Skip to main content
SpringerLink
Log in

Effects of Predator-Induced Stress and Age on Working Memory in Rats

  • Published:
The Psychological Record Aims and scope Submit manuscript

Abstract

The effects of age and predator-induced stress, by exposing rats to a cat, were examined during subsequent testing of spatial working memory. Male rats (3 months and 20 months of age) were trained on a spatial delayed-alternation task using an elevated T maze. After subgroups were given intermittent protected-exposure sessions over a 3-day period to cats or to a control condition, they were tested on the working memory task. The old rats took more trials to reach training criterion. Overall, both stress-exposed groups exhibited a decline in accuracy 24 hr later and recovered completely during the subsequent test sessions. Surprisingly, young stressed rats showed significantly greater decrements in accuracy than old stressed rats. However, exposure to the stressor resulted in decreases in response speed that were comparable for both age groups. These findings are discussed in terms of possible changes in glucocorticoids, plasma corticosterone, and endogenous opioids that are known to be affected by age and stress and have been shown to influence spatial working memory.

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

References

  • ANISMAN, H., DECATANZARO, D., & REMMINGTON, G. (1978). Escape performance following exposure to inescapable shock: Deficits in motor response maintenance. Journal of Experimental Psychology: Animal behavior Processes, 4, 179–218.

    Google Scholar 

  • ANISMAN, H., SUISSA, A., & SKLAR, L. S. (1980). Escape deficits induced by uncontrollable stress: Antagonism by dopamine and norepinephrine agonists. Behavioral and Neural Biology, 28, 34–47.

    Article  PubMed  Google Scholar 

  • BARNES, C. A. (1979). Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. Journal of Comparative and Physiological Psychology, 93, 74–104.

    Article  PubMed  Google Scholar 

  • BLANCHARD, R. J., YUDKO, E. B., RODGERS, R. J., & BLANCHARD, D. C. (1993). Defense system psychopharmacology: An ethological approach to the pharmacology of fear and anxiety. Behvioural Brain Research, 58, 155–165.

    Article  Google Scholar 

  • BOSTOCK, E., GALLAGHER, M., & KING, R. A. (1988). Effects of opioid microinjections into the medial septal area on spatial memory in rats. Behavioral Neuroscience, 102, 643–652.

    Article  PubMed  Google Scholar 

  • COLEMAN, P., & FLOOD, D. (1987). Neuron numbers and dendritic extent in normal aging and Alzheimer’s disease. Neurobiology of Aging, 8, 521.

    Article  PubMed  Google Scholar 

  • CRISP, T., STAFINSKY, J. L., HOSKINS, D. L., DAYAL, B., CHINROCK, K. M., & URAM, M. (1994). Effects of aging on spinal opioid-induced antinociception. Neurobiology of Aging, 15, 169–174.

    Article  PubMed  Google Scholar 

  • DRUGAN, R. C., & MAIER, S. F. (1983). Analgesia and opioid involvement in shock elicited activity and escape deficits produced by inescapable shock. Learning & Motivation, 14, 30–47.

    Article  Google Scholar 

  • FANSELOW, M. S. (1986). Conditioned fear-induced analgesia: A competing motivational state theory of stress analgesia. Annals of New York Academy of Sciences, 467, 40–54.

    Article  Google Scholar 

  • FANSELOW, M. S. (1994). Neural organization of the defensive behavior system responsible for fear. Psychonomic Bulletin & Review, 4, 429–438.

    Article  Google Scholar 

  • FILE, S. E., ZANGROSSI, H., JR., SANDERS, F. L., & MABBUTT, P. S. (1993). Dissociation between behavioral and corticosterone responses on repeated exposures to cat odor. Physiology & behavior, 54, 1109–1111.

    Article  Google Scholar 

  • FLOOD, J. F., CHERKIN, A., & MORLEY, J. E. (1987). Antagonism of endogenous opioids modulates memory processing. Brain Research, 422, 218–234.

    Article  PubMed  Google Scholar 

  • FOY, M. R., STANTON, M. E., LEVINE, S., & THOMPSON, R. F. (1987). Behavioral stress impairs long-term potentiation in rodent hippocampus. Behavioral and Neural Biology, 48, 138–149.

    Article  PubMed  Google Scholar 

  • FROLKIS, V. V. (1993). Stress-age syndrome. Mechanisms of Aging and Development, 69, 93–107.

    Article  Google Scholar 

  • GAGE, R. H., DUNNETT, S. B., & BJORKLUND, A. (1984). Spatial learning and motor deficits in aged rats. Neurobiology of Aging, 5, 43–48.

    Article  PubMed  Google Scholar 

  • GALLAGHER, M., BOSTOCK, E., & KING, R. (1985). Effects of opiate antagonists on spatial memory in young and old rats. Behavioral and Neural Biology, 44, 374–385.

    Article  PubMed  Google Scholar 

  • GALLAGHER, M., KING, R. A., & YOUNG, N. B. (1983). Opiate antagonists improve spatial memory. Science, 221, 975–976.

    Article  PubMed  Google Scholar 

  • GALLAGHER, M., & PELLYMOUNTER, M. A. (1988). Spatial learning deficits in old rats: A model for memory decline in the aged. Neurobiology of Aging, 9, 549–556.

    Article  PubMed  Google Scholar 

  • GEINESMAN, Y,. DETOLEDO-MORRELL, L., MORRELL, F., & HELLER, R. E. (1995). Hippocampal markers of age-related memory dysfunction: Behavioral, electrophysiological, and morphological perspectives. Progress in Neurobiology, 45, 223–252.

    Article  Google Scholar 

  • HOSKINS, B., BURTON, C. K., & HO, I. K. (1986). Differences in morphineinduced antinociception and locomotor activity in mature adult and aged mice. Pharmacology, Biochemistry & behavior, 25, 599–605.

    Article  Google Scholar 

  • HOTSENPILLER, G., & WILLIAMS, J. L. (1996). Conditioned fear and analgesia to conspecific odors: Benzodiazepine and 5-HT1 A agonists. Psychobiology, 24, 118–126.

    Google Scholar 

  • ISSA, A., ROWE, W., GAUTHIER, S., & MEANEY, M. (1990). Hypothalamicpituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. Journal of Neuroscience, 10, 3247–3254.

    PubMed  Google Scholar 

  • JACKSON, R. L., ALEXANDER, J. H., & MAIER, S. F. (1980). Learned helplessness, inactivity, and associative deficits: Effects of inescapable shock of response choice escape learning. Journal of Experimental Psychology: Animals Behavior Processes, 6, 1–20.

    Google Scholar 

  • JACKSON, R. L., MAIER, S. F., & COON, D. J. (1979). Long-term analgesic effects of inescapable shock and learned helplessness. Science, 206, 91–93.

    Article  PubMed  Google Scholar 

  • KERR, P., CAMPBELL, L., APPLEGATE, M., BRODISH, A., & LANDFIELD, P. (1991). Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. Journal of Neuroscience, 11, 1316–1324.

    PubMed  Google Scholar 

  • LANDFIELD, P., WAYMIRE, J., & LYNCH, G. (1978). Hippocampal aging and adrenocorticoids: A quantitative correlation. Science, 202, 1098–1102.

    Article  PubMed  Google Scholar 

  • LEE, R. K. K., & MAIER, S. F. (1988). Inescapable shock and attention to internal versus external cues in a water discrimination escape task. Journal of Experimental Psychology: Animal Behavior Processes, 14, 301–310.

    Google Scholar 

  • LESTER, L. S., & FANSELOW, M. S. (1985). Exposure to a cat produces opioid analgesia in rats. Behavioral Neuroscience, 4, 756–759.

    Article  Google Scholar 

  • LUINE, V., SPENCER, R., & MCEWEN, B. S. (1993). Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function. Brain Research, 616, 65–70.

    Article  PubMed  Google Scholar 

  • LUINE, V., VILLEGAS, M., MARTINEZ, C., & MCEWEN, B. S. (1994). Repeated stress causes reversible impairments of spatial memory performance. Brain Research, 639, 167–170.

    Article  PubMed  Google Scholar 

  • MAIER, S. F (1986). Stressor controllability and stress-induced analgesia. In D. D. Kelley (Ed.), Annals of the New York Academy of Sciences, 467, 55–71.

    Article  PubMed  Google Scholar 

  • MAIER, S. F., ALBIN, R. W., & TESTA, T. J. (1973). Failure to learn to escape in rats previously exposed to inescapable shock depends on the nature of the escape response. Journal of Experimental & Physiological Psychology, 85, 581–592.

    Article  Google Scholar 

  • MAIER, S. F., RYAN, S. M., BARKSDALE, C. M., & KALIN, N. H. (1986). Stressor, controllability and the pituitary-adrenal system. Behavioral Neuroscience, 100, 669–674.

    Article  PubMed  Google Scholar 

  • MCEWEN, B. S. (1992). Re-examination of the glucocorticoid hypothesis of stress and aging. Progress in Brain Research, 93, 365–378.

    Article  PubMed  Google Scholar 

  • MCEWEN, B. S., & SAPOLSKY, R. (1995). Stress and cognitive function. Recent Opinion in Neurobiology, 5, 205–216.

    Article  Google Scholar 

  • MEANEY, M., AITKEN, D., BHATNAGER, S., VAN BERKEL, C., & SAPOLSKY, R. (1988). Effects of neonatal handling on age-related impairments associated with the hippocampus. Science, 239, 766–769.

    Article  PubMed  Google Scholar 

  • ODIO, M., & BRODISH, A. (1989). Age-related adaptation of pituitaryadrenocortical responses to stress. Neuroendocrinology, 49, 382–388.

    Article  PubMed  Google Scholar 

  • PETERSON, C., MAIER, S. F., & SELIGMAN, M. E. P. (1993). Learned helplessness: A theory for the age of personal control. Oxford: Oxford University Press.

    Google Scholar 

  • PIVA, F., MAGGI, R., LIMONTA, P., DONDI, D., & MARTINI, L. (1986). Decrease of mu opioid receptors in the brain and in the hypothalamus of the aged male rat. Life Sciences, 40, 391–398.

    Article  Google Scholar 

  • ROSELLLNI, R. A. (1978). Inescapable shock interferes with the acquisition of a free appetitive operant. Animal Learning & behavior, 6, 155–159.

    Article  Google Scholar 

  • SAKSIDA, L. M., GALEA, L. A. M., & KAVALIERS, M. (1993). Predator-induced opioid and non-opioid mediated analgesia in young meadow voles: Sex differences and developmental changes. Brain Research, 617, 214–219.

    Article  PubMed  Google Scholar 

  • SAPOLSKY, R. (1985). A mechanism for glucocorticoid toxicity in the hippocampus: Increased neuronal vulnerability to metabolic insults. Journal of Neuroscience, 5, 1228–1232.

    PubMed  Google Scholar 

  • SAPOLSKY, R. (1986). Glucocorticoid toxicity in the hippocampus: Temporal aspects of synergy with kainic acid. Neuroendocrinology, 43, 440–444.

    Article  PubMed  Google Scholar 

  • SAPOLSKY, R. (1992). Stress, the aging brain, and the mechanisms of neuron death. Cambridge, MA: The MIT Press.

    Google Scholar 

  • SAPOLSKY, R., KREY, L., & MCEWEN, B. S. (1986). The adrenocortical axis in the aged rat: Impaired sensitivity to both fast and delayed feedback inhibition. Neurobiology of Aging, 7, 331–335.

    Article  PubMed  Google Scholar 

  • SONNTAG, W., GOLLSZEK, A., BRODISH, A., & ELDRIDGE, J. (1987). Diminished diurnal secretion of adreno-corticotropin but not corticosterone in old male rats: Possible relation to increased adrenal sensitivity to ACTH in vivo. Endocrinology, 120, 2308–2315.

    Article  PubMed  Google Scholar 

  • SHORS, T. J., LEVINE, S., & THOMPSON, R. F. (1990). Opioid antagonist eliminates the stress-induced impairment of long-term potentiation (LTP). Brain Research, 506, 316–318.

    Article  PubMed  Google Scholar 

  • SHORS, T. J., STEIB, T. B., LEVINE, S., & THOMPSON, R. F. (1989). Inescapable versus escapable shock modulates longer-term potentiation in the rat hippocampus. Science, 244, 224–226.

    Article  PubMed  Google Scholar 

  • SPAIN, J. W., & NEWMAN, G. C. (1991). Chronic opioids impair acquisition of both radial maze and Y-maze choice escape. Psychopharmacolog, 105, 101–106.

    Article  Google Scholar 

  • WAN, R. Q., GIVENS, B., & OLTON, D. S. (1995). Opioid modulation of working memory: Intraseptal, but not intraamygdaloid, infusions of B-endorphin impair performance in spatial alternation. Neurobiology of Learning and Memory, 63, 74–86.

    Article  PubMed  Google Scholar 

  • WARREN, D. A., CASTRO, C. A., RUDY, J. W., & MAIER, S. F. (1991). No spatial learning impairment following exposure to inescapable shock. Psychobiology, 19, 127–134.

    Google Scholar 

  • WEISS, J., GOODMAN, P, LOSITO, B., CORRIGAN, S., CHARRY, J., & BAILEY, W. (1990). Behavioral depression produced by an uncontrollable stressor: Relationship to norepinephrine, dopamine, and serotonin levels in various regions of the rat brain. Brain Research Review, 3, 167–205.

    Article  Google Scholar 

  • WILLIAMS, J. L. (1989). Ethoexperimental analysis of stress, contextual odors, and defensive behaviors. In R. J. Blanchard, P. F. Brain, D. C. Blanchard, & S. Parmigiani (Eds.), Ethoexperimental approaches to the study of behavior (pp. 214–228). Dordrecht: Martinus Nijhoff.

    Chapter  Google Scholar 

  • WILLIAMS, J. L., & BARBER, R. G. (1990). Effects of cat exposure and cat odors on subsequent amphetamine-induced stereotypy. Pharmacology, Biochemistry & behavior, 36, 375–380.

    Article  Google Scholar 

  • WILLIAMS, J. L., & GROUX, M. L. (1993). Exposure to various stressors alters preferences for natural odors in rats. Journal of Comparative Psychology, 107, 39–47.

    Article  PubMed  Google Scholar 

  • WILLIAMS, J. L., JUST, J. M., & WORLAND, P. D. (1994). Effects of repeateddefeat sessions as a colony intruder on subsequent hypoalgesia and freezing in the rat. Learning & Motivation, 25, 152–174.

    Article  Google Scholar 

  • WILLIAMS, J. L., & LIERLE, D. M. (1988). Effects of repeated defeat by a dominant conspecific on subsequent pain sensitivity. Animal Learning & behavior, 16, 477–485.

    Article  Google Scholar 

  • WILLIAMS, J. L., & MAIER, S. F. (1978). Transituational immunization and therapy of learned helplessness in the rat. Journal of Experimental Psychology: Animals Behavior Processes, 3, 240–253.

    Google Scholar 

  • WILLIAMS, J. L., ROGERS, A. G., & ADLER, A. P (1990). Prolonged exposure to conspecific and predator odors reduce fear reactions to these odors during subsequent prod-shock tests. Animal Learning & behavior, 18, 453–461.

    Article  Google Scholar 

  • WILLIAMS, J. L., & SCOTT, D. K. (1989). Influence of con specific and predatory stressors and their associated odors on defensive burying and freezing. Animal Learning & behavior, 17, 383–393.

    Article  Google Scholar 

  • WILLIAMS, J. L., WORLAND, P. D., & SMITH, M. G. (1990). Defeat-induced hypoalgesia in the rat: Effects of conditioned odors, naltrexone, and extinction. Journal of Experimental Psychology: Animal Behavior Processes, 16, 345–357.

    PubMed  Google Scholar 

  • WOOLLEY, C. S., GOULD, E., & MCEWEN, B. S. (1990). Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Research, 531, 225–231.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychology, Kenyon College, Gambier, OH, 43022, USA

    Jon L. Williams & Shelley L. Baker

  2. Denison University, OH, USA

    Jennifer E. Gress

  3. Ohio State University, USA

    Bennet Givens

Authors
  1. Jon L. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shelley L. Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer E. Gress
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bennet Givens
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This research was supported by a Kenyon College Summer Science stipend to Shelly L. Baker, a COSEN stipend to Jennifer E. Gress, and endowment funds from the Samuel B. Cummings Professorship in Psychology to Jon L. Williams.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Williams, J.L., Baker, S.L., Gress, J.E. et al. Effects of Predator-Induced Stress and Age on Working Memory in Rats. Psychol Rec 48, 355–372 (1998). https://doi.org/10.1007/BF03395277

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03395277

Search

Navigation