Laura Smale

Mammalian Diurnality: Some Facts and Gaps

A major factor contributing to the evolution of mammals was their ability to be active during the night, a niche previously underused by terrestrial vertebrates. Diurnality subsequently reemerged multiple times in a variety of independent lineages. This paper reviews some recent data on circadian mechanisms in diurnal mammals and considers general themes that appear to be emerging from this work. Careful examination of behavioral studies suggests that although subtle differences may exist, the fundamental functions of the circadian system are the same, as seems to be the case with respect to the molecular mechanisms of the clock. This suggests that responses to signals originating in the clock must be different, either within the SCN or at its targets or downstream from them. Some features of the SCN vary from species to species, but none of these has been clearly associated with diurnality. The region immediately dorsal to the SCN, which receives substantial input from it, exhibits dramatically different rhythms in nocturnal lab rats and diurnal grass rats. This raises the possibility that it functions as a relay that transforms the signal emitted by the SCN and transmits different patterns to downstream targets in nocturnal and diurnal animals. Other direct targets of the SCN include neurons containing orexin and those containing gonadotropin-releasing hormone, and both of these populations of cells exhibit patterns of rhythmicity that are inverted in at least one diurnal compared to one nocturnal species. The patterns that emerge from the data on diurnality are discussed in terms of the implications they have for the evolution and neural substrates of a day-active way of life.

Destruction of the hamster serotonergic system by 5,7-DHT: effects on circadian rhythm phase, entrainment and response to triazolam

The role of the serotonergic system in the regulation of hamster circadian rhythms was analyzed using intraventricular injection of the selective neurotoxin, 5,7-dihydroxytryptamine (5,7-DHT). Sixty days after 5,7-DHT administration, immunoreactive serotonin in the forebrain, particularly the suprachiasmatic nuclei and intergeniculate leaflets, was severely depleted in 16 animals, moderately depleted in four and only slightly affected in four. 5,7-DHT produced an immediate and sustained advance of the onset of running wheel activity relative to the 24 h light-dark (LD) cycle. Activity onset occurred 0.7 +/- 0.07 h before lights out among 5,7-DHT-treated animals compared with 0.18 +/- 0.04 h after lights out for vehicle-infused controls. This new, advanced phase angle of entrainment was maintained throughout the 60-day period of the study while the animals remained in a LD cycle, including after an 8-h phase advance of the light cycle. 5,7-DHT treatment also delayed the offset of wheelrunning in 16 of 24 animals and reduced the likelihood of a smooth pattern of reentrainment to the shifted LD cycle. The drug treatment did not affect circadian period in constant darkness, the rate of reentrainment to an 8-h phase advance or the amount of wheelrunning activity per day. In addition, 5,7-DHT treatment had no effect on the ability of triazolam, a short-acting benzodiazepine, to accelerate the rate of reentrainment to an 8-h phase advance. These observations show that ascending projections of midbrain raphe serotonin neurons participate in the regulation of the circadian activity phase but are not required for triazolam-induced acceleration of reentrainment to a phase-advanced LD cycle.

Nocturnal and diurnal rhythms in the unstriped Nile rat, Arvicanthis niloticus

In a laboratory population of unstriped Nile grass rats, Arvicanthis niloticus, individuals with two distinctly different patterns of wheel-running exist. One is diurnal and the other is relatively nocturnal. In the first experiment, the authors found that these patterns are strongly influenced by parentage and by sex. Specifically, offspring of two nocturnal parents were significantly more likely to express a nocturnal pattern of wheel-running than were offspring of diurnal parents, and more females than males were nocturnal. In the second experiment, the authors found that diurnal and nocturnal wheel-runners were indistinguishable with respect to the timing of postpartum mating, which always occurred in the hours before lights-on. Here they also found that both juvenile and adult A. niloticus exhibited diurnal patterns of general activity when housed without a wheel, even if they exhibited nocturnal activity when housed with a wheel. In the third experiment, the authors discovered that adult female A. niloticus with nocturnal patterns of wheel-running were also nocturnal with respect to general activity and core body temperature when a running wheel was available, but they were diurnal when the running wheel was removed. Finally, a field study revealed that all A. niloticus were almost exclusively diurnal in their natural habitat. Together these results suggest that individuals of this species are fundamentally diurnal but that access to a running wheel shifts some individuals to a nocturnal pattern.

Projections of the suprachiasmatic nuclei, subparaventricular zone and retrochiasmatic area in the golden hamster

The patterns of projections from the hamster suprachiasmatic nucleus, retrochiasmatic area and subpraventricular hypothalamic zone were examined using anterograde tracing with the plant lectin, Phaseolus vulgaris leucoagglutinin. Suprachiasmatic nucleus efferents comprise four major fiber groups: (i) an anterior projection to the ventral lateral septum, the bed nucleus of the stria terminalis and anterior paraventricular thalmus; (ii) a periventricular hypothalamic projection extending from the preoptic region to the premammillary area; (iii) a lateral thalamic projection to the intergeniculate leaflet and ventral lateral geniculate; and (iv) a posterior projection to the posterior paraventricular thalamus, precommissural nucleus and olivary pretectal nucleus. The retrochiasmatic area showed a similar projection pattern with several major exceptions. There are projections to endopiriform cortex, fundus striati, ventral pallidum, horizontal limb of the nucleus of the diagonal band and three separate routes to the amygdala. There are also projections laterally with fibers of the supraoptic commissures, which enter the superior thalamic radiation and innervate the caudal dorsomedial thalamic nuclei. Other fibers traveling with the commissures terminate in the ventral zona incerta. The subparaventricular zone projects to most targets of the suprachiasmatic nucleus, but not to the intergeniculate leaflet. There is a substantial input to both the subparaventricular zone and retrochiasmatic area from the suprachiasmatic nucleus, but little apparent reciprocity. There is extensive overlap of suprachiasmatic nuclei and retrochiasmatic efferents, and between retrochiasmatic and known medial amygdaloid efferents. The anatomical information is discussed in the context of circadian rhythm regulation, photoperiodism and chemosensory pathways controlling male hamster reproductive behavior.

Patterns of Association among Female Spotted Hyenas (Crocuta crocuta)

We examined subgroup association patterns among adult female members of a clan of free-living spotted hyenas ( Crocuta crocuta ) and between adult females and their juvenile offspring during three consecutive stages of development of offspring. These stages represented the approximate periods of residence of offspring at the communal den, from 1 to 8 months of age, between leaving the communal den and weaning, from 8 to 14 months, and between weaning and reproductive maturity or dispersal, from 14 to 36 months of age. Mean association indices among adult female dyads varied with social rank, with the highest mean association index observed for the alpha female. Adult females associated more closely with their adult female kin than with unrelated adult females. Female kin from high-ranking matrilines associated more closely than did kin from lower-ranking matrilines. Within mother-offspring pairs, association patterns were strongly influenced by the mothers social rank during all three stages of development of offspring, with high-ranking mother-offspring dyads associating more tightly than low-ranking dyads at each stage. Mean mother-offspring association indices declined as offspring grew older, but we found no significant differences based on sex of offspring during any of the developmental stages examined.

Dispersal Status Influences Hormones and Behavior in the Male Spotted Hyena

Male spotted hyenas (Crocuta crocuta) reach puberty at 24 months of age and then invariably emigrate from their natal clans 1 to 38 months later. Thus there are two classes of reproductively mature males in every Crocuta clan: adult natal males born in the clan and adult immigrant males born elsewhere. In one free-living hyena population in Kenya, these two groups of males were compared with respect to measures of aggression, social dominance, sexual behavior, and circulating hormone levels. Adult natal males engaged in higher hourly rates of aggression than did immigrants, won all fights with immigrants, and were socially dominant to immigrants. In addition, adult natal males engaged in far lower hourly rates of sexual behavior with resident females than did immigrants, and natal males were never observed to copulate with natal females. Mean basal plasma cortisol values did not differ between the two groups of adult males, but cortisol concentrations in immigrants were positively correlated with tenure in the clan and with immigrant male social rank. Adult natal males had plasma testosterone levels significantly lower than those of immigrants. Social rank and plasma testosterone values were positively correlated among immigrant males. Thus two different relationships appear to exist between circulating testosterone and social rank in male Crocuta: one apparent in immigrants and the other in natal adult males. Our results suggest that dispersal might disinhibit testosterone secretion in postpubertal male hyenas.

Wheel-Running Rhythms in Arvicanthis niloticus

Wheel-running behaviour of the Nile grass rat, Arvicanthis niloticus, was studied under a variety of lighting conditions to characterize circadian rhythms in this species. A series of lighting schedules was used to determine the nature of entrainment, the rates of reentrainment after 6-h phase shifts, and the stability of free-running rhythms in constant light (LL) and constant dark (DD). All 15 individuals showed peaks of activity around dawn and dusk, 11 were more likely to run when lights were on and 4 were more likely to run when the lights were off. Three of the latter animals were completely crepuscular, but 1 showed a distinctly different and relatively nocturnal pattern, remaining active well into the dark phase. All 7 animals that were exposed to 6-h phase advances and delays reentrained to both shifts within 9 days. Stable and precise free-running rhythms were exhibited by all animals in LL and DD, and periods were longer in LL than DD. The ratio of the active to the inactive phase was significantly higher in LL than in DD or LD conditions. We conclude that A. niloticus exhibit predominantly diurnal running rhythms, with peaks of activity occurring around dawn and dusk, and that their rhythms are stable and precise and respond rapidly and predictably to changes in lighting conditions.

Dim Nighttime Light Impairs Cognition and Provokes Depressive-Like Responses in a Diurnal Rodent

Circadian disruption is a common by-product of modern life. Although jet lag and shift work are well-documented challenges to circadian organization, many more subtle environmental changes cause circadian disruption. For example, frequent fluctuations in the timing of the sleep/wake schedule, as well as exposure to nighttime lighting, likely affect the circadian system. Most studies of these effects have focused on nocturnal rodents, which are very different from diurnal species with respect to their patterns of light exposure and the effects that light can have on their activity. Thus, the authors investigated the effect of nighttime light on behavior and the brain of a diurnal rodent, the Nile grass rat. Following 3 weeks of exposure to standard light/dark (LD; 14:10 light [~150 lux] /dark [0 lux]) or dim light at night (dLAN; 14:10 light [~150 lux] /dim [5 lux]), rats underwent behavioral testing, and hippocampal neurons within CA1, CA3, and the dentate gyrus (DG) were examined. Three behavioral effects of dLAN were observed: (1) decreased preference for a sucrose solution, (2) increased latency to float in a forced swim test, and (3) impaired learning and memory in the Barnes maze. Light at night also reduced dendritic length in DG and basilar CA1 dendrites. Dendritic length in the DG positively correlated with sucrose consumption in the sucrose anhedonia task. Nighttime light exposure did not disrupt the pattern of circadian locomotor activity, and all grass rats maintained a diurnal activity pattern. Together, these data suggest that exposure to dLAN can alter affective responses and impair cognition in a diurnal animal.

A comparative analysis of the distribution of immunoreactive orexin A and B in the brains of nocturnal and diurnal rodents

BackgroundThe orexins (hypocretins) are a family of peptides found primarily in neurons in the lateral hypothalamus. Although the orexinergic system is generally thought to be the same across species, the orexins are involved in behaviors which show considerable interspecific variability. There are few direct cross-species comparisons of the distributions of cells and fibers containing these peptides. Here, we addressed the possibility that there might be important species differences by systematically examining and directly comparing the distribution of orexinergic neurons and fibers within the forebrains of species with very different patterns of sleep-wake behavior.MethodsWe compared the distribution of orexin-immunoreactive cell bodies and fibers in two nocturnal species (the lab rat, Rattus norvegicus and the golden hamster, Mesocricetus auratus) and two diurnal species (the Nile grass rat, Arvicanthis niloticus and the degu, Octodon degus). For each species, tissue from the olfactory bulbs through the brainstem was processed for immunoreactivity for orexin A and orexin B (hypocretin-1 and -2). The distribution of orexin-positive cells was noted for each species. Orexin fiber distribution and density was recorded and analyzed using a principal components factor analysis to aid in evaluating potential species differences.ResultsOrexin-positive cells were observed in the lateral hypothalamic area of each species, though there were differences with respect to distribution within this region. In addition, cells positive for orexin A but not orexin B were observed in the paraventricular nucleus of the lab rat and grass rat, and in the supraoptic nucleus of the lab rat, grass rat and hamster. Although the overall distributions of orexin A and B fibers were similar in the four species, some striking differences were noted, especially in the lateral mammillary nucleus, ventromedial hypothalamic nucleus and flocculus.ConclusionThe orexin cell and fiber distributions observed in this study were largely consistent with those described in previous studies. However, the present study shows significant species differences in the distribution of orexin cell bodies and in the density of orexin-IR fibers in some regions. Finally, we note previously undescribed populations of orexin-positive neurons outside the lateral hypothalamus in three of the four species examined.

Differences in the suprachiasmatic nucleus and lower subparaventricular zone of diurnal and nocturnal rodents

Diurnal and nocturnal species are profoundly different in terms of the temporal organization of daily rhythms in physiology and behavior. The neural bases for these divergent patterns are at present unknown. Here we examine functional differences in the suprachiasmatic nucleus (SCN) and one of its primary targets in a diurnal rodent, the unstriped Nile grass rat (Arvicanthis niloticus) and in a nocturnal one, the laboratory rat (Rattus norvegicus). Grass rats and laboratory rats were housed in a 12:12 light:dark cycle, and killed at six time points. cFos-immunoreactive rhythms in the SCN of grass rats and laboratory rats were similar to those reported previously, with peaks early in the light phase and troughs in the dark phase. However, cFos-immunoreactivity in the lower subparaventricular zone (LSPV) of grass rats rose sharply 5 h into the dark phase, and remained high through the first hour after light onset, whereas in laboratory rats it peaked 1 h after light onset and was low at all other sampling times. Daily cFos rhythms in both the SCN and the LSPV persisted in grass rats, but not in laboratory rats, after extended periods in constant darkness. In grass rats, the endogenous cFos rhythm in the LSPV, but not the SCN, was present both in calbindin-positive and in calbindin-negative cells. Cells that expressed cFos at night in the region of the LSPV in grass rats were clearly outside of the boundaries of the SCN as delineated by Nissl stain and immunoreactivity for vasopressin and vasoactive intestinal peptide. The LSPV of the grass rat, a region that receives substantial input from the SCN, displays a daily rhythm in cFos expression that differs from that of laboratory rats with respect to its rising phase, the duration of the peak and its dependence on a light/dark cycle. These characteristics may reflect the existence of mechanisms in the LSPV that enable it to modulate efferent SCN signals differently in diurnal and nocturnal species.