Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ELF :

extremely low frequency

Hz :

hertz

References

  • Able KP (1994) Magnetic orientation and magnetoreception in birds. Prog Neurobiol 42: 449–473

    Google Scholar 

  • Aloyo VJ, Romano AG, Harvey JA (1993) Evidence for an involvement of the μ-type of opioid receptor in the modulation of learning. Neuroscience 55: 511–519

    Google Scholar 

  • August PV, Ayvazian SG, Anderson JGT (1989) Magnetic orientation in a small mammal, Peromyscus leucopus. J Mammal 70: 1–9

    Google Scholar 

  • Beatty WW (1983) Opiate antagonists, morphine and spatial memory in rats. Pharmacol Biochem Behav 19: 397–401

    Google Scholar 

  • Betancur C, Dell'Omo G, Alleva E (1994) Magnetic field effects on stress-induced analgesia in mice: modulation by light. Neurosci Lett 182: 147–150

    Google Scholar 

  • Bovet J, Dolivo M, George C, Cogniati A (1988) Homing behavior of wood mice (Apodemus) in a geomagnetic anomaly. Z Saeugetierkd 53: 333–340

    Google Scholar 

  • Brocklehurst B, McLauchlan KA (1996) Free radical mechanisms for the effects of environmental electromagnetic fields on biological systems. Int J Radiat Biol 69: 3–24

    Google Scholar 

  • Bucci DJ, Chiba AA, Gallagher M (1995) Spatial learning in male and female Long-Evans rats. Behav Neurosci 109: 180–183

    Google Scholar 

  • Burda H, Marhold S, Westenberger T, Wiltschko R, Wiltschko W (1990) Evidence for magnetic compass orientation in the subterranean rodent Cryptomys hottentotus (Bathyergidae). Experientia 46: 528–530

    Google Scholar 

  • Canili T, Cook RG, Miczek KA (1990) Opiate antagonists enhance working memory of rats in the radial maze. Pharmacol Biochem Behav 36: 521–525

    Google Scholar 

  • Chipkin RE, Coffin VL (1991) Analgesic and acute central nervous system side effects of the intravenously administered enkephalinase inhibitor SCH 32615. Pharmacol Biochem Behav 38: 21–27

    Google Scholar 

  • Chipkin RE, Berger JE, Billard W, Iorio LC, Chapman R, Barnett A (1988) Pharmacology of SCH 34826, an orally active enkephalinase inhibitor. J Pharmacol Exp Ther 245: 829–838

    Google Scholar 

  • Corey DT (1978) The determination of exploration and neophobia. Neurosci Biobehav Rev 2: 235–253

    Google Scholar 

  • Desjardins C, Bronson FH, Blank JL (1986) Genetic selection for reproductive photoresponsiveness in deer mice. Nature 322: 172–173

    Google Scholar 

  • Decker MW, McGaugh JL (1991) The role of interactions between the cholinergic systems and neuromodulatory systems in learning and memory. Synapse 7: 151–168

    Google Scholar 

  • Decker MW, Introini-Collison IB, McGaugh JL (1989) Effects of naloxone on Morris water-maze learning in the rat: enhanced acquisition with pretraining but not posttraining administration. Psychobiology 17: 270–275

    Google Scholar 

  • Del Seppia C, Ghione S, Luschi P, Papi F (1995) Exposure to oscillating magnetic fields influences sensitivity to electrical stimuli. I. Experiments on pigeons. Bioelectromagnetics 16: 290–294

    Google Scholar 

  • Etienne AS, Maurer R, Saucy F, Teroni E (1986) Short-distance homing in the golden hamster after a passive outward journey. Anim Behav 34: 696–715

    Google Scholar 

  • Francis DD, Zaharia MD, Shanks N, Anisman H (1995) Stressinduced disturbances in Morris water-maze performance: interstrain variability. Physiol Behav 58: 57–65

    Google Scholar 

  • Frye CA (1995) Estrus-associated decrements in a water maze task are limited to acquisition. Physiol Behav 57: 5–14

    Google Scholar 

  • Galea LAM, Saksida L, Kavaliers M, Ossenkopp K-P (1994a) Naloxone facilitates spatial learning in a water-maze task in female, but not male, adult nonbreeding meadow voles. Pharmacol Biochem Behav 47: 265–271

    Google Scholar 

  • Galea LAM, Kavaliers M, Ossenkopp K-P, Innes DGL, Hargreaves EL (1994b). Sexually dimorphic spatial learning varies seasonally in two populations of deer mice. Brain Res 635: 18–26

    Google Scholar 

  • Galea LAM, Kavaliers M, Ossenkopp K-P, Hampson E (1995) Gonadal hormone levels and spatial learning performance in the morris water maze in male and female meadow voles, Microtus pennsylvanicus. Horm Behav 29: 106–125

    Google Scholar 

  • Galea LAM, Kavaliers M, Ossenkopp K-P (1996). Sexually-dimorphic spatial learning in meadow voles, Microtus pennsylvanicus, and deer mice, Peromyscus maniculatus. J Exp Biol 199: 195–200

    Google Scholar 

  • Gallagher M, King RA, Young NB (1983). Opiate antagonists improve spatial memory. Science 221: 975–976

    Google Scholar 

  • Gaulin SJC, FitzGerald RW (1986) Sex differences in spatial ability: An evolutionary hypothesis and test. Am Nat 127: 74–88

    Google Scholar 

  • Gaulin SJC, FitzGerald RW (1989) Sexual selection for spatial learning ability. Anim Behav 37: 322–331

    Google Scholar 

  • Gaulin SJC, FitzGerald RW, Wartell MS (1990) Sex differences in spatial ability and activity in two vole species (Microtus ochrogaster and M. pennsylvanicus). J Comp Psychol 104: 88–93

    Google Scholar 

  • Innis NK, Ossenkopp K-P, Prato FS, Sestini E (1986) Behavioral effects of exposure to nuclear magnetic resonance imaging: II spatial memory tests. Magn Reson Imaging 4: 281–284.

    Google Scholar 

  • Introini-Collison IB, Ford L, McGaugh JL (1995) Memory impairment induced by intraamygdala β-endorphin is mediated by noradrenergic influences. Neurobiol Learn Mem 63: 200–205

    Google Scholar 

  • Jiang H-K, Owyang V, Hong J-S, Gallagher M (1989) Elevated dynorphin in the hippocampal formation of aged rats: relation to cognitive impairment on a spatial task. Proc Nat Acad Sci USA 86: 2948–2951

    Google Scholar 

  • Kavaliers M, Colwell DD (1995) Exposure to stable flies reduces spatial learning in mice: involvement of endogenous opioid systems. Med Vet Entomol 9: 300–306

    Google Scholar 

  • Kavaliers M, Galea LAM (1995) Sex differences in the expression and antagonism of swim stress-induced analgesia in deer mice vary with the breeding season. Pain 63: 327–334

    Google Scholar 

  • Kavaliers M, Innes DGL (1993) Sex differences in the antinociceptive effects of the enkephalinase inhibitor, SCH 34826. Pharmacol Biochem Behav 46: 777–780

    Google Scholar 

  • Kavaliers M, Ossenkopp K-P, Hirst M (1984) Magnetic fields abolish the enhanced nocturnal analgesic resposnes to morphine in mice. Physiol Behav 32: 261–264

    Google Scholar 

  • Kavaliers, M., Ossenkopp K-P (1986) Magnetic field inhibition of morphine-induced analgesia and behavioral activity in mice: evidence for involvement of calcium ions. Brain Res 379: 30–38

    Google Scholar 

  • Kavaliers M and Ossenkopp K-P (1987a) Day-night rhythms of opioid and non-opioid stress-induced analgesia: differential inhibitory effects of exposure to magnetic fields. Pain 32: 223–229

    Google Scholar 

  • Kavaliers M, Ossenkopp K-P (1987b) Calcium channel involvement in magnetic field inhibition of morphine-induced analgesia. Naunyn Schmiedebergs Arch Pharmacol 336: 308–315

    Google Scholar 

  • Kavaliers M, Eckel LA, Ossenkopp K-P (1993) Brief exposure to 60 Hz magnetic fields improves sexually dimorphic spatial learning performance in the meadow vole, Microtus pennsylvanicus. J Comp Physiol A 173: 241–248

    Google Scholar 

  • Kavaliers M, Prato FS, Thomas A (1996) ELF magnetic fields increase opioid-induced analgesia in the land snail consistent with the predictions of the parametric resonance model (PRM) for K +. Bioelectromag Soc Abstr 18: 64–65

    Google Scholar 

  • Kirschvink JL, Walker MM (1985) Particle size considerations for magnetite-based magnetoreception. In: Kirschvink JL, Jones DJ, MacFadden BJ (eds) Magnetite biomineralization and magnetoreception in organisms: A new biomagnetisim. Plenum Press, New York, pp 243–256

    Google Scholar 

  • Kvist SBM, Selander R-K (1994) Open field thigmotaxis during various phases of the reproductive cycle. Scand J Psychol 35: 220–229

    Google Scholar 

  • Lamberty Y, Gower AJ (1988) Investigations into sex-related differences in locomotor activity, place learning and passive avoidance responding in NMRI mice. Physiol Behav 44: 787–790

    Google Scholar 

  • Lednev VV (1994) Interference with the vibrational energy sublevels of ions bound in calcium-binding proteins as the basis for the interaction of weak magnetic fields with biological systems, In: Frey AH (ed) On the nature of electromagnetic field interactions with biological systems. RG Landes, Austin, Texas pp 59–72

    Google Scholar 

  • Madden RC, Phillips JB (1987) An attempt to demonstrate magnetic compass orientation in two species of mammals. Anim Learn Behav 15: 130–134

    Google Scholar 

  • Mather JG (1985) Magnetoreception and the search for magnetic material in rodents. In Kirschvink JL, Jones DS, MacFadden BJ (eds) Magnetite biomineralization and magnetoreception in organisms: A new biomagnetism. Plenum Press, New York, pp 509–533

    Google Scholar 

  • Mather JG, Baker RR (1980) A demonstration of navigation by small rodents using an orientation cage. Nature 284: 259–262

    Google Scholar 

  • Mather JG, Baker RR (1981) Magnetic sense of direction in woodmice for route-based navigation. Nature 291: 152–155

    Google Scholar 

  • McNamara RK, Skeleton RW (1991) Pretraining morphine impairs acquisition and performance in the Morris water maze: motivation rather than amnesia. Psychobiology 19: 313–322

    Google Scholar 

  • McNamara RK, Skeleton RW (1993) The neuropharmacological and neurochemical basis of place learning in the Morris water maze. Brain Res Rev 18: 33–49

    Google Scholar 

  • Messing RB, Jensen RA, Martinez JL, Spiehler VR, Vasquez BJ, Soumireus-Mourat B, Liang KC, McGaugh JL (1979) Naloxone enhancement of memory. Behav Neural Biol 27: 266–275

    Google Scholar 

  • Mogil JS, Sternberg WF, Kest B, Marek P, Liebeskind JC (1993) Sex differences in the antagonism of swim stress-induced analgesia: effects of gonadectomy and estrogen replacement. Pain 53: 17–25

    Google Scholar 

  • Morris RGM (1984) Development of a water maze procedure for studying spatial learning in the rat. J Neurosci Methods 11: 47–60

    Google Scholar 

  • Nelson RJ, Kita M, Blom JMC, Rhyne-Grey J (1992) Photoperiod influences the critical calorie intake necessary to maintain reproduction among male deer mice (Peromyscus maniculatus). Biol Reprod 46: 226–232

    Google Scholar 

  • Ossenkopp K-P, Barbieto R (1978) Bird orientation and the geomagnetic field: A review. Neurosci Biobehav Rev 2: 255–270

    Google Scholar 

  • Ossenkopp K-P, Kavaliers M (1987) Morphine-induced analgesia and exposure to 60-Hz magnetic fields: inhibition of nocturnal analgesia is a function of magnetic field intensity. Brain Res 418: 356–360

    Google Scholar 

  • Ossenkopp K-P, Kavaliers M, Prato FS, Teskey GC, Sestini E, Hirst M (1985) Exposure to nuclear magnetic resonance imaging procedures attenuates morphine-induced analgesia in mice. Life Sci 37: 1507–1514

    Google Scholar 

  • Ossenkopp K-P, Innis NK, Prato FS, Sestini E (1986) Behavioral effects of exposure to nuclear magnetic resonance imaging: I. Open-field behavior and passive avoidance learning in rats. Magn Reson Imaging 4: 275–280

    Google Scholar 

  • Papi F, Ghione S, Rosa C, Del Seppia C, Luschi P (1995) Exposure to oscillating magnetic fields influences sensitivity to electrical stimuli. II. Experiments on humans. Bioelectromagnetics 16: 295–300

    Google Scholar 

  • Perrot-Sinal TS, Kostenuik MA, Ossenkopp K-P, Kavaliers M (1996a) Sex differences in performance in the Morris water maze and the effects of initial non-stationary hidden platform training. Behav Neurosci (in press)

  • Perrot-Sinal TS, Heale VR, Ossenkopp K-P, Kavaliers M (1996b) Sexually dimorphic aspects of locomotor activity. In: meadow voles, Microtus pennsylvanicus the effects of exposure to fox odor. Behav Neurosci (in press)

  • Phillips JB (1986) Magnetic compass orientation in the eastern redspotted newt (Notophthalamus vivridescens). J. Comp Physiol A 186: 103–109

    Google Scholar 

  • Prato FS, Ossenkopp K-P, Kavaliers M, Sestini E (1987) Attenuation of morphine-induced analgesia in mice by exposure to magnetic resonance imaging: differential effects of the static, radio frequency and time-varying magnetic field components. Magn Reson Imaging 5: 9–14

    Google Scholar 

  • Prato FS, Carson JJL, Ossenkopp K-P, Kavaliers M (1995) Possible mechanisms by which extremely low frequency magnetic fields affect opioid function. FASEB J 9: 807–814

    Google Scholar 

  • Prato FS, Kavaliers M, Carson JJL (1996) Behavioral evidence that magnetic field effects in the land snail, Cepaea nemoralis, may not depend on magnetite or induced electric currents. Bioelectromagnetics 17: 123–130

    Google Scholar 

  • Roof RL, Havens MD (1992) Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Res 572: 310–313

    Google Scholar 

  • Saucier D, Cain DP (1995) Spatial learning without NMDA receptor-dependent long-term potentiation. Nature 378: 186–188

    Google Scholar 

  • Schenk S (1987) Comparison of spatial learning in woodmice (Apodemus sylvaticus) and hooded rats (Rattus norvegieus). J Comp Psychol 101: 150–158

    Google Scholar 

  • Shors TJ, Dryver E (1992) Stress impedes exploration and the acquisition of spatial information in the eight-arm radial maze. Psychobiology 20: 247–253

    Google Scholar 

  • Stickel LF (1968) Home range and travels. In: King JA (ed) Biology of Peromyscus (Rodentia), American Society of Mammologists, Stillwater, Oklahoma, pp 373–411

    Google Scholar 

  • Treit D, Fundytus M (1989) Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 31: 959–962

    Google Scholar 

  • Whishaw IQ (1995) A comparison of rats and mice in a swimming pool place task and matching to place task: some surprising differences. Physiol Behav 58: 687–693

    Google Scholar 

  • Whishaw IQ, Cassel J-C, Jarrard LE (1995) Rats with fimbria-fornix lesions display a place response in a swimming pool: a dissociation between getting there and knowing where. J Neurosci 15: 5779–5788

    Google Scholar 

  • Williams CL, Meck WH (1991) The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16: 155–176

    Google Scholar 

  • Williams CL, Barnett AM, Meck WH (1990) Organizational effects of early gonadal secretions on sexual differentiation in memory. Behav Neurosci 194: 84–97

    Google Scholar 

  • Wiltschko W, Wiltschko R (1995) Magnetic Orientation in Animals Springer, Berlin, Heidelberg, New York

    Google Scholar 

  • Wolff JO (1989) Social behavior. In: Kirkland Jr GL, Layne JN (eds), Advances in the Study of Peromyscus (Rodentia). Texas Tech University Press, Lubbock Texas, pp 271–291

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Oral Biology, Faculty of Dentistry, Department of Psychology and Neuroscience Program and Bioelectromagnetics Western, University of Western Ontario, N6A 5C1, London, Ontario, Canada

    M. Kavaliers, K. -P. Ossenkopp, F. S. Prato, D. G. L. Innes, L. A. M. Galea, D. M. Kinsella & T. S. Perrot-Sinal

  2. Department of Nuclear Medicine and Magnetic Resonance, St. Joseph's Health Centre and Lawson Research Institute, N6A 4L6, London, Ontario, Canada

    F. S. Prato

Authors
  1. M. Kavaliers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. -P. Ossenkopp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. S. Prato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. G. L. Innes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. A. M. Galea
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. M. Kinsella
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. T. S. Perrot-Sinal
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kavaliers, M., Ossenkopp, K.P., Prato, F.S. et al. Spatial learning in deer mice: sex differences and the effects of endogenous opioids and 60 Hz magnetic fields. J Comp Physiol A 179, 715–724 (1996). https://doi.org/10.1007/BF00216135

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00216135

Key words

Search

Navigation