title: Distinct retinohypothalamic innervation patterns predict the developmental emergence of species-typical circadian phase preference in nocturnal Norway rats and diurnal nile grass rats.
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.
authors.affiliation: Program in Behavioral and Cognitive Neuroscience, Department of Psychology, University of Iowa, Iowa City 52242, USA.
authors.forename: William D
authors.initials: WD
authors.lastname: Todd
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Gall
authors.forename: Joshua A
authors.initials: JA
authors.lastname: Weiner
authors.forename: Mark S
authors.initials: MS
authors.lastname: Blumberg
mesh_terms: D000367:Age Factors; D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D002940:Circadian Rhythm / Q000502:physiology*; D005260:Female; D008297:Male; D010286:Paraventricular Hypothalamic Nucleus / Q000166:cytology / Q000254:growth & development / Q000502:physiology*; D017440:Photoperiod; D051219:Pituitary Adenylate Cyclase-Activating Polypeptide / Q000378:metabolism; D017729:Presynaptic Terminals / Q000378:metabolism; D016760:Proto-Oncogene Proteins c-fos / Q000378:metabolism; D051381:Rats; D011914:Rats, Inbred BN / Q000502:physiology*; D012160:Retina / Q000166:cytology / Q000254:growth & development / Q000502:physiology*; D012890:Sleep / Q000502:physiology; D013045:Species Specificity; D013493:Suprachiasmatic Nucleus / Q000166:cytology / Q000254:growth & development / Q000502:physiology*; D014660:Vasoactive Intestinal Peptide / Q000378:metabolism; D014795:Visual Pathways / Q000166:cytology / Q000254:growth & development / Q000502:physiology*; D014851:Wakefulness / Q000502:physiology
chemical_list: D051219:Pituitary Adenylate Cyclase-Activating Polypeptide; D016760:Proto-Oncogene Proteins c-fos; D014660:Vasoactive Intestinal Peptide