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1 Departamento de Neurociencias, Instituto de Fisiología Celular and 2 Departamento de Anatomía, Facultad de Medicina, Universidad Nacional Autónoma de México, D.F. 04510 México
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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The reciprocal connections between the paraventricular thalamic nucleus (PVT) and the suprachiasmatic nuclei suggest that PVT may participate in the regulation of circadian rhythms. We studied in rats the effect of lesions of the anterior and midposterior regions of the PVT on phase shifts of drinking circadian rhythm induced by light pulses at circadian times 6, 12, and 23, as well as the phase shifts produced by electrical or glutamatergic stimulation of the anterior PVT at the same circadian times. Lesion of the anterior PVT abolishes the advances induced by light during late subjective night, whereas midposterior PVT lesions did not affect the phase shifts. Electrical stimulation or glutamate injections in the anterior PVT mimic the phase-shifting effects of light pulses. These results indicate the participation of the anterior PVT as a modulator of entrainment of circadian rhythms to light.
phase advances; paraventricular thalamic nucleus stimulation; paraventricular thalamic nucleus lesions; suprachiasmatic nucleus modulation; photic entrainment
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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IN MAMMALS, THE SUPRACHIASMATIC nuclei (SCN) of the hypothalamus are the main pacemaker driving many behavioral, neuroendocrine, and autonomic circadian rhythms (20). Photic input to the SCN via the retinohypothalamic tract allows entrainment of circadian rhythmicity to the light-dark cycle (29). Other inputs to the SCN arising from the intergeniculate leaflet (17) and the mesencephalic raphe nuclei (30) modulate the entrainment of rhythmicity to light, either increasing or decreasing the response of the pacemaker to light, and seem to be involved in entrainment to nonphotic stimuli as well (29).
Another input to the SCN arises from the anterior part of the paraventricular thalamic nucleus (PVT) (25, 27). This nucleus is part of the thalamic midline nuclei and has been architecturally divided into anterior and posterior subregions (5, 27). The PVT is a multisensorial structure and receives inputs from different nuclei from the brain stem, as well as the prefrontal cortex, amygdala, and many hypothalamic cell groups including the SCN (5, 16). Efferents from the SCN project to the posterior PVT (37, 38). The reciprocal connections of PVT with the SCN, along with the inputs to PVT from other components of the circadian system such as the subparaventricular zone and the intergeniculate leaflet, suggest that PVT might play a role in the regulation of circadian rhythms. However, to this moment, such a role has not been completely elucidated. Electrolitic lesions of the PVT in hamsters have no effect in either the expression of locomotor circadian rhythms in a 14:10-h photoperiod or in its ability to reentrain to an 8-h advance in the time of light onset (12). In blind rats, however, electrolitic lesion of the PVT produces lengthening of the free running period and concentrates the locomotor activity to the late subjective night (26). On the other hand, lesion of the posterior PVT increases food intake mainly during the light phase, which may be due to a disruption of information that regulates feeding where the PVT may serve as a convergence relay for the efferents from the circadian timing system, the hypothalamic nuclei involved in feeding and the limbic system (6).
The phase response curve (PRC) is a valuable tool to study the dynamics and mechanisms of entrainment of circadian pacemakers to a discrete stimulus in subjects maintained under constant conditions and therefore expressing free running circadian rhythmicity. Typically, the PRC to light shows three characteristic regions; a nonresponsive interval during the subjective day (dead zone), while phase delays and advances are induced by light during the early and late subjective night, respectively (10). The use of the PRC has allowed for dissection among the different neurochemical and intracellular signaling pathways involved in light-induced phase advances or delays (14, 15).
In the present study, we used the PRC as the experimental tool to study the role of PVT in the process of entrainment to light of the circadian rhythm of drinking behavior in rats. First, we studied the effect of lesions of the anterior and midposterior regions of the PVT on the phase shifts induced by light pulses presented at the three characteristic regions of the PRC [dead zone at circadian time (CT) 6, phase delays at CT12, and phase advances at CT23]. We also studied the phase shifts of circadian rhythmicity produced by electrical or chemical stimulation of the PVT at the same three circadian times. Present results indicate that 1) lesions of the anterior PVT alter the shape of the PRC to light by abolishing the advances induced by light during late subjective night and 2) electrical or chemical stimulation of PVT mimics the phase-shifting effects of light pulses.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Adult male Wistar rats weighing 180-200 g were used. Animals were housed individually in Plexiglas cages in a room with constant red light (DD; 50 lx). Drinking behavior was continuously monitored with a computerized system (1). Temperature in the room was kept between 20 and 22°C, and water and food were provided ad libitum. All experimental procedures were conducted according to the institutional guide for care and use of animal experimentation for the Unversidad Nacional Autónoma de México, which comply with the guiding principles for research from the American Physiological Society (3).
Surgery
All surgical procedures were performed in antiseptical conditions and under deep anesthesia with chloral hydrate (400 mg/kg body wt ip). For the first experiment, animals were randomly assigned to one of three groups; the first group received electrolytic lesions of the anterior PVT (AP
1.0 mm from bregma; L 0.0; V 6.0 from the
skull surface), and the second group received lesions of the
midposterior PVT (AP 2.6; L 0.0; V 5.5). The lesion was made by
passing 1-mA direct current for 45 s through a stainless steel
electrode (0000) insulated except for 0.5 mm at the tip. A third group
of rats (sham lesioned) was treated exactly the same as rats receiving
lesions but no current was passed through the electrode. Animals were
allowed to recover for a week after surgery before starting the
behavioral recording.
For the second experiment, rats were implanted with a bipolar
chrome-nickel electrode (300-µm diameter) in the anterior PVT (AP
1.0; L 0.0; V 5.5); each electrode tip was welded to a miniature connector and the assemble was fixed to the skull with stainless steel
screws and dental acrylic. This electrode was used to electrically stimulate the nucleus in the free moving animal.
For the third experiment, animals were implanted with a stainless steel cannula (25 gauge) 3 mm above the anterior PVT, which was fixed to the skull with stainless steel screws and dental acrylic. This cannula was used as a guide to introduce an injector (27 gauge) into PVT to administer either vehicle or glutamate solutions to the free moving animal.
Behavioral Recordings
Behavioral recordings consisted of counting the number of touches to the water spout in 15-min bins. Data were stored in magnetic media and graphed as double-plot actograms for later inspection and further analysis. Estimation of activity onset (CT12) was done in a 10- to 15-day segment as follows: first, data were filtered to plot only those bins with values equal or above the mean for that segment, and the first bin of activity for each day of the segment was identified. Then a line was fitted by linear regression to adjust these activity onsets. Such line was plotted on a nonfiltered actogram for illustration purposes and indicates the estimated CT12 for each day of the segment. Other circadian times at which animals were manipulated, such as CT6 and CT23, were calculated from the estimated CT12. After the experimental manipulations (light pulses, electrical or chemical stimulation of PVT), CT12 was estimated during the next 10 consecutive cycles that showed a stable phase and a period similar to the one previous to the stimulus, and the line was projected to the day when the manipulation occurred. The transient cycles were counted from the day the light pulse was applied to the previous day when stable phase and period were found. Phase shifts induced by the experimental manipulations were measured from the difference of CT12 regression lines between the segments before and after the manipulation.Stimulation Procedures
At the selected time of stimulation, each rat was transferred into a Plexiglas cage. Light stimulation consisted of 1-h light pulses of 400 lx (at the bottom of the cage). Electrical stimulation was provided by a Grass S-8800 electrical stimulator and consisted of a train of square direct current pulses (10 ms, 0.3 mA) at 0.5 Hz during 30 min. For the chemical stimulation, each rat received 1 µl of glutamate (1.5 µg/µl) in phosphate buffer saline (50 mM, pH 7.2) with a Hamilton microsyringe (7001) attached to a stainless steel injector (27 gauge) by tygon tubing. All procedures were carried out under red dim light (50 lx) with the exception of the light pulses that were applied inside the light-tight chamber provided with a 40-W white fluorescent tube. Control animals were handled as described but no stimulus was provided. For the chemical stimulation, control animals were injected with 1 µl of vehicle.Histology
At the end of the experiments, the animals were deeply anestethized with an overdose of pentobarbital sodium (200 mg/kg body wt ip) and transcardially perfused with physiological saline solution (NaCl, 0.9%) followed by 4% paraformaldehyde in phosphate buffer (0.1 M, pH 7.2). The brain was removed and cryoprotected in successive sucrose solutions (10, 20, and 30%). Four sets of serial coronal sections 40-µm thick were obtained with a cryostat, from the anterior to the posterior commissures. One set of sections was stained for Nissl with cresyl violet, dehydrated with alcohol, cleared with xylene, and placed under a coverslip with permount. Serial reconstruction of the lesion placement or the position of either the electrode or the cannula was made from camera lucida drawings at ×40.Experimental Design
Experiment 1.
This experiment was aimed to determine the effect of PVT lesions (PVTx)
on light-induced phase shifts at three different circadian times. Three
groups of nine rats each (sham lesions, anterior PVTx, and midposterior
PVTx) were studied. Each animal received a light pulse (400 lx, 1 h) at CT6, CT12, or CT23 in a
counterbalanced design; these time points were selected to explore the
main regions of the PRC (dead zone, delays, and advances,
respectively). After a baseline recording of 15 days, animals were
stimulated at the selected time as previously described and then
recorded for at least 15 additional days. The last 10 days of recording
were used as the baseline for the next experimental segment. At the end of the experiment, all lesioned animals were processed for histology as
described. The effects of the light stimulation on the magnitude and
direction of the phase shifts and the number of transients were
estimated as previously described. To determine the effect of the
lesion on the endogenous period of rhythmicity, this parameter was
estimated by the 
2 periodogram (36), and
the mean values were compared among the three groups by a one-way ANOVA
followed by the Tukey post hoc test. In this and the remaining
experiments, data were analyzed with the DiSPAC software developed and
validated in our laboratory (1). Statistical comparisons
were made using Statistica v 4.3 (Stat-Soft).
Experiment 2. This experiment was aimed at determining the effect of electrical stimulation of the anterior PVT on the phase of activity onset at three different circadian times. One group of nine animals was implanted with a twisted bipolar electrode for electrical stimulation of PVT; at the three circadian times selected (CT6, CT12, and CT23), animals were stimulated or sham manipulated in a counterbalanced design as follows. After recovery from surgery, animals were recorded under DD for 10 days to establish CT12 (activity onset) and to determine the proper time of stimulation. After electrical stimulation, the recording continued for 15 days. The last 10 days of recording were used as the baseline for the next experimental segment. The parameters under study were the same as those of experiment 1. The effect of electrical stimulation and the time of manipulation on the direction and magnitude of the phase shifts were analyzed with a two-way ANOVA for repeated measurements followed by the Tukey post hoc test. At the end of the experiment, the animals were processed for histology to verify the position of the electrode in the brain.
Experiment 3. To rule out the effect of electrical stimulation of fibers on passage or retrograde stimulation from terminals at the level of PVT, this experiment was aimed to determine the effect of glutamate stimulation at three different circadian times in the anterior PVT on the phase of activity onset. Twenty-seven animals were implanted with a stainless steel guide cannula to place an injector to chemically stimulate the nucleus with glutamate. These animals were randomly assigned to one of three groups (CT6, CT12, and CT23). The animals from each group (n = 9) were injected at only one of the circadian times with glutamate and vehicle in a counterbalanced design. After recovery from surgery, animals were recorded under DD for 10 days to establish CT12 and to determine the time for next day injection with either glutamate or vehicle. The recording then continued for 15 days, the last 10 days of recording were used as the baseline for the next injection. Phase shifts were estimated as previously described. The effect of time of chemical stimulation on direction and magnitude of the shifts were analyzed with a one-way ANOVA for independent groups followed by the Tukey post hoc test. At the end of the experiment, animals were processed for histology to verify the position of the injector in the brain.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Experiment 1
Histological verification of the group with anterior PVTx showed that only five animals had complete destruction of the PVT (Fig. 1A), three animals showed varying degrees of partial damage of the dorsal aspect of the nucleus, and in one subject the lesion completely spared PVT. Complete lesions of the anterior PVT also involved surrounding thalamic nuclei such as the paratenial, centromedial, anteromedial, and stria medularis. With respect to the lesion of the midposterior PVT group, in six animals the lesion involved the middle and most of the midposterior parts of PVT and extended in varying degrees into the surrounding thalamic nuclei, such as the nucleus paratenialis, nucleus dorsal intermedius, lateral habenular nucleus, and middorsal nucleus of the thalamus (Fig. 1B). In the remaining three animals of this group, the lesion affected only partially the midposterior PVT. The results from animals with complete lesion of PVT (either anterior or midposterior) will be reported separate from those with incomplete lesions.
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According to the periodogram, the endogenous period of rhythmicity showed a nonsignificant decrease in animals with lesion of both anterior PVT (24.35 ± 0.19 min, means ± SE) and midposterior PVT (24.19 ± 0.10 min) with respect to sham-lesioned animals (24.41 ± 0.09 min). No evident effect of the lesions was found in the architecture of the rhythm.
Light pulses in sham-lesioned animals induced phase shifts of
rhythmicity similar to those found in intact animals (Fig.
2), at CT6 no evident shifts
were found (6.6 ± 5.5 min, means ± SE), whereas at
CT12 and CT23, light-induced phase delays
(102.5 ± 5.6 min) or phase advances (98.3 ± 5.9 min) were
present, respectively. Animals with lesion of the midposterior
PVT (Fig. 2) showed a similar pattern of light-induced phase shifts at
CT6 (12.5 ± 6.02 min) and CT12 (86.7 ± 4.59 min) and slightly larger advances induced at CT23
(123.8 ± 7.5 min) than sham-lesioned animals. In contrast,
animals with lesion of the anterior PVT (Fig. 2) did not show phase
advances at CT23 but rather phase delays (97.5 ± 5.7 min), although they showed similar effects of light at CT6 and CT12 (13.5 ± 7.6 and 109.8 ± 6.7 min,
respectively) as their sham controls. These results are summarized in
Fig. 3. Statistical analysis indicated
significant differences in the phase shifts induced at CT23
in the group with anterior PVT lesion with respect to the other two
groups [F(2,17) = 132.1, P < 0.0001; Tukey test P < 0.01].
Animals with incomplete PVT lesion showed similar phase responses to
those found in sham-lesioned controls. The shifts for anterior and
posterior PVT incomplete lesions were as follows: at CT6,
1.9 ± 14.6 and 10 ± 6.2; at CT12, 109 ± 6.1 and 105 ± 10.7; and at CT23, 95 ± 29.4 and 86.7 ± 4.1.
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Experiment 2
The electrode tract was found within the boundaries of the anterior part of PVT in eight animals (Fig. 4,
). In the remaining rat, the
electrode was found lateral to the nucleus and was discarded from the
experiment (Fig. 4, *). The effects of the electrical stimulation of
PVT and the sham manipulation at the three circadian times studied are
summarized in Fig. 5. No effects on the
phase of the free running rhythm were found after the sham
manipulations at any of the circadian times nor after electrical
stimulation of PVT at CT6. In contrast, electrical
stimulation of PVT at CT12 and CT23 induced,
respectively, significant phase delays (78.5 ± 7.9 min) and
phase advances (91.8 ± 6.9 min), with a magnitude similar to
those induced by light pulses in intact animals (see Fig. 3) in
comparison to the sham manipulations at such times [F(1,7) = 58.2, P < 0.0001; Tukey P < 0.05].
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Experiment 3
The tip of the injection cannula was found within the anterior PVT in 23 of 27 implanted animals (Fig. 4,
) as follows: in seven
animals from the group injected at CT6 and in eight animals from each of the groups studied at CT12 and CT23,
respectively. In the remaining four animals, the tip of the cannula was
found lateral or ventral to the PVT and was discarded from the
experiment (Fig. 4, 
). Also, one animal from each of the groups
injected at CT12 and CT23 was randomly selected
and discarded from the study to have an equal number of animals
(n = 7) in each group.
The effect of glutamate or vehicle administration on the phase of the
free running rhythm at the three circadian times under study is
summarized in Fig. 6. No phase shifts
were found after injection of vehicle at any of the circadian times or
after the injection of glutamate at CT6. In contrast,
injection of glutamate at CT12 induced phase delays
(97.5 ± 8 min), whereas glutamate at CT23 induced
phase advances (77 ± 9.3 min); such effects were statistically
significant compared with the effects of vehicle administered at the
same circadian times [F(2,18) = 23.2, P < 0.0001; Tukey P < 0.05].
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Present data indicate that inputs to the SCN arising from the anterior portion of PVT play an important role in the shape of the PRC to light of drinking rhythm in rats kept under DD. Electrolytic lesion of anterior PVT results in atypical phase delays induced by light pulses during late subjective night (CT23) instead of the phase advances found at this circadian time in sham-lesioned animals. This effect was specific of lesions of the anterior PVT that project to the SCN, because neither lesions of the midposterior PVT nor lesions sparing most of the anterior PVT affected the phase shifts. Although the mechanism involved in such effect remains to be studied, we may speculate that PVT inputs to the SCN enable the mechanisms affected by light during late subjective night, which are involved in the phase advances in SCN neurons.
In the present study, we did not find differences in the free running period in constant darkness among sham, anterior, and midposterior PVT-lesioned rats. A previous study with blinded rats indicated that lesions of anterior PVT lengthen the free running period of locomotor activity in constant darkness and shift the density of activity bouts toward the late subjective night (26). In contrast, electrolytic lesions of anterior PVT in hamsters do not alter the free running period of locomotor activity in constant darkness (12). Such differences were attributed either to the differences in organization of the circadian system between these species or to the absence of retinal inputs to the SCN. Present results support the notion that changes in period found in the previous study may be due to the lack of retinal inputs.
In other rodents such as hamsters and mice, inputs to the SCN arising from the intergeniculate leaflet and the median raphe nucleus (MRN) participate with opposite effects in the entrainment of circadian rhythmicity by modulating the response of SCN neurons to light. Lesion of the intergeniculate leaflet decreases phase advances to light pulses, shortens the free running period, reduces the incidence of splitting in constant light, and prevents the lengthening of free running period induced by increasing illumination (17). On the other hand, lesion of serotoninergic neurons in the MRN increases phase delays induced by light pulses, increases the incidence of splitting in constant light, and lengthens the free running period in constant light (29, 30). Such studies indicate that inputs arising from intergeniculate leaflet increase the response of SCN to light, whereas inputs arising from the MRN decrease this response. Present findings indicate that PVT projections to the SCN are at least partially involved in setting the direction of the phase shift of the circadian pacemaker to light. Further studies are needed to characterize the effects of light at other circadian times to clarify whether phase advances occur at other times or are absent in PVT-lesioned animals.
Electrical or chemical stimulation of the anterior PVT at the three characteristic circadian times of the PRC produced similar phase responses as those obtained by light. Because glutamate receptors are not present in fibers on passage, shifts found after glutamate stimulation of PVT indicate that these effects are due to activation of PVT neurons rather than to activation of fibers running through the stimulated area. Excitatory amino acid input to the SCN from PVT has previously been suggested from studies showing retrograde transport to PVT neurons of D-[3H]aspartate injected into the SCN in hamsters (11) and rats (24). Thus it is possible that phase responses induced by PVT stimulation may be due to release of excitatory amino acids in the SCN from fibers arising from the anterior PVT, because it is widely accepted that excitatory amino acids, most likely N-acetylaspartylglutamate, from retinal ganglion cells are neurotransmitters involved with the response of SCN neurons to light (29).
Phase shifts in circadian rhythmicity induced by electrical or chemical stimulation of PVT differ from those shifts induced by stimulation of other SCN inputs. Electrical stimulation of the intergeniculate leaflet (35) or stimulation of the SCN with neuropeptide Y (2), which is released in the SCN from fibers arising from the intergeniculate leaflet, induces a nonphotic (or dark pulse) type of PRC. Electrical stimulation of the raphe (23) or stimulation of the SCN with agonists to serotonin, which is released from fibers originated from the MRN, induces a nonphotic type of PRC via serotonin receptors (7-9, 13, 34). In contrast, others found a PRC similar to that induced by light pulses but with systemic administration of quipazine, a nonselective agonist to serotonin receptors (19, 21, see Ref. 30 for a review). It is clear that activation of different receptors in SCN neurons has selective effects on the phase of the pacemaker, which depends not only of the chemical signal involved but also on the status of the pacemaker at the time at which the stimulus is presented.
PVT has been implicated in visceral and autonomic functions (5, 16). In particular, the role in the control of some aspects of the sleep-wake states has been suggested from the dense innervation of this nucleus by the locus ceruleus and the raphe nuclei (4, 18, 22, 28) as well as the conspicuous expression of c-fos during wakefulness in both nocturnal and diurnal animals (31, 32). The present study clearly indicates the participation of the anterior PVT in the nonparametric entrainment of circadian rhythms to light. The results suggest that integrity of the anterior PVT is necessary for an adequate response of the pacemaker to light during late subjective night. It remains to be established whether PVT acts directly on SCN neurons or presynaptically on the terminals of the retinohypothalamic tract as well as the nature of the transmitter(s) involved. Furthermore, present data also suggest that anterior PVT inputs to the SCN may induce phase shifts in the pacemaker by acting through a similar neurochemical system as that involved in the response to light pulses.
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ACKNOWLEDGEMENTS |
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We thank J. L. Chavez for skillful technical assistance.
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FOOTNOTES |
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This study was supported by grants from Consejo Nacional de Ciencia y Tecnología (33034-N), Dirección General de Asuntos del Personal Académico de la Universidad Nacional Autónoma de México (IN-204800), and Omnilife 2000.
Address for reprint requests and other correspondence: R. Aguilar-Roblero, Neurociencias, IFC/UNAM, Apartado Postal 70-253, México D. F. 04510, Mexico (E-mail: raguilar{at}ifisiol.unam.mx).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
July 8, 2002;10.1152/ajpregu.00259.2002
Received 10 May 2002; accepted in final form 28 June 2002.
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TOP
ABSTRACT
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MATERIALS AND METHODS
RESULTS
DISCUSSION
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