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Phase shifting capacity of the circadian pacemaker determined by the SCN neuronal network organization.

vanderLeest HT, Rohling JH, Michel S, Meijer JH - PLoS ONE (2009)

Bottom Line: The effects of light on the circadian system are strongly dependent on the photoperiod to which animals are exposed.Application of N-methyl-D-aspartate (NMDA) induced sustained increments in electrical activity that were not significantly different in the slices from long and short photoperiods.We conclude that the photoperiodic dependent phase responses are determined by the SCN and propose that synchronization among SCN neurons enhances the phase shifting capacity of the circadian system.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Cell Biology, Laboratory for Neurophysiology, Leiden University Medical Center, Leiden, The Netherlands.

ABSTRACT

Background: In mammals, a major circadian pacemaker that drives daily rhythms is located in the suprachiasmatic nuclei (SCN), at the base of the hypothalamus. The SCN receive direct light input via the retino-hypothalamic tract. Light during the early night induces phase delays of circadian rhythms while during the late night it leads to phase advances. The effects of light on the circadian system are strongly dependent on the photoperiod to which animals are exposed. An explanation for this phenomenon is currently lacking.

Methodology and principal findings: We recorded running wheel activity in C57 mice and observed large amplitude phase shifts in short photoperiods and small shifts in long photoperiods. We investigated whether these different light responses under short and long days are expressed within the SCN by electrophysiological recordings of electrical impulse frequency in SCN slices. Application of N-methyl-D-aspartate (NMDA) induced sustained increments in electrical activity that were not significantly different in the slices from long and short photoperiods. These responses led to large phase shifts in slices from short days and small phase shifts in slices from long days. An analysis of neuronal subpopulation activity revealed that in short days the amplitude of the rhythm was larger than in long days.

Conclusions: The data indicate that the photoperiodic dependent phase responses are intrinsic to the SCN. In contrast to earlier predictions from limit cycle theory, we observed large phase shifting responses in high amplitude rhythms in slices from short days, and small shifts in low amplitude rhythms in slices from long days. We conclude that the photoperiodic dependent phase responses are determined by the SCN and propose that synchronization among SCN neurons enhances the phase shifting capacity of the circadian system.

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Acute responses in multiunit electrical activity to NMDA application at CT15.(A, B) NMDA application (10 µM) at CT 15 induced an increase in firing rate that was recorded by extracellular multiunit electrodes. The magnitude of the NMDA response is similar in slices from long and short day animals and in both photoperiods, a plateau was reached during the application. (C) The magnitude of the acute response to NMDA, measured as the relative increase in discharge rate, was not different between day lengths (p>0.3).
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pone-0004976-g003: Acute responses in multiunit electrical activity to NMDA application at CT15.(A, B) NMDA application (10 µM) at CT 15 induced an increase in firing rate that was recorded by extracellular multiunit electrodes. The magnitude of the NMDA response is similar in slices from long and short day animals and in both photoperiods, a plateau was reached during the application. (C) The magnitude of the acute response to NMDA, measured as the relative increase in discharge rate, was not different between day lengths (p>0.3).

Mentions: NMDA induced a sustained increment in SCN electrical discharge in slices from both photoperiods (Figure 3). The relative increase in electrical activity was 32.2±9.1% (n = 5) of baseline discharge in short days and 43.9±8.0% (n = 5) of baseline discharge in long days. No significant differences in responsiveness to NMDA were observed (p>0.1). Despite the similarity in acute NMDA responses, the resulting phase shifts were significantly larger in short days (−3.2±0.50 h, 6 control and 5 experimental slices) compared to long days (0.0±0.89 h, 6 control and 5 experimental slices; p<0.006; Figure 2). We also calculated the phase shift based on a secondary phase marker, the time of half maximum value on the rising slope of the electrical discharge peak. With this phase marker we found the same difference in phase shift between long and short day length, indicating the robustness of the measured differences in phase shift (difference in phase shift between day lengths: 3.2±0.86 h; p<0.002).


Phase shifting capacity of the circadian pacemaker determined by the SCN neuronal network organization.

vanderLeest HT, Rohling JH, Michel S, Meijer JH - PLoS ONE (2009)

Acute responses in multiunit electrical activity to NMDA application at CT15.(A, B) NMDA application (10 µM) at CT 15 induced an increase in firing rate that was recorded by extracellular multiunit electrodes. The magnitude of the NMDA response is similar in slices from long and short day animals and in both photoperiods, a plateau was reached during the application. (C) The magnitude of the acute response to NMDA, measured as the relative increase in discharge rate, was not different between day lengths (p>0.3).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2655235&req=5

pone-0004976-g003: Acute responses in multiunit electrical activity to NMDA application at CT15.(A, B) NMDA application (10 µM) at CT 15 induced an increase in firing rate that was recorded by extracellular multiunit electrodes. The magnitude of the NMDA response is similar in slices from long and short day animals and in both photoperiods, a plateau was reached during the application. (C) The magnitude of the acute response to NMDA, measured as the relative increase in discharge rate, was not different between day lengths (p>0.3).
Mentions: NMDA induced a sustained increment in SCN electrical discharge in slices from both photoperiods (Figure 3). The relative increase in electrical activity was 32.2±9.1% (n = 5) of baseline discharge in short days and 43.9±8.0% (n = 5) of baseline discharge in long days. No significant differences in responsiveness to NMDA were observed (p>0.1). Despite the similarity in acute NMDA responses, the resulting phase shifts were significantly larger in short days (−3.2±0.50 h, 6 control and 5 experimental slices) compared to long days (0.0±0.89 h, 6 control and 5 experimental slices; p<0.006; Figure 2). We also calculated the phase shift based on a secondary phase marker, the time of half maximum value on the rising slope of the electrical discharge peak. With this phase marker we found the same difference in phase shift between long and short day length, indicating the robustness of the measured differences in phase shift (difference in phase shift between day lengths: 3.2±0.86 h; p<0.002).

Bottom Line: The effects of light on the circadian system are strongly dependent on the photoperiod to which animals are exposed.Application of N-methyl-D-aspartate (NMDA) induced sustained increments in electrical activity that were not significantly different in the slices from long and short photoperiods.We conclude that the photoperiodic dependent phase responses are determined by the SCN and propose that synchronization among SCN neurons enhances the phase shifting capacity of the circadian system.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Cell Biology, Laboratory for Neurophysiology, Leiden University Medical Center, Leiden, The Netherlands.

ABSTRACT

Background: In mammals, a major circadian pacemaker that drives daily rhythms is located in the suprachiasmatic nuclei (SCN), at the base of the hypothalamus. The SCN receive direct light input via the retino-hypothalamic tract. Light during the early night induces phase delays of circadian rhythms while during the late night it leads to phase advances. The effects of light on the circadian system are strongly dependent on the photoperiod to which animals are exposed. An explanation for this phenomenon is currently lacking.

Methodology and principal findings: We recorded running wheel activity in C57 mice and observed large amplitude phase shifts in short photoperiods and small shifts in long photoperiods. We investigated whether these different light responses under short and long days are expressed within the SCN by electrophysiological recordings of electrical impulse frequency in SCN slices. Application of N-methyl-D-aspartate (NMDA) induced sustained increments in electrical activity that were not significantly different in the slices from long and short photoperiods. These responses led to large phase shifts in slices from short days and small phase shifts in slices from long days. An analysis of neuronal subpopulation activity revealed that in short days the amplitude of the rhythm was larger than in long days.

Conclusions: The data indicate that the photoperiodic dependent phase responses are intrinsic to the SCN. In contrast to earlier predictions from limit cycle theory, we observed large phase shifting responses in high amplitude rhythms in slices from short days, and small shifts in low amplitude rhythms in slices from long days. We conclude that the photoperiodic dependent phase responses are determined by the SCN and propose that synchronization among SCN neurons enhances the phase shifting capacity of the circadian system.

Show MeSH