Duncan G. L. Innes

Sexually dimorphic spatial learning varies seasonally in two populations of deer mice

Spatial learning in photoperiodically induced breeding (reproductive) and non-breeding (non-reproductive) adult male and female deer mice (Peromyscus maniculatus) was examined in a Morris water-maze task. Sexually mature, adult male and female deer mice that were derived from either a mainland population (P. m. artemisiae) or an island population (P. m. angustus) were required to learn the spatial position of a hidden, submerged platform in a water maze. Deer mice were tested either during the breeding season (summer; long day photoperiod) or during the non-breeding season (winter; short day photoperiod) with a total of six blocks of four trials conducted in a single day. Retention was tested with two probe trials which occurred one and three days after acquisition. During the breeding season male spatial task acquisition was superior to female spatial task acquisition for both populations. In contrast, during the non-breeding season there were no significant sex differences in spatial acquisition for either population. This change in sexually dimorphic spatial learning was due to female spatial-performance decreasing from non-breeding season to the breeding season and male spatial-performance increasing over the same period. Both populations displayed similar seasonal variations in sexually dimorphic water-maze task performance. There were, however, overall population differences in water-maze task performance that were related to the ecology of the mice, with the insular mice displaying shorter latencies to reach the hidden platform than did the mainland deer mice.(ABSTRACT TRUNCATED AT 250 WORDS)

Sex and day-night differences in opiate-induced responses of insular wild deer mice, Peromyscus maniculatus triangularis

We examined the effects of mu and kappa opiate agonists on the day- and night-time nociceptive, locomotory and ingestive behaviors of an island population of wild male and female deer mice, Peromyscus maniculatus triangularis. The prototypical mu opiate agonist, morphine, had significant analgesic and locomotory effects, which were blocked by naloxone, and the specific delta opiate antagonist, ICI 154,129, respectively. The specific kappa opiate agonist, U-50,488, had significant analgesic actions and inhibitory effects on locomotor activity, as well as stimulating feeding. Significant day-night variations occurred in the analgesic and activity responses, with the mu and kappa opiate agonists having significantly greater effects at night. There were also prominent sex differences in responses; male deer mice displaying significantly greater levels of mu and kappa opiate-induced analgesia and alterations in activity than female animals. These sex differences in opiate-induced effects were most pronounced at night, female deer mice displaying reduced day-night rhythms of responsiveness. These results demonstrate the existence of significant day-night rhythms and sex differences in the mu and kappa opiate behavioral responses of a wild population of rodents.

Spatial learning in deer mice: Sex differences and the effects of endogenous opioids and 60 Hz magnetic fields

We examined the effects of brief exposure to weak 60 Hz extremely low frequency (ELF) magnetic fields and opioid systems on spatial behavior and learning in reproductive adult male and female deer mice, Peromyscus maniculatus. Sex differences were evident in spatial performance, with male deer mice displaying significantly better performance than female mice in the Morris water maze, whereby animals had to acquire and retain the location of a submerged hidden platform. Brief (maximum 5 min) exposure to weak (100 μT) 60 Hz magnetic fields during task acquisition significantly improved female performance, eliminating the sex differences in acquisition. The opiate antagonist, naltrexone, also improved female acquisition, though significantly less than the magnetic fields. These facilitatory effects involved alterations of “non-spatial” (task familiarization and reduction of related anxiety/aversive related behaviors) and possibly “spatial” aspects of the task. Enhancement of enkephalin activity with the enkephalinase inhibitor, SCH 34826, significantly reduced task performance by male deer mice. Both naltrexone and the 60 Hz magnetic fields attenuated the enkephalin mediated reductions of spatial performance. These findings indicate that brief exposure to 60 Hz magnetic fields can enhance water maze task acquisition by deer mice and suggest that these facilitatory effects on spatial performance involve alterations in opioid activity.

Sex differences in the effects of neuropeptide FF and IgG from neuropeptide FF on morphine- and stress-induced analgesia

There is evidence suggesting that the endogenous mammalian octapeptide FLFQPQRFamide (F8Fa or neuropeptide FF, NPFF) has modulatory effects on opioid-mediated analgesia in rodents. There is also substantial evidence for sex differences in opioid analgesia, whereby male rats and mice display greater levels of opioid-mediated analgesia than females. In the present study, determinations were made of the effects of NPFF and IgG from antiserum against NPFF on morphine- and restraint stress-induced opioid analgesia in male and female deer mice. Intracerebroventricular (ICV) administrations of NPFF (0.10-10 micrograms) reduced in a dose-dependent manner morphine- and stress-induced analgesia in both male and female mice, with NPFF having markedly greater antagonistic effects in the male than female mice. Additionally, ICV administrations of NPFF-IgG increased the levels of morphine- and stress-induced analgesia and significantly reduced basal nociceptive sensitivity in male mice, whereas, in female mice, NPFF-IgG had no significant effects on either opioid-mediated analgesia or nociceptive sensitivity. These results indicate that there are sex differences in the modulatory effects of NPFF on opioid-mediated analgesia.

Novelty-induced opioid analgesia in deer mice (Peromyscus maniculatus): sex and population differences

Exposure to a new environment elicited significant, naloxone (1.0 mg/kg) reversible analgesic responses in three different populations of deer mice; Peromyscus maniculatus artemisiae from the mainland, and P. m. angustus and P. m. triangularis from small marine islands. In all cases male deer mice displayed significantly greater levels of analgesia than females. In addition, the levels of analgesia were significantly greater in the insular than in the mainland populations. These results indicate that there are substantial sex and population differences in the novelty-induced analgesia displayed by natural and laboratory populations of deer mice.

Male scent-induced analgesia in the deer mouse, Peromyscus maniculatus: Involvement of benzodiazepine systems

Exposure to bedding taken from the soiled home cage of an isolated male resident elicited a significant increase in the nociceptive responses of male deer mice, Peromyscus maniculatus artemisiae, from mixed sex pairs. The analgesia induced by exposure to the male scent was insensitive to the opiate antagonist, naloxone, and was blocked by either pre- or post-olfactory exposure injections of the benzodiazepine antagonist, Ro 15-1788, or agonist, diazepam. This non-opioid analgesia was of brief duration (15-30 min) and rapid onset, being evident after 1 min of exposure to the olfactory cues. Bedding treated with the novel odor of peppermint also induced analgesia in the deer mice. This analgesia was opioid mediated, being blocked by naloxone and insensitive to the benzodiazepine manipulations. Exposure to either fresh bedding, or the soiled bedding of another mixed sex pair of deer mice, had no significant effect on nociception. These results indicate that exposure of male deer mice to the olfactory cues associated with a potentially threatening individual (dominant/aggressive isolated male) elicits an analgesic response that involves alterations in the activity of benzodiazepine systems.

Developmental changes in opiate-induced analgesia in deer mice: sex and population differences

We examined developmental changes in nociception and mu (morphine) and kappa (U-50,488) opiate-induced analgesia in male and female deer mice of two different populations; Peromyscus maniculatus artemisiae from a mainland region and P. m. angustus from a small island. Both populations displayed significant developmental changes in nociception and morphine (10 mg/kg) and U-50,488 (10 mg/kg)-induced analgesia. Basal thermal response latencies (nociceptive responses) and the levels of mu and kappa opiate-induced analgesia increased over 14-35 days of age, with maximum analgesic responses in adults (35+ days of age). In both of the populations, young (neonatal-weaning) male mice displayed significantly higher thermal response latencies and greater levels of naloxone (1.0 mg/kg) antagonized opiate-induced analgesia than young females. There were also population differences in the levels of analgesia, the insular mice displaying greater mu and lower kappa opiate-induced analgesic responses than the mainland animals. The population differences in mu and kappa opiate-induced analgesia were evident in young and adult mice of both sexes. These results show that there are significant sex and population differences in nociception and opiate-induced analgesia in young (neonatal-weaning) and adult deer mice.

Sex differences in the effects of Tyr-MIF-1 on morphine- and stress-induced analgesia

There is evidence suggesting that the endogenous tetrapeptide, Tyr-MIF-1 (Tyr-Prol-Leu-Gly-amide), has antagonistic or modulatory effects on opioid-mediated analgesia. There is also substantial evidence for sex differences in opioid effects, whereby male rodents display greater levels of opioid-mediated analgesia than females. In the present study, determinations were made of the effects of Tyr-MIF-1 on morphine- and restraint stress-induced opioid analgesia in adult male and female deer mice, Peromyscus maniculatus. Intraperitoneal treatment with Tyr-MIF-1 (0.10-10 mg/kg) reduced morphine- and stress-induced analgesia in both male and female mice, with Tyr-MIF-1 having markedly greater antagonistic effects in male than female mice. These results indicate that there are sex differences in the modulatory (antiopiate) effects of Tyr-MIF-1 on opioid-mediated analgesia.

Plasma Testosterone Levels Are Related to Various Aspects of Locomotor Activity in Wild-Caught Male Meadow Voles (Microtus pennsylvanicus)

The relationship between plasma testosterone levels and locomotor activity in wild-caught sexually mature male meadow voles (Microtus pennsylvanicus) was assessed in the laboratory. Several aspects of locomotor activity were monitored for 1 h on two consecutive days using the automated Digiscan activity monitoring system. Plasma testosterone levels were determined immediately following the second day of activity monitoring. Significant Pearson correlations were obtained between plasma testosterone levels and total distance traveled [r(10) = 0.55, p < 0.05] and amount of time spent in movement [r(10) - 0.55, p < 0.05] on the second day. The wild voles showed a reduction in activity levels from the first to the second day of activity monitoring, which is indicative of habituation to a novel environment. This study provides direct evidence for a significant correlation between laboratory measures of behavioral activity and plasma testosterone levels in a wild-caught rodent. These findings indicate that previous assessments of hormone-behavior relationships in laboratory-bred rodents are consistent with the relationship between hormones and behavior in wild rodents.

Sex differences in magnetic field inhibition of morphine-induced responses of wild deer mice, Peromyscus maniculatus triangularis

An exposure for 60 min to a 0.5 Hz weak rotating magnetic field (1.5-90 G) reduced the day-time locomotory and analgesic effects of morphine (10 mg/kg) in a wild population of deer mice. Peromyscus maniculatus triangularis. Females displayed significantly lower levels of morphine-induced responses and sensitivity to the inhibitory effects of the magnetic fields than did the males. These responses indicate that there are sex differences in the effects of weak magnetic fields on the opiate-mediated responses of a wild rodent, with males being more responsive to the magnetic stimuli than females.