Response properties of avian hippocampal formation cells in an environment with unstable goal locations.

The response properties of 48 right (n=24) and left (n=24) hippocampal formation (HF) cells were examined by recording from freely moving homing pigeons as they foraged in an open-field environment with unstable goal locations. Compared to previous results based on HF recordings from environments with stable goal locations, the spatial signal of the HF neurons recorded in the present study was substantially diminished; there was little indication of PATH cells found in previous HF recordings and nothing resembling place cells routinely recorded in rat hippocampus under similar conditions. However, lateralized response properties were detected. Right HF cells dramatically reduced their firing rates during a foraging session, resulting in very low reliability scores. By contrast, left HF cells maintained firing rates throughout sessions and displayed modestly higher reliability scores compared to right HF neurons. Notable was one striking group of cells (n=13), predominantly found in the right HF, that displayed rate maps characterized by numerous, discrete areas of above baseline firing rates, overall very low firing rates and higher specificity than other cells recorded in this study. Overall, the data emphasize the importance of stable goal locations in shaping the spatial response profile of homing pigeon HF neurons and demonstrate the persistence of lateralized response properties under conditions when space explains little of the temporal variation in firing rate.

Gonadal hormone effects on entrained and free-running circadian activity rhythms in the developing diurnal rodent Octodon degus.

The slowly maturing, long-lived rodent Octodon degus (degu) provides a unique opportunity to examine the development of the circadian system during adolescence. These studies characterize entrained and free-running activity rhythms in gonadally intact and prepubertally gonadectomized male and female degus across the first year of life to clarify the impact of sex and gonadal hormones on the circadian system during adolescence. Gonadally intact degus exhibited a delay in the phase angle of activity onset (Psi(on)) during puberty, which reversed as animals became reproductively competent. Gonadectomy before puberty prevented this phase delay. However, the effect of gonadal hormones during puberty on Psi(on) does not result from changes in the period of the underlying circadian pacemaker. A sex difference in Psi(on) and free-running period (tau) emerged several months after puberty; these developmental changes are not likely to be related, since the sex difference in Psi(on) emerged before the sex difference in tau. Changes in the levels of circulating hormones cannot explain the emergence of these sex differences, since there is a rather lengthy delay between the age at which degus reach sexual maturity and the age at which Psi(on) and tau become sexually dimorphic. However, postnatal exposure to gonadal hormones is required for sexual differentiation of Psi(on) and tau, since these sex differences were absent in prepubertally gonadectomized degus. These data suggest that gonadal hormones modulate the circadian system during adolescent development and provide a new model for postpubertal sexual differentiation of a central nervous system structure.

Odor-facilitated reentrainment in male and female juvenile Octodon degus.

The social, diurnal rodent, Octodon degus, exhibits faster reentrainment rates of circadian activity when exposed to olfactory social cues from females already entrained to the new light cycle (donors) during reentrainment after a phase shift of the light:dark (LD) cycle. However, adult degus display sex differences in the use of olfactory stimuli to accelerate reentrainment, with intact males requiring odors from at least two females for accelerated reentrainment, while odors from a single female are sufficient for faster recovery for females. In addition, adult gonadal hormones modulate responsiveness to the rate-enhancing olfactory stimuli. The present study examines responsiveness to reentrainment-accelerating odors in juvenile animals just prior to puberty. We report that the sex difference in sensitivity observed in adults is not evident in juveniles; both males and females, when exposed to odors from one unfamiliar adult, accelerated reentrainment of circadian activity after a 6-h phase-advance of the LD cycle. In conjunction with adult data, these results suggest that the sensitivity-reducing role of testosterone does not change across the life span, while the sensitivity-enhancing role of ovarian hormones in females occurs only post-pubertally.

Odor-specific effects on reentrainment following phase advances in the diurnal rodent, Octodon degus.

Reentrainment following phase shifts of the light-dark (LD) cycle is accelerated in Octodon degus in the presence of olfactory social cues (i.e., odors) produced by conspecifics. However, not all odors from conspecifics were effective in facilitating reentrainment after a phase advance. In the current experiments, we examined whether nonanimal odors, odors from another species, or conspecific odors, including those manipulated by steroid hormones, can cause the same increased reentrainment of wheel-running activity as odors from an intact, adult female degu. A variety of odors, each selected to probe a particular aspect of the reentrainment acceleration phenomenon, were presented to a group of phase-shifting female degus. The shifting females (test animals) responded to odors of intact, female degu donors with decreased reentrainment time, but odors of ovariectomized (OVX), OVX with a single hormone replacement capsule (estradiol or progesterone) or phase-shifting females had no effect. Multiple males were effective odor donors, whereas a single male was ineffective in earlier studies. Rats and cloves were not effective in accelerating reentrainment. Furthermore, odors from rats delayed reentrainment. We conclude that the odors that effectively accelerate degu reentrainment after a phase advance of the LD cycle are species specific. We also report that repeated phase shifts, followed by complete recovery of phase relationships, do not alter the rate of recovery from a phase shift over time. These data suggest that in O. degus, a social species, odors may reinforce and strengthen the salience of the photic zeitgeber and/or facilitate synchronization of rhythms between animals.

Ovarian hormones influence olfactory cue effects on reentrainment in the diurnal rodent, Octodon degus.

Octodon degus, a social hystricomorph rodent, responds to olfactory cues from a gonadally intact female entrained to a light-dark cycle (LD) by accelerating reentrainment of running wheel activity following a 6-h phase advance of the LD cycle. In this study, we examined the role of ovarian hormones in the production of and responsiveness to olfactory social cues in females. Experiment 1: intact females were sequentially phase-advanced 6 h with photic cues alone, or in the presence of an intact female donor, ovariectomized (OVX) donor, a castrated male, or a castrated male with testosterone replacement. Acceleration of reentrainment occurred only in the presence of the intact female donor while reentrainment was delayed by OVX donors. Experiment 2: OVX females undergoing a 6-h phase advance did not accelerate reentrainment in the presence of an intact female donor compared to reentrainment with photic cues alone. Thus, ovarian hormones are necessary for both the production of and responsiveness to olfactory cues. Experiment 3: OVX females implanted with estrogen-filled Silastic capsules did not accelerate reentrainment following the 6-h phase advance in the presence of an intact donor, whereas animals implanted with a combination of estrogen- and progesterone-filled capsules (Experiment 4) reduced the length of time needed to reentrain in the presence of an intact donor. Therefore, combined progesterone and estrogen are sufficient for responsiveness to the effective olfactory cue in intact donor females. These data clarify that the sex difference in sensitivity to non-photic odor effects on circadian reentrainment is caused by both the testosterone's inhibitory effects (Octodon degus. J. Biol. Rhythms 18 (2003) 43-50) and the enhancing effects of progesterone and estrogen.

Pubertal development of sex differences in circadian function: an animal model.

UNLABELLED: The development of adult circadian function, particularly sexual dimorphism of function, has been well studied only in rapidly developed rodents. In such species development is complete by weaning. Data from adolescent humans suggest that significant development occurs during the pubertal period. We hypothesized that a more slowly developing rodent might better mimic the changes in circadian function around puberty in humans and allow us to determine the underlying neural changes. Entrained and free-running circadian rhythms were analyzed and correlated with pubertal development in male and female Octodon degus (degu) that remained gonadally intact or were gonadectomized at weaning. Brains were collected during development to measure androgen and estrogen receptors in the suprachiasmatic nuclei (SCN) Adult circadian period does not develop until 10-12 months of age in degus, long after the onset of gonadal maturation (3-5 months). The timing of circadian period maturation correlates with the appearance of steroid receptors in the SCN. Changes in free-running rhythms only occurred in gonadally intact degus. Adult phase angles of activity onset develop between 2 and 3 months of age (comparing results of two experiments), soon after the onset of pubertal changes. CONCLUSION: The development of sexually dimorphic adult circadian period occurs after gonadal puberty is complete and requires the presence of gonadal steroids. The delay in development until after gonadal puberty is likely due to the delayed appearance of steroid receptors in the SCN. Phase is not sexually dimorphic and changes in the absence of steroid hormones.

Testosterone suppresses circadian responsiveness to social cues in the diurnal rodent Octodon degus.

The diurnal, social rodent Octodon degus displays a robust sex difference in the ability to use social cues to facilitate reentrainment following a phase advance of the light cycle. Adult females housed with a female social cue donor reentrained 25% to 40% faster than did females reentraining alone. However, reentrainment rates of males were unaffected by exposure to female social cues during reentrainment. The authors hypothesized that males were less sensitive to the reentrainment-enhancing effects of social cues and that their higher threshold to the stimuli could be overcome if the social cues were either increased in strength or salience. Housing a male with two females significantly shortened the time to reentrain following a 9-h phase advance (p = 0.002). Housing with a sister had no effect on reentrainment. Therefore, male degus are able to respond to social cues but require the stimulus to be stronger than that for females. The effect of testosterone was tested by comparing reentrainment rates of castrated males before and after testosterone replacement both with and without a female social cue donor. Castrated males responded to a single female social cue donor, reentraining 35% faster than when housed alone (p = 0.006), whereas the time to reentrainment of intact males and males with testosterone capsule implants did not differ. Intact females were also implanted with testosterone and phase shifted with and without donors. Testosterone treatment eliminated the increase in reentrainment rates in the presence of social cues. The authors conclude that the rate of recovery from odor-enhanced phase shifts is modulated by activational effects of testosterone in male degus. Testosterone is also effective in suppressing social cue responsiveness in females, suggesting that testosterone's effects on responsiveness are not sexually dimorphic. This hormonal effect likely occurs by altering sensory system functions or CNS response to sensory information.