B. C.; Lindsley, D. B. Influences of hypothalamic stimuli upon septal and hippocampal electrical activity in the cat. Brain Res. 107:55-68; 1976. 19. Yeckel, M. F.; Berger T. W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc. Natl. Acad. Sci. USA 87: 5832-5836; 1990. 20. Zemicki, B. Pretrigeminal preparation. Arch. Ital. Biol. 124:133196; 1986.
0 Pergamon Press
plc,
0361-9230191 $3.00 + .OO
1991. Printed in the U.S.A.
Hippocampal and Cortical EEG Activity in Rats With Transected Hypothalamus L. GLIN,’
B. ZERNICK12 AND C. GOTTESMANN3
Laboratoire de Psychophysiologie, Faculte’ des Sciences, Universite’ de Nice, Part Valrose, 06034, Nice cedex, France Received
1 December
1989
GLIN, L., B. ZERNlCIU AND C. GOTTBSMANN. Hippocampal and corrical EEG acriviry in rats wirh rransecred hyporhalamus. BRAIN RBS BULL 27(5) 637440, 1991.-The brain was transected in eight rats: the transection passed through the posterior pole of the superior colliculi and ended down at midhypothalamic level. The EEG activity in the dorsal hippocampus and cortex showed continuously slow, high amplitude waves. Thus the posterior hypothalamus is critical for the previously described hippocampal theta rhythm found in rats transected at the posthypothalamic level.
Hippocampal theta rhythm
Hypothalamic transection
Posterior hypothalamus
Rat
taxically calibrated holder at an angle 45” backwards from the vertical plane in rats 1, 2 and 6-8 and at an angle of 50” in rats 3-5. The transection plane was aimed to pass the basi-horizontal plane A8-All, depending on the size of the rat. The spatula was inserted in the midline, just behind the sinus, pushing it slightly forward. Then it was slightly withdrawn, turned laterally and inserted again. The same procedure was repeated at the other side and the spatula was withdrawn. Just after the transection the ether anesthesia was discontinued. Other methodological details for brain stem transections can be found elsewhere (20). The cortical EEG activity was recorded mono- and bipolarly from the frontal cortex by means of silver ball electrodes of about 1 mm diameter placed on the dura. The reference electrode was screwed to the skull in front of the olfactory bulb at the midline. The EEG activity of the right dorsal hippocampus CA, area (A 3.4; L 2.6; +2.3) was recorded with a multipolar twisted electrode made of insulated (except at the tip) stainless steel wires of 100 pm. In rats 3, 6 and 7 the position of the electrode was changed vertically 1.5 mm with 0.5~mm steps in the later period of recording. The recording started 1 h after the transection (about 9 a.m.) and lasted about 6 h, but in rats 1 and 2 about 24 h. The recording samples were taken every 20 mitt for about 5 min, but at night break (10 p.m.-6 a.m.) in rats 1 and 2. The rectal temperature of the preparations was maintained at 37°C. After the transection the rats were given subcutaneously 2 ml of 5% glucose solution. Rats 1 and 2 were given glucose four times. Level of transections and deep electrode location were conformed on 20-p paraffin sections stained by Nissl and KliiverBarrera techniques. Dorsally, the transection passed the posterior pole of the superior colliculus in rats l-4 and was just behind it
IN the intact animal the hippocampal theta activity depends on the activating influences from the brain stem [(10,17), for review see (2)]. However, long-lasting episodes of continuous theta activity are present in rat (8) and cat (9) intercollicular cerveau isole preparations. Moreover, we have recently found that theta activity is abundant in the majority of precollicular rats: in some preparations the theta rhythm occupied above 50% of recording time and could be induced or its frequency increased by electrical stimulation of the medial posterior hypothalamus (7). These results suggest that in the intact animal the hippocampal theta activity is reduced by some brain stem influences [see (5)], presumably issued from the medial raphe nucleus (13). Moreover, one can suppose that in the precollicullar rat the disinhibited posterior hypothalamus is responsible for the presence of theta rhythm (7). This hypothesis is tested in the present study. METHOD
Reliable information was obtained from eight male Wistar rats. They were identified with numbers according to the level of transection: it was most rostral in rats 1 and 2 and most caudal in rats 7 and 8. Rats weighed about 250 g but rats 6 and 7 about 350 g. Rats 1 and 2 were anesthetized with thiopental sodium (Pentothal, 60 mg/kg, IP) and rats 3-8 were deeply anesthetized with ether. They were placed into the stereotaxic apparatus according to Konig and Klippel coordinates (11). The bone over the cerebellum was removed and the dura cut. The transection was performed with a blunt, flat, thin spatula. The width of its tip was 4.5 mm. The spatula was guided by a plate attached to a stereo-
‘On leave of absence from Dtpartement de Biologie et Physiologie, Faculte des Sciences, Universite d’Abidjan, 22 BP 582 Abidjan, C&e d’Ivoire. ‘On leave of absence from Department of Neurophysiology, Nencki Institute of Experimental Biology, Pasteura 3, 01093 Warsaw, Poland. sRequests for reprints should be addressed to C. Gottesmann, Laboratoire de Psychophysiologie, Faculte des Sciences, Pam Valrose, 06034 Nice cedex, France.
637
C&IN, ZERNlCKI
AND GOlTESMANN
Right
Left
FIG. 1. Transections in rats 7 and 8 (shown with broken solid lines) according to the atlas of KGnig and Klippel (11). Abbreviations: CA, commissura anterior; CC, crus cerebri; CO, chiasma opticum; F, columna fomicis; FMT, fasciculus mamillothaiamicus; FR, fascicuius retroflexus; ha, nucleus anterior hypothalami; hdv, nucleus dorsomedialis hypothaiami, pars vent&is; hl, nucleus later&s hypothalami; LM, lemiscus media&; mml, nucleus mamillaris medialis, pars lateralis; pal, nucleus preopticus lateralis. SN. substantia nigra: TO tractus opticus.
639
THETA ACTIVITY AND HYPOTHALAMUS
RAT 7 FCxA HFCr
RAT 8
FIG. 2. The EEG activity in the frontal cortex and dorsal hippocampus in rats 7 and 8. In rat 7 is seen cortical typical synchronized EEG activity without any theta rhythm in the hippocampus (95 min after transection). In rat 8 theta activity in the hippocampus is accompanied by slow-wave, high amplitude EEG activity in the cortex (90 min after transection). Calibration: 100 )LV, 1 s.
in rats 5-8. Ventrally, it was just behind the chiasma in rats l-4 and at the level of the infundibulum in rats 5-8. The transection was complete in rats 1, 2 and 6. In rats 5 and 7 it was complete, except in the left thalamus. In rat 3 the transection was not complete laterally on the right, in rat 4 on the left, and in rat 8 on both sides (Fig. 1). In all cases the medial hypothalamus was bilaterally cut. The tip of the deep electrode was always in the hippocampus. RESULTS
In all rats both hippocampal and cortical EEG records showed continuous, slow-wave, high amplitude activity (Fig. 2). In the hippocampus this pattern was never interrupted by theta rhythm in rats 1, 2 and 4. In rats 3 and 7 a few l-s episodes of theta appeared. In rats 5 and 6 there were several episodes of theta, each of a few seconds duration; the theta did not exceed 1% of the recording time. In contrast, in rat 8 (with incomplete transection laterally) the continuous theta rhythm took about 30% of the recording time; its mean frequency being 4 c/s (Fig. 2). During theta rhythm the cortical EEG activity remained unchanged (Fig. 2). However, in rats 3 and 4 theta rhythm appeared during an episode of EEG flattening lasting about 20 s. In the cortical EEG activity the spindles were never observed in rats l-5. In rats 6 and 8, abortive spindles occasionally appeared. In rat 7 the abortive spindles with some EEG desynchronization in the intermediate lulls took about 30% of the recording
time. These spindles could be due to preservation lamic reticular nucleus (16).
of tbe tba-
DISCUSSION
Just prior to paradoxical sleep (PS) the rat (3) and cat (6) show a short-lasting intermediate electrophysiological stage characterized by high amplitude cortical spindles (index of deep slow-wave sleep) and low frequency hippocampal theta rhythm (index of central activation). This unusual pattern association is massively extended at the expense of PS by low doses of barbiturates (3). We hypothetized a long time ago that this theta rhythm has to appear through a disinhibitory process and that it corresponds to a state of the cerveau isole preparation (4). In confirmation, we found that the intercollicularly transected rat (8) and cat (6) show for hours high amplitude cortical spindles and continuous or almost continuous low frequency theta rhythm. This result shows that in front of the intercollicular level there is a theta rhythm trigger, able to induce monotonous theta rhythm. In the following study we found that precollicular transections can be followed by a large amount of theta rhythm (7). Since medio-posterior hypothalamic stimulation induced or modulated this theta rhythm, we hypothetized that this structure is a trigger zone of the theta activity of the precollicularly transected preparation (7). Our present results show that rats transected at the midhypothalamic level do not virtually show any theta rhythm. The few
640
GLIN, ZERNICKI AND GOTTESMANN
seconds episodes of theta rhythm could be of hippocampal origin [as theta rhythm recorded in slice preparations, (12)] or could be generated in the entorhinal cortex (1) which is related to hippocampus CA, area by several synaptic pathways (19). In contrast, abundant theta rhythm was found in rat 8 with the uncomplete transection laterally. Consequently, the structures triggering the theta rhythm would be situated in the posterior hypothalamus, as postulated by Wilson et al. (18). However, our results suggest that this trigger zone could be rather diffuse as suggested by Robinson and Whishaw (15). Altogether the results suggest that since during sleep the medial raphe nucleus [which inhibits theta rhythm appearance, (13)] is silent or almost silent just prior to PS (14) the low frequency theta rhythm of the intermediate stage of sleep occurs through a disinhibition of the hypothalamic trigger. Since during PS the medial raphe nucleus remains silent, the theta rhythm would be also mainly of hypothalamic origin during this sleep stage. Only the slight ionic Increase of frequency o&-ring dking-PS anh
the stronger transient
increase occurring during the phasic motor activities (particularly during rapid eye movements) could be of lower brain stem origin. The only lower brain stem influences. mainly from the pontine level, are probably not strong enough to generate the high frequency synchronized theta rhythm of PS. In fact, the electrolytic lesion of the posterior hypothalamus decreases the frequency of theta rhythm during PS (15). However, the electrolytic lesion destroys both the cells and ascending fibers. It would be interesting to destroy selectively the hypothetic hypothalamic trigger cells by ibotenic acid to study the characteristics of theta rhythm during sleep. ACKNOWLEDGEMENTS
This study was partially supported by a grant from PACA Regional Council. We thank Dr. A. Kosmal for help in histological analysis of data and Dr. G. Gandolfo for his help at the very beginning of this research.
REFERENCES 1. Alonso, A.; Garcia-Austt, E. Neuronal sources of theta rhythm in the entorhinal cortex of the rat. II. Phase relations between unit discharges and theta field potentials. Exp. Brain Res. 67502-509; 1987. 2. Bland, B. H. The physiology and pharmacology of hippocampal formation theta rhythms. Prog. Neurobiol. 26:1-54; 1986. 3. Gottesmann, D. Donnees sur l’activitk corticale au tours du sommeil profond chez le rat. C. R. Sot. Biol. (Paris) 158:1829-1834: 1964. 4. Gottesmann, C. Recherche sur la psychophysiologie du sommeil chez le rat. Paris: Presses du Palais-Royal; 1967. 5. Gottesmann, C. What the cerveau isolC preparation tells us nowadays about sleep-wake mechanisms? Neurosci. Biobehav. Rev. 12: 39-48; 1988. 6. Gottesmann, C.; Gandolfo, B.; Zemicki, B. Intermediate stage of sleep in the cat. J. Physiol. (Paris) 79:365-372; 1984. 7. Gottesmann, C.; Gandolfo, G.; Zemicki, B. Hippocampal theta activity in the acute precollicular rat. Brain Res. Bull. 22:959-962; 1989. 8. Gottesmann, C.; User, P.; Gioanni, H. Sleep: a physiological cerveau is016 stage? Waking Sleep 4:1-7; 1980. 9. Gottesmann, C.; Zemicki, B.; Gandolfo, G. Hippocampal theta activity in the acute cerveau is016 cat. Acta Neurobiol. Exp. (Warsz.) 41:251-255; 1981. 10. Green, J. D.; Arduini, A. Hippocampal electrical activity in arousal. J. Neurophysiol. 17:532-557; 1954. 11. Kiinig; J.F.R.; Klippel, R. A. The rat brain. A stereotaxic atlas. Baltimore: Williams and Wilkins Co.; 1963.
12. Konopacki, J.; Maciver, M. B.; Bland, B. H.; Roth, S. H. Theta in hippocampal slices: Relation to synaptic responses of dentate neurons. Brain Res. Bull. 18:25-27; 1987. 13. Maru, E.; Takahashi, L. K.; Iwahara, S. Effects of median raphe nucleus lesions on hippocampal EEG in the freely moving rat. Brain Res. 163:223-234; 1979. 14. Rasmussen, K.; Heym, J.; Jacobs, B. L. Activity of serotonin-containing neurons on nucleus centralis superior of freely moving cats. Exp. Neurol. 83:302-317; 1984. 15. Robinson, T. E.; Whishaw, I. Q. Effects of posterior hypothalamic lesions on voluntary behavior and hippocampal electroencephalograms in the rat. J. Comp. Physiol. Psychol. 86:768-786; 1974. 16. Steriade, M.; Domich, L.; Oakson, G.; Deschsnes, M. The deafferented reticular thalamic nucleus generates spindle rhythmicity. J. Neurophysiol. 57:2&l-273; 1987. 17. Vertes, R. P. An analysis of ascending brain stem systems involved in hippocampal synchronization and desynchronization. J. Neurophysiol. 46:1140-1159; 1981. 18. Wilson, C. L.; Motter, B. C.; Lindsley, D. B. Influences of hypothalamic stimuli upon septal and hippocampal electrical activity in the cat. Brain Res. 107:55-68; 1976. 19. Yeckel, M. F.; Berger T. W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc. Natl. Acad. Sci. USA 87: 5832-5836; 1990. 20. Zemicki, B. Pretrigeminal preparation. Arch. Ital. Biol. 124:133196; 1986.