Skip to main content
Log in

Preferences for cocaine- or pup-associated chambers differentiates otherwise behaviorally identical postpartum maternal rats

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale and objectives

Our previous work uncovered a differential preference of maternal female rats for cues associated with pups versus cues associated with cocaine at three different postpartum time points. Our current study examines the preference for these cues in conjunction with an assessment of the capacity to express the maternal behavior at one of these time points. We examined dams at day 10 postpartum using a procedure that included two additional controls, and a complete assessment of the expression of maternal behavior and locomotor activity.

Methods

A conditioned place-preference procedure was used to determine the preference for cocaine- or pup-associated cues. The two controls were (1) a preconditioning test to verify no initial chamber preference and (2) a separate control group of postpartum day-10 dams exposed to chambers and cues but not to unconditioned stimuli. The expression of maternal behavior was determined by measurement of maternal nest building, retrieval of pups to the nest, grooming, crouching over pups, nursing, and maternal aggression. Locomotor activity was measured with an automated apparatus.

Results

Dams conditioned with cocaine or pups showed a preference for either the cocaine-associated chamber or the pup-associated chamber, confirming the existence of two similar-sized preference groups at this time point. Regardless of preference, dams had equal and robust expression of maternal behavior and similar locomotor capacity. The pre-conditioning test showed no initial chamber preferences and did not alter the conditioned preference response. The use of unconditioned stimuli in the place-preference conditioning procedure was effective and necessary for the preference response.

Conclusion

Our current study has revealed that differences in the motivational state of the maternal dam emerge even while the expression of maternal behavior is constant and substantial. The data suggest that the difference in preference is a very specific appetitive response that is not linked to expression of maternal behavior or locomotor capacity.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1A, B.
Fig. 2.
Fig. 3A–D.

Similar content being viewed by others

References

  • Bardo MT, Bevins RA (2000) Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology 153:31–43

    CAS  PubMed  Google Scholar 

  • Bardo MT, Neisewander JL, Pierce RC (1990) Novelty-induced place preference behavior in rats: effects of opiate and dopaminergic drugs. Pharmacol Biochem Behav 32:683–687

    Article  Google Scholar 

  • Bardo MT, Rowlett JK, Harris MJ (1995) Conditioned place preference using opiate and stimulant drugs: a meta- analysis. Neurosci Biobehav Rev 19:39–51

    CAS  PubMed  Google Scholar 

  • Belzung C, Le Pape G (1994) Comparison of different behavioral test situations used in psychopharmacology for measurement of anxiety. Physiol Behav 56:623–628

    CAS  PubMed  Google Scholar 

  • Blanchard DC, Blanchard RJ (1999) Cocaine potentiates defensive behaviors related to fear and anxiety. Neurosci Biobehav Rev 23:981–991

    CAS  PubMed  Google Scholar 

  • Blanchard RJ, Kaawaloa JN, Hebert MA, Blanchard DC (1999) Cocaine produces panic-like flight responses in mice in the mouse defense test battery. Pharmacol Biochem Behav 64:523–528

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS (1996) Biochemical basis of parental behavior in the rat. In: Rosenblatt JS, Snowden CT (eds) Advances in the study of behavior, vol 25. Academic Press, New York, pp 215–242

  • Bruckner JV, Jiang WD, Ho BT, Levy BM (1982) Histopathological evaluation of cocaine-induced skin lesions in the rat. J Cutan Pathol 9:83–95

    CAS  PubMed  Google Scholar 

  • Campbell JO, Wood RD, Spear LP (2000) Cocaine and morphine-induced place conditioning in adolescent and adult rats. Physiol Behav 68:487–493

    Article  CAS  PubMed  Google Scholar 

  • Carr GD, Phillips AG, Fibiger HC (1988) Independence of amphetamine reward from locomotor stimulation demonstrated by conditioned place preference. Psychopharmacology 94:221–226

    CAS  PubMed  Google Scholar 

  • Carr GD, Fibiger HC, Phillips AG (1989) Conditioned place preference as a measure of drug reward. In: Liebman JM, Cooper SJ (eds) The neuropharmacological basis of reward. Oxford University Press, New York, pp 264–319

  • Durazzo TC, Gauvin DV, Goulden KL, Briscoe RJ, Holloway FA (1994) Cocaine-induced conditioned place approach in rats: the role of dose and route of administration. Pharmacol Biochem Behav 49:1001–1005

    Article  CAS  PubMed  Google Scholar 

  • Eikelboom R, Stewart J (1982) Conditioning of drug-induced physiological responses. Psychol Rev 89:507–528

    CAS  PubMed  Google Scholar 

  • Erb SM, Parker LA (1994) Individual differences in novelty-induced activity do not predict strength of amphetamine-induced place conditioning. Pharmacol Biochem Behav 48:581–586

    CAS  PubMed  Google Scholar 

  • Fahrbach SE, Pfaff DW (1982) Hormonal and neural mechanisms underlying maternal behavior. In: Pfaff DW (ed) The physiological mechanisms of motivation. Springer, Berlin Heidelberg New York, pp 253–285

  • Fleming AS, Cheung U, Myhal N, Kessler Z (1989) Effects of maternal hormones on 'timidity' and attraction to pup-related odors in female rats. Physiol Behav 46:449–453

    CAS  PubMed  Google Scholar 

  • Fleming AS, Korsmit M, Deller M (1994) Rat pups are potent reinforcers to the maternal animal: effects of experience parity, hormones, and dopamine function. Psychobiology 22:44–53

    CAS  Google Scholar 

  • Gong W, Neill DB, Justice JB Jr (1996) Locomotor response to novelty does not predict cocaine place preference conditioning in rats. Pharmacol Biochem Behav 53:191–196

    CAS  PubMed  Google Scholar 

  • Hebert MA, Blanchard DC, Blanchard RJ (1999) Intravenous cocaine precipitates panic-like flight responses and lasting hyperdefensiveness in laboratory rats. Pharmacol Biochem Behav 63:349–360

    Article  PubMed  Google Scholar 

  • Hecht GS, Spear NE, Spear LP (1999) Changes in progressive ratio responding for intravenous cocaine throughout the reproductive process in female rats. Dev Psychobiology 20:136–145

    Article  Google Scholar 

  • Johns JM, Noonan LR, Zimmerman LI, Li L, Pedersen CA (1994) Effects of chronic and acute cocaine treatment on the onset of maternal behavior and aggression in Sprague-Dawley rats. Behav Neurosci 108:107–112

    Article  CAS  PubMed  Google Scholar 

  • Johns JM, Lubin DA, Walker CH, Meter KE, Mason GA (1997) Chronic gestational cocaine treatment decreases oxytocin levels in the medial preoptic area, ventral tegmental area and hippocampus in Sprague-Dawley rats. Neuropeptides 31:439–443

    CAS  PubMed  Google Scholar 

  • Johns JM, Nelson CJ, Meter KE, Lubin DA, Couch CD, Ayers A, Walker CH (1998) Dose-dependent effects of multiple acute cocaine injections on maternal behavior and aggression in Sprague-Dawley rats. Dev Neurosci 20:525–532

    Article  CAS  PubMed  Google Scholar 

  • Kalinichev M, Rosenblatt JS, Morrell JI (2000a) The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats. Behav Neurosci 114:196–210

    Article  CAS  PubMed  Google Scholar 

  • Kalinichev M, Rosenblatt JS, Nakabeppu Y, Morrell JI (2000b) Induction of c-fos-like and fosB-like immunoreactivity reveals forebrain neuronal populations involved differentially in pup-mediated maternal behavior in juvenile and adult rats. J Comp Neurol 416:45–78

    Article  CAS  PubMed  Google Scholar 

  • Khantzian EJ (1985) The self-medication hypothesis of addictive disorders: focus on heroin and cocaine dependence. Am J Psychiatry 142:1259–1264

    Google Scholar 

  • Klebaur JE, Bardo MT (1999) Individual differences in novelty seeking on the playground maze predict amphetamine conditioned place preference. Pharmacol Biochem Behav 63:131–136

    Article  CAS  PubMed  Google Scholar 

  • Klebaur JE, Bevins RA, Segar TM, Bardo MT (2001) Individual differences in behavioral responses to novelty and amphetamine self-administration in male and female rats. Behav Pharmacol 12:267–275

    CAS  PubMed  Google Scholar 

  • Kosten TA, Miserendino MJ (1998) Dissociation of novelty- and cocaine-conditioned locomotor activity from cocaine place conditioning. Pharmacol Biochem Behav 60:785–791

    CAS  PubMed  Google Scholar 

  • Lee A, Clancy S, Fleming AS (1999) Mother rats bar-press for pups: effects of lesions of the MPOA and limbic sites on maternal behavior and operant responding for pup-reinforcement. Behav Brain Res 100:15–31

    CAS  PubMed  Google Scholar 

  • Mattson BJ, Morrell JI (2001) Neuronal fos expression in dams with preferences for cocaine- or pup-conditioned contexts (abstract). Soc Neurosci 31:647.15

    Google Scholar 

  • Mattson BJ, Williams S, Rosenblatt JS, Morrell JI (2001) Comparison of two positive reinforcing stimuli: pups and cocaine throughout the postpartum period. Behav Neurosci 115:683–694

    Article  CAS  PubMed  Google Scholar 

  • Mayer AD, Rosenblatt JS (1980) Hormonal interaction with stimulus and situational factors in the initiation of maternal behavior in nonpregnant rats. J Comp Physiol Psychol 94:1040–1059

    CAS  PubMed  Google Scholar 

  • Mayer AD, Rosenblatt JS (1998) A method for regulating the duration of pregnancy and the time of parturition in Sprague-Dawley rats (Charles River CD strain). Dev Psychobiol 32:131–136

    Article  CAS  PubMed  Google Scholar 

  • Mayer AD, Monroy MA, Rosenblatt JS (1990) Prolonged estrogen-progesterone treatment of nonpregnant ovariectomized rats: factors stimulating home-cage and maternal aggression and short- latency maternal behavior. Horm Behav 24:342–364

    CAS  PubMed  Google Scholar 

  • McBride WJ, Murphy JM, Ikemoto S (1999) Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies. Behav Brain Res 101:129–152

    CAS  PubMed  Google Scholar 

  • Mucha RF, van der KD, O'Shaughnessy M, Bucenieks P (1982) Drug reinforcement studied by the use of place conditioning in rat. Brain Res 243:91–105

    CAS  PubMed  Google Scholar 

  • Nader MA, Woolverton WL (1991) Effects of increasing the magnitude of an alternative reinforcer on drug choice in a discrete-trials choice procedure. Psychopharmacology 105:169–174

    CAS  PubMed  Google Scholar 

  • Nader MA, Woolverton WL (1992) Effects of increasing response requirement on choice between cocaine and food in rhesus monkeys. Psychopharmacology 108:295–300

    CAS  PubMed  Google Scholar 

  • Nomikos GG, Spyraki C (1988) Cocaine-induced place conditioning: importance of route of administration and other procedural variables. Psychopharmacology 94:119–125

    Google Scholar 

  • Numan M (1994) Maternal behavior. In: Knobil E, Neill J (eds) The physiology of reproductive behavior, 2nd edn. Raven Press, New York, pp 221–302

  • Parker LA (1992) Place conditioning in a three or four choice apparatus: role of stimulus novelty in drug-induced place conditioning. Behav Neurosci 106:294–306

    CAS  PubMed  Google Scholar 

  • Rescorla RA (1967) Pavlovian conditioning and its proper control procedures. Psych Rev 74:71–80

    CAS  Google Scholar 

  • Schechter MD, Calcagnetti DJ (1993) Trends in place preference conditioning with a cross-indexed bibliography, 1957–1991. Neurosci Biobehav Rev 17:21–41

    CAS  PubMed  Google Scholar 

  • Schechter MD, Calcagnetti DJ (1998) Continued trends in the conditioned place preference literature from 1992 to 1996, inclusive, with a cross-indexed bibliography. Neurosci Biobehav Rev 22:827–846

    CAS  PubMed  Google Scholar 

  • Scoles MT, Siegel S (1986) A potential role of saline trials in morphine-induced place preference conditioning. Pharmacol Biochem Behav 35:583–587

    Google Scholar 

  • Scott DW, Morrell JI, Vernotica EM (1997) Focal necrotizing panniculitis and vascular necrosis in rats given subcutaneous injections of cocaine hydrochloride. J Cutan Pathol 24:25–29

    CAS  PubMed  Google Scholar 

  • Shippenberg TS, Heidbreder C (1995) Sensitization to the conditioned rewarding effects of cocaine: pharmacological and temporal characteristics. J Pharmacol Exp Ther 273:808–815

    CAS  PubMed  Google Scholar 

  • Smith KS, Mattson BJ, Morrell JI (2002) A quantitative analysis of neural substrates engaged in the motivation to perform maternal behavior (abstract). Soc Neurosci 32:878.13

    Google Scholar 

  • Spear LP, Frambes NA, Kirstein CL (1989) Fetal and maternal brain and plasma levels of cocaine and benzoylecgonine following chronic subcutaneous administration of cocaine during gestation in rats. Psychopharmacology 97:427–431

    CAS  PubMed  Google Scholar 

  • Vernotica EM, Morrell JI (1998) Plasma cocaine levels and locomotor activity after systemic injection in virgin and in lactating maternal female rats. Physiol Behav 64:399–407

    Article  CAS  PubMed  Google Scholar 

  • Vernotica EM, Lisciotto CA, Rosenblatt JS, Morrell JI (1996a) Cocaine transiently impairs maternal behavior in the rat. Behav Neurosci 110:315–323

    Article  CAS  PubMed  Google Scholar 

  • Vernotica EM, Rosenblatt JS, Morrell JI (1996b) Acute cocaine disrupts all components of established maternal behavior in the rat (abstract). Soc Neurosci 1887

  • Vernotica EM, Rosenblatt JS, Morrell JI (1999) Microinfusion of cocaine into the medial preoptic area or nucleus accumbens transiently impairs maternal behavior in the rat. Behav Neurosci 113:377–390

    Article  CAS  PubMed  Google Scholar 

  • Wansaw M, Williams SE, Rosenblatt JS, Morrell JI (2001) Stress and habituation: variables affecting conditioned place preference in maternal rodents (abstract). Soc Neurosci 31:77.8

    Google Scholar 

  • Wansaw M, Williams SE, Rosenblatt JS, Morrell JI (2002) Cocaine- and pup-induced conditioned place preference in the lactating, maternal rat (abstract). Soc Neurosci 32:181.15

    Google Scholar 

  • Welker WI (1957) "Free" versus "forced" exploration of a novel situation by rats. Psychol Rep 3:95–108

    Google Scholar 

  • Wise RA (1989) The brain and reward. In: Leibman JM, Cooper SJ (eds) The neuropharmacological basis of reward. Clarendon Press, Oxford, pp 377–424

  • White NM, Hiroi N (1992) Pipradol conditioned place preference is blocked by SCH23390. Pharmacol Biochem Behav 43:377–380

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by PHS 5 S06 GM 08223–15.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brandi J. Mattson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mattson, B.J., Williams, S.E., Rosenblatt, J.S. et al. Preferences for cocaine- or pup-associated chambers differentiates otherwise behaviorally identical postpartum maternal rats. Psychopharmacology 167, 1–8 (2003). https://doi.org/10.1007/s00213-002-1351-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-002-1351-4

Keywords

Navigation