Lesions of the Intergeniculate Leaflet Lead to a Reorganization in Circadian Regulation and a Reversal in Masking Responses to Photic Stimuli in the Nile Grass Rat

Gall, Andrew J.; Smale, Laura; Yan, Lili; Núñez, Antonio A.

doi:10.1371/journal.pone.0067387

Cited by 31 publications

(64 citation statements)

References 47 publications

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“…The effect of light intensity on alpha is likely to reflect masking, with light expanding the active period and darkness reducing it in a diurnal mammal. These results are similar to what we have seen previously in intact grass rats (Gall et al, 2013). …”

Section: Discussionsupporting

confidence: 93%

The contribution of the pineal gland on daily rhythms and masking in diurnal grass rats, Arvicanthis niloticus

Shuboni

Agha

Groves

et al. 2016

Behavioural Processes

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Melatonin is a hormone rhythmically secreted at night by the pineal gland in vertebrates. In diurnal mammals, melatonin is present during the inactive phase of the rest/activity cycle, and in primates it directly facilitates sleep and decreases body temperature. However, the role of the pineal gland for the promotion of sleep at night has not yet been studied in non-primate diurnal mammalian species. Here, the authors directly examined the hypothesis that the pineal gland contributes to diurnality in Nile grass rats by decreasing activity and increasing sleep at night, and that this could occur via effects on circadian mechanisms or masking, or both. Removing the pineal gland had no effect on the hourly distribution of activity across a 12:12 light-dark (LD) cycle or on the patterns of sleep-like behavior at night. Masking effects of light at night on activity were also not significantly different in pinealectomized and control grass rats, as 1 hr pulses of light stimulated increases in activity of sham and pinealectomized animals to a similar extent. In addition, the circadian regulation of activity was unaffected by the surgical condition of the animals. Our results suggest that the pineal gland does not contribute to diurnality in the grass rat, thus highlighting the complexity of temporal niche transitions. The current data raise interesting questions about how and why genetic and neural mechanisms linking melatonin to sleep regulatory systems might vary among mammals that reached a diurnal niche via parallel and independent pathways.

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Section: Discussionsupporting

confidence: 93%

The contribution of the pineal gland on daily rhythms and masking in diurnal grass rats, Arvicanthis niloticus

Shuboni

Agha

Groves

et al. 2016

Behavioural Processes

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“…These 28 animals were the same used in a previous report, which describes the behavioral effects of IGL lesions that also extended beyond the IGL (see [6] for surgical and histological details). Female grass rats do not exhibit estrous cycles in the laboratory [17], and do not differ from males in masking responses to light [3].…”

Section: Methodsmentioning

confidence: 99%

“…We recently showed that light pulses result in a significant reduction in activity levels following IGL lesions in diurnal grass rats ( Arvicanthis niloticus ), whereas control grass rats exhibit a significant increase in activity levels [6]. Therefore, destroying the IGL in these diurnal animals alters their masking patterns to resemble those of nocturnal animals.…”

Section: Introductionmentioning

confidence: 99%

“…Based on our earlier observations [6], we predicted that the SCN's response to light would be unaffected by the IGL lesions, since the effects of light on the period of activity rhythms was unaffected by IGL lesions. In addition, we predicted that one or more brain areas outside the SCN would exhibit a reversal in Fos expression following light pulses given to IGL-lesioned animals.…”

Section: Introductionmentioning

confidence: 99%

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Intergeniculate leaflet lesions result in differential activation of brain regions following the presentation of photic stimuli in Nile grass rats

Gall

Yan

Smale

et al. 2014

Neuroscience Letters

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The intergeniculate leaflet (IGL) plays an important role in the entrainment of circadian rhythms and the mediation of acute behavioral responses to light (i.e., masking). Recently, we reported that IGL lesions in diurnal grass rats result in a reversal in masking responses to light as compared to controls. Here, we used Fos as a marker of neural activation to examine the mechanisms by which the IGL may influence this masking effect of light in grass rats. Specifically, we examined the patterns of Fos activation in retinorecipient areas and in brain regions that receive IGL inputs following 1-h light pulses given during the early night in IGL-lesioned and sham-operated grass rats. Three patterns emerged: (1) IGL lesions had no effect on the Fos response to light, (2) IGL lesions resulted in a reversal in Fos responses to light, and (3) IGL lesions resulted in a lack of a Fos response to light. Of specific interest were the suprachiasmatic nucleus (SCN) and the olivary pretectal nucleus (OPT), both of which are retinorecipient and connect reciprocally with the IGL. Light-induced Fos expression in the SCN was unaffected by IGL lesions, whereas the OPT exhibited a significant reduction in Fos expression following a light pulse in animals with IGL lesions. Altogether, our results suggest that the OPT, but not the SCN, exhibits a reversal in Fos responses to light following IGL lesions that reverse masking responses in diurnal grass rats. Our results suggest that interconnections between the IGL and downstream brain areas (e.g., OPT) may play a role in determining the direction of the behavioral response to light.

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“…In addition, we recently provided evidence that the IGL and OPT are involved in the masking response to light in the diurnal grass rat (Gall et al, 2013;Gall et al, 2014). However, it is not yet known if the SCN or vSPVZ contributes to masking in diurnal species.…”

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confidence: 99%

Suprachiasmatic Nucleus and Subparaventricular Zone Lesions Disrupt Circadian Rhythmicity but Not Light-Induced Masking Behavior in Nile Grass Rats

et al. 2016

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The ventral subparaventricular zone (vSPVZ) receives direct retinal input and influences the daily patterning of activity in rodents, making it a likely candidate for the mediation of acute behavioral responses to light (i.e., masking). We performed chemical lesions aimed at the vSPVZ of diurnal grass rats (Arvicanthis niloticus) using N-methyl-D,L-aspartic acid (NMA), a glutamate agonist. Following NMA lesions, we placed grass rats in various lighting conditions (e.g., 12:12 light-dark, constant dark, constant light); presented a series of light pulses at circadian times (CT) 6, 14, 18, and 22; and placed them in a 7-h ultradian cycle to assess behavioral masking. Extensive bilateral lesions of the vSPVZ disrupted the expression of circadian rhythms of activity and abolished the circadian modulation of masking responses to light, without affecting light-induced masking behavior per se. We also found that in diurnal grass rats, NMA was capable of destroying not only neurons of the vSPVZ but also those of the suprachiasmatic nucleus (SCN), even though excitotoxins have been ineffective at destroying cells within the SCN of nocturnal rodents. The vulnerability of the grass rat's SCN to NMA toxicity raises the possibility of a difference in density of receptors for glutamate between nocturnal and diurnal species. In cases in which damage extended to the SCN, masking responses to light were present and similar to those displayed by animals with damage restricted to the vSPVZ. Thus, extensive bilateral lesions of the SCN and vSPVZ disrupted the expression of circadian rhythms without affecting acute responses to light in a diurnal species. Our present and previous results suggest that retinorecipient brain areas other than the SCN or vSPVZ, such as the intergeniculate leaflet or olivary pretectal nucleus, may be responsible for the mediation of masking responses to light in the diurnal grass rat.

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Lesions of the Intergeniculate Leaflet Lead to a Reorganization in Circadian Regulation and a Reversal in Masking Responses to Photic Stimuli in the Nile Grass Rat

Cited by 31 publications

References 47 publications

The contribution of the pineal gland on daily rhythms and masking in diurnal grass rats, Arvicanthis niloticus

The contribution of the pineal gland on daily rhythms and masking in diurnal grass rats, Arvicanthis niloticus

Intergeniculate leaflet lesions result in differential activation of brain regions following the presentation of photic stimuli in Nile grass rats

Suprachiasmatic Nucleus and Subparaventricular Zone Lesions Disrupt Circadian Rhythmicity but Not Light-Induced Masking Behavior in Nile Grass Rats

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