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Can Too Much Glutamate Change Circadian Rhythms

Written By Friday, April 1, 2022 Add Comment Edit

Accepted on 27 May 2021Submitted on 13 Mar 2021

ane. Introduction

Circadian rhythmicity is inherent to all organisms and is one of the main characteristics of biological systems. It is present in most biochemical and molecular processes, from the transcription of genes in cellular nuclei to the control of the jail cell bicycle [ ane ], and it participates considerably in physiological and behavioral mechanisms. In mammals, the suprachiasmatic nucleus (SCN) located in the anterior hypothalamus of the brain is considered the central circadian regulatory nucleus that responds to the environmental lite-nighttime cycle [ 2 ]. The cadre machinery of circadian rhythmicity in the SCN is a transcriptional-translational feedback loop of a set of clock genes [ 3 ].

Although the SCN is crucial for the generation of biological rhythms in mammals, the expression and regulation of clock genes are non unique to that nucleus. The rhythmic expression of the same clock genes that regulate the oscillator in the SCN is widely distributed among other areas of the brain and the spinal cord [ 4 ] and many peripheral cells and tissues, including the liver, intestine, middle, and retina [ v , half dozen ].

It is well established that communication betwixt neuronal circuits in the central nervous system is based on the interaction of diverse inhibitory, excitatory and modulatory synaptic influences; these influences are mediated by a series of neurotransmitters and neuromodulators. In many neuronal nuclei and centers in the encephalon, information technology has been demonstrated that several neurotransmitters evidence rhythmic variations in concentration [ vi ], but at that place is practically no experimental evidence about possible twenty-four hour period-night fluctuations in neurotransmitter levels in the spinal string. Knowledge of such variations coupled to a calorie-free-dark wheel could be of utmost importance for understanding the expression of sensory, nociceptive, proprioceptive, and motor processes in the spinal cord. In this study, we analyzed cyclic variations in the level of several neurotransmitters (glutamate, GLU [excitatory, seven ]; gamma-aminobutyric acid, GABA [inhibitory, 7 ]; dopamine, DA [inhibitory transmitter at the spinal level, viii ]); serotonin, SER [more often than not inhibitory, 9 ]; epinephrine, Eastward and norepinephrine, NE [both facilitate inhibitory and excitatory transmission in the spinal cord, ten , 11 ]) during a 12 h dark-12 h light cycle in the lumbar spinal cord of rats.

ii. Materials and methods

2.1 Animals and experimental pattern

Male Wistar rats, provided past our institutional fauna house, were accommodated in individual acrylic cages with ad libitum access to food and h2o and were maintained under a 12:12 h low-cal-dark cycle (lights on at half-dozen:00 AM) and controlled temperature (22 ± 1°C). At the historic period of lxx days, rats were sorted into six groups (n = 10 animals per group) and each group was randomly selected for sacrifice by cervical dislocation at 08:00, 12:00, 16:00, 20:00, 24:00 and 04:00 hours, twenty-four hours fourth dimension, and afterward decapitated. Then, their lumbar spinal string was extracted by negative pressure injection of saline applied with a 20 ml-syringe through the vertebral central culvert at the spinal sacral level (S2-S3). Experiments were conducted following the guidelines of the Mexican Official Norm (NOM-062-ZOO-1999) and National Institutes of Health Guide NIH Publication No. 8023 (revised in 1996) for the Care and Apply of Laboratory Animals and approved by the Institutional Bioethical Committee for Intendance and Handling of Laboratory Animals (UPEAL-Protocol 013-02, CINVESTAV).

2.2 Determination of endogenous amino acids (GLU and GABA) in the rat spinal cord

Samples of each spinal cord extract (10 mg) were subjected to sonication for xxx seconds, with an distension of 30%, homogenized with 200 µL of 30% methanol and centrifuged at 3,500 rpm for 5 min. The pellets were washed and resuspended in one N NaOH, and the amount of total protein in each sample was determined by the Bradford method.

The supernatant was analyzed with a high-pressure liquid chromatography (HPLC) system with electrochemical detection (ECD, Intro Antec Leyden). The separation of GABA (inhibitory neurotransmitter) and GLU (excitatory neurotransmitter) was achieved with a 2.1 × 50 mm dC18 column (Atlantis, Waters; mobile phase: 100 mM disodium hydrogen phosphate, twenty% methanol, 3.5% acetonitrile, pH 6.7, adjusted with phosphoric acid). Then, each neurotransmitter was measured past precolumn derivation and ECD. Briefly, a derivation was achieved by mixing 12 µL of working derivation reagent (vi.75 mg OPA, 2.5% methanol, 1.25 µL two-b-mercaptoethanol and 97.5% 0.i M sodium tetraborate buffer) with thirty µL of filtered supernatant (nylon membrane/0.45 µm pore size). The derivation was detected with a burnished carbon electrode (VT-03 Antec Leyden) set at ± 550 mV.

ii.3 Determination of endogenous catecholamines (DA, SER, E and NE) in the rat spinal cord

The spinal cord tissue was homogenized in 200 µL of perchloric acid per sample and centrifuged at 3,500 rpm for five min. The pellets were washed and resuspended in 1 Due north NaOH, and the corporeality of full protein in each sample was determined by the Bradford method. The catecholamine concentration in the sample supernatant was analyzed by HPLC and fluorescence detection (excitation/emission = 279/320 nm, Waters 2475 Multiλ Fluorescence Detector, Waters Corporation). The samples were passed through a C18 column (Supelco, Sigma Aldrich). The mobile stage was 9.48 mg/L monochloroacetic acid, 189 mg/50 EDTA, 166 mg/L i-octane sulfonic acid, and iv.5% acetonitrile, pH 3.ii, adapted with NaOH. The chromatograms were processed by using Empower Software, Us.

two.iv Data analysis

Data are expressed equally the amount of neurotransmitter (ng) per milligram of protein present in tissue sample extracts. The concentration of each neurotransmitter per hour was averaged (±S.E.1000., north = 10). Rhythmic oscillation parameters (acrophase, mesor, null-amplitude and percent of rhythmicity) were adamant with the cosinor examination past using R software, v.iii.6, which established the best adjustment of data to a sinusoidal waveform. Because the cosinor exam adjusted the experimental data to a sinusoidal waveform, we decided to use the F test and Pearson'south correlation coefficient (r) to appraise the fettle of the sinusoidal curve with the experimentally obtained concentration values of each neurotransmitter. In improver, to institute a possible synchronization betwixt the day-night variations in the concentration of the different neurotransmitters analyzed, Pearson'due south correlation coefficient was calculated betwixt pairs of neurotransmitters. For graphic construction, we used the data processed with Chronos Fit software [ 12 ]. Differences between time points were analyzed by ane-way ANOVA, followed past the Pupil-Newman-Keuls mail service hoc multiple comparison analysis method (Sygma plot v12.0, Systat Software Inc.). In all cases, statistical significance was gear up at p < 0.05.

3. Results

3.1 Variations in the concentration of spinal GABA and glutamate during the day-night bicycle

GABA and glutamate in the lumbar spinal cord showed fluctuations in their levels that followed a sinusoidal curve during a light-dark bicycle (F test, p < 0.02; r(GABA) = 0.87 and r(GLU) = 0.88, respectively; Figure 1A ). The level of GABA began to increase at the middle function of the light phase and reached its maximal value in the dark phase at ~xx:00 h, almost one 60 minutes after the lights went off, while the lowest level of GABA was adamant at the 08:00 h fourth dimension point ( Figure 1A ). The mesor and nix-amplitude values were 33.68 and 26.02, respectively.

Figure one

Changes in neurotransmitter levels in the lumbar spinal cord of rats during a lite-dark cycle. A) Gamma-aminobutyric acid (GABA; open circles), B) glutamate (GLU; airtight circles), C) dopamine (DA; open triangles), D) serotonin (SER; airtight triangles), E) epinephrine (E; open squares) and F) norepinephrine (NE; closed squares). Values are the hateful ± S.E.M. for 8–10 rats. Cosinor fitting was significant in the GABA, GLU, DA, and SER concentration curves and experimental data (F test, p < 0.001) but not for the Due east and NE curves. The bar on the X centrality indicates the light and nighttime periods.

When comparison the GABA levels between time points, a pregnant difference between the values obtained at 08:00 and xx:00 h was establish (one-fashion ANOVA, p < 0.05, Student-Newman-Keuls postal service hoc exam). In the instance of GLU ( Effigy 1B ), variations in the detected level adjusted well to a 24 h sinusoidal bend (F test, p < 0.01; rGLU = 0.81), which was like to that of GABA ( Effigy 1A ). The highest value was obtained at 20:00 h, and the lowest level was obtained at 08:00 h. GLU had an acrophase value of nineteen:31 h and mesor and zero-aamplitude values of 214.four and 160.6, respectively. Significant differences in GLU levels were adamant between 08:00 h and 16:00 h and between 08:00 h and 20:00 h (one-style ANOVA, p < 0.05, Student-Newman-Keuls post hoc test). These results indicate that the concentration of GABA and GLU in the spinal cord varied during the light-dark bicycle.

3.2 Fluctuation of the spinal concentration of catecholamines during the light-nighttime bike

DA and SER followed a like sinusoidal function (rDA = 0.96 and rSER = 0.91; P = 0.037, cosinor function; Figure 1C and 1D ). The DA concentration reached its highest level during the light stage at 12:00 h, while the lowest level was observed at 20:00 h ( Figure 1C ). The rhythmic parameter acrophase reached a value of ii:44, and a mesor value of 2.67 and zilch-aamplitude of ii.04 was determined. Meaning differences in DA levels were found between time points 12:00 h and 20:00 h (one-fashion ANOVA, p < 0.05, Student-Newman-Keuls mail hoc test).

In the case of SER, the variation in its level in the spinal cord during a 12:12 calorie-free-night bicycle too followed a sinusoidal part (F, p < 0.02, r(SER) = 0.91; Figure 1D ). With the acrophase at x:xviii h, most four hours before the lights turned on, a mesor value of 55.06 and null-aamplitude of 23.72 were observed. These information indicated that the levels of DA and SER in the spine also showed a circadian variation of almost 24 h, but they appear to differ with respect to GABA and GLU sinusoidal curves past approximately 12 h ( Figure 1A and 1B ). In contrast, the levels of E and NE in the spine showed no meaning variations during the low-cal-dark bicycle (rE = 0.35 and rNE = 0.53; F test, p = 0.60 and p = 0.70, respectively), and as a consequence, they did non follow any sinusoidal variation.

3.3 Synchronization of fluctuations in neurotransmitter levels in the spine during the solar day-night bicycle

Due to the time grade similarities shown past the changes in the levels of GABA and GLU, DA and SER, just non E and NE, it is assumed that these neurotransmitters are correlated and highly synchronized. To explore the latter concept in this study, we determined the Pearson'south coefficient of correlation (r) of the averaged light-dark variations in the levels of the aforementioned pairs of neurotransmitters in the spine in this study. Table ane shows the r values calculated for all pairs of neurotransmitters analyzed. Only GABA-GLU and DA-SER pairs showed the largest r values (r > 0.nine), while the rest of the neurotransmitter pairs had relatively smaller r values (r < 0.6). These results could suggest that the levels of GABA-GLU and DA-SER neurotransmitter pairs fluctuate in a synchronized style in the spine during a day-night menses.

Tabular array ane

Pearson'due south coefficient of correlation values (r) for the concentration of pairs of neurotransmitters in the lumbar spinal cord of rats.

iv. Discussion

In this written report, nosotros found that the level of GABA, GLU, DA, and SER in the lumbar spinal string appears to fluctuate in a sinusoidal oscillation during a 12:12 light-nighttime bike, while the levels of E and NE do not seem to fluctuate in a circadian day-dark bicycle. GLU and GABA are two of the most abundant neurotransmitters in the central nervous system [ seven ]. Several studies have reported the presence of cyclic rhythms in the GLU system in the CNS, with a maximal nocturnal increase [ 13 ]. In fact, several studies accept demonstrated circadian rhythmicity in the expression of proteins related to glutamatergic neurotransmission, including NMDA receptor subunits and glutamate transporters [ fourteen ]. Such cyclic rhythm changes could influence the GLU-glutamine metabolic bicycle and the number of neurotransmitters released from glutamatergic synapses. Such influences could specially affect the chief afferent terminals ending in the spinal dorsal horn, and it could induce the variation in GLU concentration during a light-nighttime cycle (12:12), equally evidenced in this study.

In the case of GABA, it has been reported that the number of GABA-A receptors in the cerebral cortex fluctuates rhythmically, with their maximum value occurring at nighttime [ xv ]. Most importantly, it has been demonstrated that GABA in the SCN has an essential office in the regulation of cyclic rhythmicity and that the GABAergic system within the SCN region also exhibits circadian rhythmicity in rats [ sixteen , 17 ].

Brain monoamines, such every bit DA and SER, are involved in the regulation of several essential physiological functions, including the circadian rhythm. Information technology has been shown that DA receptors exert directly or indirect influences on circadian clock genes and proteins in several encephalon areas [ 18 ]. Schade and collaborators [ nineteen ] reported that in the nuclei accumbens and striatum, DA levels present a circadian rhythm with a maximal diurnal increment. Since most dopaminergic projections to the spinal cord originate from the hypothalamic A11 region [ 20 ], a probable synchronization between DA synthesis in the A11 region and between DA synthesis and the aggregating of DA in the lumbar spinal cord could be expected. Such a possibility could occur because our results indicate that DA levels in the lumbar spinal cord fluctuate rhythmically during a light-dark cycle, with a maximal peak occurring during the calorie-free stage. In addition, and in concordance with our results, Clemens and collaborators [ 21 ] showed that tyrosine hydroxylase, a charge per unit-limiting enzyme for the production of DA, presents higher levels during the day in comparison to levels present at dark in the spinal cord. Like to DA, SER levels vary rhythmically in the lumbar spinal cord across the light-nighttime cycle, demonstrating higher concentration values in the calorie-free flow.

Serotonergic descending axons originate from several nuclei in the brainstem, peculiarly from the ventrolateral periaqueductal gray nucleus and the nucleus raphe magnus, whose activation induces an antinociceptive effect in the spinal cord [ 22 ].

It is well known that neuronal ensembles in the lumbar spinal cord participate in an ample repertoire of sensory and motor processes, such as sensorial integration, pain, voluntary and nonvoluntary movements, posture and control of locomotion [ 23 ]; in the sensory and motor processes where these neuronal ensembles are involved, the participation of neurotransmitter systems has item relevance. In a previous study, it was determined that changes in forebrain SER levels during the lite-nighttime transition covaried significantly with changes in the levels of alert waking, a behavioral measure of the time spent in agile walking [ 24 ]. Co-ordinate to the latter, it is tempting to propose a possible relationship betwixt the light-dark variability in the level of neurotransmitters in the spine and the cyclic variations in pain sensitivity and locomotor activity.

In rats, sensitivity to hurting is modulated past neuronal and neurotransmitter ensembles in the spinal dorsal horn [ 25 ]. The expression of these ensembles varies in a low-cal-night blueprint, with a minimal sensitivity to pain at the transition from calorie-free to darkness and maximal sensitivity a few hours before the transition from darkness to low-cal [ 26 ]. Meanwhile, locomotor activeness is controlled by neural circuits (central pattern generators) located in intermediate and ventral regions of the spinal gray matter [ 27 ]. This activity increases during the nighttime phase and decreases in the light stage [ 28 ]. Co-ordinate to the latter, information technology could be assumed that both physiological processes, hurting sensitivity and locomotor action, are modulated by independent sets of neurons and neurotransmitters located in the dorsal and ventral spinal regions; these independent sets of neurons and transmitters seem to vary, but not in stage with the day-night bicycle.

Since our results were obtained by using the unabridged lumbar spinal cord, which prevented u.s.a. from discerning the occurrence of regional variations in the levels of neurotransmitters in the spine, we assume that the levels of neurotransmitters in the spine determined at each time indicate along a lite-night period was due to the sum of several sensory and motor neuronal processes that occur in the spinal cord at each fourth dimension point. Therefore, nosotros consider that it is not feasible to establish a close relationship between lite-night variations in the level of neurotransmitters of the entire spinal cord and variations in individual physiological processes or behaviors. To found this relationship, it would be necessary to apply an experimental epitome different from the one used in the present written report.

Regarding E and NE, to the best of our knowledge, there are practically no experimental reports in the literature about the cyclic rhythmicity of Eastward and NE in the spinal cord of mammals. Our results reveal that the spinal levels of these monoamine neurotransmitters do not have significant differences between time points during a light-dark bicycle, which is indicative of the possible absence of circadian rhythmicity in the level of E and NE in the spine. However, equally mentioned higher up, our results practice not let u.s. to exclude the possibility of the activation of 2 different sensory and/or motor processes that use NE and Due east as neurotransmitters in such mode that their algebraic sum may alter or cancel the lite-dark variation in NE and Eastward levels, every bit observed in this study. These processes would be located in the dorsal and ventral regions of the spinal cord, and occur in parallel but would be completely desynchronized (i.e., i increases the level of NE and Due east in the spine during the calorie-free phase and the other increases the level of NE and E during the dark stage). This possibility needs to be evaluated with experimental approaches other than those used in this written report.

Every bit pointed out in the Results section, the fourth dimension class similarities and high correlation values for the changes in spinal concentrations of GABA and GLU and of DA and SER are notable. Due to the latter, temporal synchronization betwixt the circadian clocks of both pairs of neurotransmitters could be proposed. It is possible that such temporal synchronization of neurotransmitter pairs could be related to the dynamic rest of excitation and inhibition that occurs in neuronal circuits, which has been considered essential for the proper functioning of the brain and spinal cord [ 29 , xxx ]. Withal, this proposal needs to exist analyzed with other experimental approaches to disclose the relative importance of the variations in the neurotransmitter concentration for neuronal communication in the spinal string.

Finally, information technology is important to highlight the need to evaluate the twenty-four hour period-dark variation in the expression of clock genes, neurotransmitter receptors, and transporters at the lumbar spinal string level to characterize the possible role of genetic and synaptic mechanisms in the physiological function of each of the neurotransmitters analyzed; moreover, such an evaluation could also reveal the possible routes of interaction between different circadian rhythms, such every bit those between the nucleus accumbens and the spinal cord.

5. Conclusions

The results obtained in this study demonstrate that the spinal concentration of GLU, GABA, DA, and SER vary during the 24 h day-night menstruation, indicating that they are subjected to synchronized circadian rhythms coupled to a light-dark wheel. In dissimilarity, Due east and NE levels do non seem to follow a circadian oscillation. Further studies are needed to evaluate the functional office of these light-dark fluctuations in the level of neurotransmitters in the spine that may influence the essential action of spinal neuronal ensembles and the expression of sensory and motor-related behaviors during a lite-dark cycle.

Acknowledgements

This work was partially supported by a PhD fellowship granted to Shantal Jiménez-Zárate by CONACyT and to I. Jiménez-Estrada from the Sistema Nacional de Investigadores (SNI-3491) México. We would like to thank Veronica Vargas and Cindy Xilonen Hinojosa for their excellent experimental help and American Periodical Experts for English grammar proofreading of the article.

Competing Interests

The authors have no competing interests to declare.

Writer Contributions

Jiménez-Zárate, Beatriz Shantal: Research, Methodology, data analysis, Writing – Original Draft. Piña Leyva, Celia: Dissection, data analysis. Rodríguez-Sánchez, Marina: HPLC measurements and data analysis. Florán Garduño Benjamín: Data analysis and discussion. Jiménez-Zamudio Luis Antonio: Planning of experiments and information analysis; Jiménez-Estrada Ismael: Conceptualization, planning of experiments, Supervision, Project direction, Funding, data assay, Writing – review & editing.

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