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Mice deficient of glutamatergic signaling from intrinsically photosensitive retinal ganglion cells exhibit abnormal circadian photoentrainment.

Purrier N, Engeland WC, Kofuji P - PLoS ONE (2014)

Bottom Line: The relative contribution of each neurotransmitter system for the circadian photoentrainment and other NIF visual responses is still unresolved.Other NIF responses such as the PLR and negative masking responses to light were also partially attenuated.Overall, these results suggest that glutamate from ipRGCs drives circadian photoentrainment and negative masking responses to light.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota, United States of America.

ABSTRACT
Several aspects of behavior and physiology, such as sleep and wakefulness, blood pressure, body temperature, and hormone secretion exhibit daily oscillations known as circadian rhythms. These circadian rhythms are orchestrated by an intrinsic biological clock in the suprachiasmatic nuclei (SCN) of the hypothalamus which is adjusted to the daily environmental cycles of day and night by the process of photoentrainment. In mammals, the neuronal signal for photoentrainment arises from a small subset of intrinsically photosensitive retinal ganglion cells (ipRGCs) that send a direct projection to the SCN. ipRGCs also mediate other non-image-forming (NIF) visual responses such as negative masking of locomotor activity by light, and the pupillary light reflex (PLR) via co-release of neurotransmitters glutamate and pituitary adenylate cyclase-activating peptide (PACAP) from their synaptic terminals. The relative contribution of each neurotransmitter system for the circadian photoentrainment and other NIF visual responses is still unresolved. We investigated the role of glutamatergic neurotransmission for circadian photoentrainment and NIF behaviors by selective ablation of ipRGC glutamatergic synaptic transmission in mice. Mutant mice displayed delayed re-entrainment to a 6 h phase shift (advance or delay) in the light cycle and incomplete photoentrainment in a symmetrical skeleton photoperiod regimen (1 h light pulses between 11 h dark periods). Circadian rhythmicity in constant darkness also was reduced in some mutant mice. Other NIF responses such as the PLR and negative masking responses to light were also partially attenuated. Overall, these results suggest that glutamate from ipRGCs drives circadian photoentrainment and negative masking responses to light.

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Related in: MedlinePlus

Vglut2-cKO mice exhibit abnormal entrainment to a skeleton photoperiod.Representative actograms from control (A) and Vglut2-cKO animals (B) under skeleton photoperiod light cycles (1 hour light pulses, 12 h apart). Control mice photoentrain to the 1-h light pulses and restrict their activity to one of the dark periods. Vglut2-cKO mice showed a variable degree of photoentrainment with some activity in both dark periods. Shaded regions of the activity records indicate periods of darkness.
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pone-0111449-g004: Vglut2-cKO mice exhibit abnormal entrainment to a skeleton photoperiod.Representative actograms from control (A) and Vglut2-cKO animals (B) under skeleton photoperiod light cycles (1 hour light pulses, 12 h apart). Control mice photoentrain to the 1-h light pulses and restrict their activity to one of the dark periods. Vglut2-cKO mice showed a variable degree of photoentrainment with some activity in both dark periods. Shaded regions of the activity records indicate periods of darkness.

Mentions: The variable circadian rhythmicity in DD for the Vglut2-cKO mice precluded us from performing light pulse experiments at defined circadian times to establish a phase response curve. Instead, to further evaluate circadian photoentrainment, we subjected the mice to a skeleton photoperiod in which light pulses of one hour duration were given 11 h apart to simulate dawn and dusk light exposure in nocturnal animals [28]. Under these conditions, it was expected that the locomotor activity would consolidate in one of the two dark periods between light pulses with inactivity in the opposite dark period. Indeed the control mice entrained to these light pulses with locomotor activity largely restricted to one of the dark periods (Figure 4A). The Vglut2-cKO mice, on the other hand, displayed variable photoentrainment with some mice showing extensive locomotor activity across both dark periods (Figure 4B).


Mice deficient of glutamatergic signaling from intrinsically photosensitive retinal ganglion cells exhibit abnormal circadian photoentrainment.

Purrier N, Engeland WC, Kofuji P - PLoS ONE (2014)

Vglut2-cKO mice exhibit abnormal entrainment to a skeleton photoperiod.Representative actograms from control (A) and Vglut2-cKO animals (B) under skeleton photoperiod light cycles (1 hour light pulses, 12 h apart). Control mice photoentrain to the 1-h light pulses and restrict their activity to one of the dark periods. Vglut2-cKO mice showed a variable degree of photoentrainment with some activity in both dark periods. Shaded regions of the activity records indicate periods of darkness.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4214747&req=5

pone-0111449-g004: Vglut2-cKO mice exhibit abnormal entrainment to a skeleton photoperiod.Representative actograms from control (A) and Vglut2-cKO animals (B) under skeleton photoperiod light cycles (1 hour light pulses, 12 h apart). Control mice photoentrain to the 1-h light pulses and restrict their activity to one of the dark periods. Vglut2-cKO mice showed a variable degree of photoentrainment with some activity in both dark periods. Shaded regions of the activity records indicate periods of darkness.
Mentions: The variable circadian rhythmicity in DD for the Vglut2-cKO mice precluded us from performing light pulse experiments at defined circadian times to establish a phase response curve. Instead, to further evaluate circadian photoentrainment, we subjected the mice to a skeleton photoperiod in which light pulses of one hour duration were given 11 h apart to simulate dawn and dusk light exposure in nocturnal animals [28]. Under these conditions, it was expected that the locomotor activity would consolidate in one of the two dark periods between light pulses with inactivity in the opposite dark period. Indeed the control mice entrained to these light pulses with locomotor activity largely restricted to one of the dark periods (Figure 4A). The Vglut2-cKO mice, on the other hand, displayed variable photoentrainment with some mice showing extensive locomotor activity across both dark periods (Figure 4B).

Bottom Line: The relative contribution of each neurotransmitter system for the circadian photoentrainment and other NIF visual responses is still unresolved.Other NIF responses such as the PLR and negative masking responses to light were also partially attenuated.Overall, these results suggest that glutamate from ipRGCs drives circadian photoentrainment and negative masking responses to light.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota, United States of America.

ABSTRACT
Several aspects of behavior and physiology, such as sleep and wakefulness, blood pressure, body temperature, and hormone secretion exhibit daily oscillations known as circadian rhythms. These circadian rhythms are orchestrated by an intrinsic biological clock in the suprachiasmatic nuclei (SCN) of the hypothalamus which is adjusted to the daily environmental cycles of day and night by the process of photoentrainment. In mammals, the neuronal signal for photoentrainment arises from a small subset of intrinsically photosensitive retinal ganglion cells (ipRGCs) that send a direct projection to the SCN. ipRGCs also mediate other non-image-forming (NIF) visual responses such as negative masking of locomotor activity by light, and the pupillary light reflex (PLR) via co-release of neurotransmitters glutamate and pituitary adenylate cyclase-activating peptide (PACAP) from their synaptic terminals. The relative contribution of each neurotransmitter system for the circadian photoentrainment and other NIF visual responses is still unresolved. We investigated the role of glutamatergic neurotransmission for circadian photoentrainment and NIF behaviors by selective ablation of ipRGC glutamatergic synaptic transmission in mice. Mutant mice displayed delayed re-entrainment to a 6 h phase shift (advance or delay) in the light cycle and incomplete photoentrainment in a symmetrical skeleton photoperiod regimen (1 h light pulses between 11 h dark periods). Circadian rhythmicity in constant darkness also was reduced in some mutant mice. Other NIF responses such as the PLR and negative masking responses to light were also partially attenuated. Overall, these results suggest that glutamate from ipRGCs drives circadian photoentrainment and negative masking responses to light.

Show MeSH
Related in: MedlinePlus