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Distinct retinohypothalamic innervation patterns predict the developmental emergence of species-typical circadian phase preference in nocturnal Norway rats and diurnal nile grass rats
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Distinct retinohypothalamic innervation patterns predict the developmental emergence of species-typical circadian phase preference in nocturnal Norway rats and diurnal nile grass rats

William D Todd, Andrew J Gall, Joshua A Weiner and Mark S Blumberg
Journal of comparative neurology (1911), Vol.520(14), pp.3277-3292
10/01/2012
DOI: 10.1002/cne.23098
PMCID: PMC3676184
PMID: 22431036
url
https://doi.org/10.1002/cne.23098View
Published (Version of record) Open Access

Abstract

How does the brain develop differently to support nocturnality in some mammals, but diurnality in others? To answer this question, one might look to the suprachiasmatic nucleus (SCN), which is entrained by light via the retinohypothalamic tract (RHT). However, because the SCN is more active during the day in all mammals studied thus far, it alone cannot determine circadian phase preference. In adult Norway rats (Rattus norvegicus), which are nocturnal, the RHT also projects to the ventral subparaventricular zone (vSPVZ), an adjacent region that expresses an in-phase pattern of SCN-vSPVZ neuronal activity. In contrast, in adult Nile grass rats (Arvicanthis niloticus), which are diurnal, an anti-phase pattern of SCN-vSPVZ neuronal activity is expressed. We hypothesized that these species differences result in part from a weak or absent RHT-to-vSPVZ projection in grass rats. Here, using a developmental comparative approach, we assessed species differences in behavior, hypothalamic activity, and RHT anatomy. We report that a robust retina-to-vSPVZ projection develops in Norway rats around the end of the second postnatal week when nocturnal wakefulness and the in-phase pattern of neuronal activity emerge. In grass rats, however, such a projection does not develop and the emergence of the anti-phase pattern during the second postnatal week is accompanied by increased diurnal wakefulness. When considered within the context of previously published reports on RHT projections in a variety of species, the current findings suggest that how and when the retina connects to the hypothalamus differentially shapes brain and behavior to produce animals that occupy opposing temporal niches.
Paraventricular Hypothalamic Nucleus - physiology Vasoactive Intestinal Peptide - metabolism Retina - growth & development Age Factors Species Specificity Visual Pathways - cytology Male Suprachiasmatic Nucleus - physiology Paraventricular Hypothalamic Nucleus - cytology Visual Pathways - physiology Rats, Inbred BN - physiology Retina - cytology Suprachiasmatic Nucleus - cytology Female Sleep - physiology Visual Pathways - growth & development Proto-Oncogene Proteins c-fos - metabolism Rats Behavior, Animal - physiology Circadian Rhythm - physiology Photoperiod Retina - physiology Animals Pituitary Adenylate Cyclase-Activating Polypeptide - metabolism Suprachiasmatic Nucleus - growth & development Presynaptic Terminals - metabolism Wakefulness - physiology Paraventricular Hypothalamic Nucleus - growth & development

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