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Psychobiology of Mothering:

Psychobiology of Mothering:. a comparison of rat and human mothers. Alison S. Fleming Centre for Study of Biological Communications University of Toronto at Mississauga. Maternal Behavior : Human and Animal Models. SENSORY HORMONES EXPERIENCE DEVELOPMENT NEURAL GENETIC. SENSORY

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Psychobiology of Mothering:

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  1. Psychobiology of Mothering: a comparison of rat and human mothers Alison S. Fleming Centre for Study of Biological Communications University of Toronto at Mississauga

  2. Maternal Behavior: Human andAnimalModels SENSORY HORMONES EXPERIENCE DEVELOPMENT NEURAL GENETIC SENSORY HORMONES EXPERIENCE DEVELOPMENT NEURAL GENETIC

  3. human Rat St Joseph’s, 1907 Erindale, 1963 Our work is done In S Ontario under a veil of smog in beautiful buildings, with all their original features essentially untouched

  4. Setting up the straw woman TWO PSYCHONEUROLOGICAL SYSTEMS • Liking/Wanting • stimulus salience, ‘reward’ • Nucleus accumbens (NAcc) • Doing (or, the quality of) • Attention (selective, shifting, flexibility, strategies), attentiveness • Medial prefrontal cortex (mPFC)

  5. One (of a number) of unifying principles tying these systems and functions together may be thedopamine system (PFC) (NAC)

  6. One (of a number) of unifying principles tying these systems and functions together is thedopamine system (PFC) (NAC)

  7. Adapted from Bauer, 1983-pup odours • See also Fleming et al.,, 1987, 1989-odors pups • Farrell & Alberts, 2002-ultrasound pup • Lee, Fleming et al., 2000-bar press rat • Mattson, Williams, Rosenblatt, & Morrell (2000)-cpp rat • Fleming, Corter, Franks, Surbey, Schneider., & Steiner, 1993-odor humans • Stallings et al., 2002-cries humans • Purhonen et al., 2001; in press-cries eeg • Fleming, Ruble, Flett, & Van Wagner, 1990-increase response to babies • Lovic & Fleming, 2004; Lovic, in prep-attention and mothering • Lovic & Fleming, 2004; Lovic, in prep Gonzalez, Steiner, & Fleming., in prep Fleming & Gonzalez, 2008-attention and mat behavior-humans Numan et. al., 2007-di agonist and mat behavior rat (Li & Fleming, 2004ab; Numan et al., 2005; Stern & Lonstein, 2001-da antagonists and mb (Fleming, Korsmit, & Deller, 1994)- da antagonists and cpp • attentio

  8. Stimulus Salience Reward LIKING / WANTING

  9. Pup Retrieval General Licking Crouching

  10. P, E, Prl, Oxy Maternal responsiveness grows across pregnancy and peaks at parturition under influence of hormones CORT, Prl, Oxy HIGH MPOA limbic system Maternal Responsiveness Maternal experience LOW No maternal experience Day 16 Onset Pregnancy Parturition

  11. New Mother Rats are More Attracted to Lactating Nest Odors than to Clean or Diestrous Nest Odor Virgin Rats Show No significant Preference pup nest-clean=0 Pre-part Post-part Adapted from Bauer, 1983 See also Fleming et al.,, 1987, 1989

  12. Olfactory Preferences for Lactating Nest Odours also shown by Virgins Primed with (P & E) Hormones Fleming et al., 1987, 1989

  13. New Mother rats are more alerted by Pup Ultrasounds (pup ultrasounds vs. pup silent) than are Virgin Non-maternal Rats abcd b a c d BEFORE BIRTH PART AFTER BIRTH Farrell & Alberts, 2002

  14. Attractive stimuli become rewarding stimuli:New Mother Rats Show a Higher Level of Bar-press Responses Than do Virgins When Pups are Used as the Reward Stimuli (CRF schedule) Virgin levels Lee, Fleming et al., 2000

  15. New Mothers Prefer Pup-associated chamber to Cocaine-associated chamber in CPP (early postpartum period; days 4-7) Preference is Reversed to Non-postpartum Levels Later in Postpartum Period (days 12-15) cocaine pup Mattson, Williams, Rosenblatt, & Morrell (2000)

  16. Among Humans as well, New Mothers are Often Very Responsive to Their Infants and Find Infant Cues Attractive

  17. New Mothers (day 2pp) are More Attracted to Infant Body Odors, But Not to Control Odors, Than are Non-mothers (VAS, pleasantness) urine NEUTRAL Infant T-shirt spice Fleming, Corter, Franks, Surbey, Schneider., & Steiner, 1993

  18. Mothers with More Postpartum Experience tend to also Find Infant Odors to be More Attractive pos neg 52,585 2,210 120,370 15,318 1,10 105,375 Fleming, Corter et al., 1993

  19. On self-report measures (VAS) Mothers are more alerted by infant cries than are non-mothers Stallings et al., 2002 VAS cry stimuli Heart-rate monitor

  20. Using auditory Event Related Potentials (N100) , mothers are more alerted to infant cries than are non-mothers - however they are also more alerted to a novel tone-hence, effects are non-specific Purhonen et al., 2001; in press

  21. With Postpartum Experience New Mothers Become Increasingly More Positive About the Baby- and less positive about their partners(DON’T WORRY, IT RETURNS IN TIME FOR THE NEXT BABY) Fleming, Ruble, Flett, & Van Wagner, 1990

  22. DOING ATTENTION (selective,flexibility) Maternal attentiveness and sensitivity

  23. General Licking

  24. Mothers Exhibiting Higher Levels of Selective Attention Show Increased Pup Licking , and fewer movements into and out of nest ATTENTION (ID/ED Task) r=0.62, P<.05 R=-0.667 attention Licking Lovic & Fleming, 2004; Lovic, in prep

  25. Human Mothers also show large variations in Maternal ‘Sensitivity’ and Contingent Responding

  26. More Variation

  27. Mothers who Show Reduced Attention (on CANTAB: Set-Shifting Task) also Show Reduced Maternal Sensitivity Ainsworth Sensitivity Rating Scales Attention ED Shift on CANTAB Maternal Sensitivity -.25 Cambridge Neuropsychological Test Automated Battery Administered via a touch screen computer Measures components of executive functioning; . Gonzalez, Steiner, & Fleming., in prep Fleming & Gonzalez, 2008 Numbers=stand. β weights

  28. Summary • Pups are first attractive, then rewarding, to the new mother • Rewarding properties of pups enhanced by hormones and by experience • Rewarding and salient pups regulate mothers’ approach and contact with the young. They enhance her motivation to mother • To mother ‘sensitively’ and appropriately mothers must not only be motivated, but must also be attentive to the infant, and show flexibility; HENCE, SHOW GOOD EXECUTIVE FUNCTION

  29. WHAT ABOUT THE BRAIN?

  30. MATERNAL CIRCUIT: Brain Areas Associated with Maternal/Associated Behaviors MPOA is the FINAL COMMON PATH Inhibition of Maternal Behavior Olfactory Bulb Odor of Pups MPFC NA VMH Reinforce/ Memory attention VP MPOA MAM VTA Fear system mPFC:ATTENTION, Impulsivity MPOA and VMH: Maternal Behavior AMYGDALA: Emotions NAcc:Stimulus Salience, Rewards Motivation

  31. MATERNAL CIRCUIT: Brain Areas Associated with Maternal/Associated Behaviors Here focus on the Nucleus Accumbens Inhibition of Maternal Behavior Olfactory Bulb Odor of Pups MPFC NA VMH Reinforce/ Memory attention VP MPOA MAM VTA Fear system mPFC:ATTENTION, Impulsivity MPOA and VMH: Maternal Behavior AMYGDALA: Emotions NAcc:Stimulus Salience, Rewards Motivation

  32. Dopamine Action in Nucleus Accumbens is important for the onset of maternal behavior • Dopamine receptor agonist(D1) enhances onset of maternal behavior (Numan et. al., 2007) • DA receptor antagonists (D1 &/ D2) • delay onset of maternal behavior, primarily retrieval (Li & Fleming, 2004ab; Numan et al., 2005; Stern & Lonstein, 2001) • block formation of a CPP preference for pup-paired box (over other box) (Fleming, Korsmit, & Deller, 1994)

  33. Infusions of DA antagonists into Nucleus Accumbens Immediately After a Maternal Experience also, Block Consolidation of Maternal Experience at retention D2 ANT (sulperide) CONT D1 ANT (SCH) D1&D2 ANT Parada et al., 2008

  34. Dopamine release is associated with mothering THREE MICRODIALYSIS STUDIES Dopamine is Released in the Nucleus Accumbens in response to pups and is affected by • Postpartum status • Hormones (gestational/part) • Maternal Experiences microdialysis studies assessing dopamine by HPLC Students on project: Veronica Afonso, Samantha King , Stephanie Grella, Natalia Pinzon , Christine Burton Diptendu Chatterjee

  35. COLLECTION: 1uL/min for 8-min NACsh SAMPLING PROCEDURE probe placement SAMPLING Non-Homecage HPLC: Output Data HPLC with ECD • See Afonso et al. TEST 1 (microdialysis samples collected at 1ul/min) TEST 1 (microdialysis samples collected at 1ul/min) TEST 1 (microdialysis samples collected at 1ul/min) TEST 1 (microdialysis samples collected at 1ul/min) TEST 1 (microdialysis samples collected at 1ul/min) TEST 1 (samples collected at 1ul/min) Pup-stimuli sampling (24 min, 3 samples) Food-reward stimuli sampling (8 min, 1 sample) TEST 1 (samples collected at 1ul/min) Pup-stimuli sampling (24 min, 3 samples) Food-reward stimuli sampling (8 min, 1 sample) TEST 1 (samples collected at 1ul/min) Pup-stimuli sampling (24 min, 3 samples) Food-reward stimuli sampling (8 min, 1 sample) Pup-stimuli sampling (24 min, 3 samples) Food-reward stimuli sampling (8 min, 1 sample) Pup-stimuli sampling (24 min, 3 samples) Food-reward stimuli sampling (8 min, 1 sample) TIME TIME Pup-stimuli sampling (24 min, 3 samples) Food-reward stimuli sampling (8 min, 1 sample) Baseline sampling (no stimuli) TIME Pup-stimuli sampling (24 min, 3 samples) Food-reward stimuli sampling (8 min, 1 sample) Baseline sampling (no stimuli) TIME Pup-stimuli sampling (24 min, 3 samples) Food-reward stimuli sampling (8 min, 1 sample) Baseline sampling (no stimuli) TIME Baseline sampling (no stimuli) Baseline sampling (no stimuli) CHOICE TASK After sampling, all females were given an 8-min choice task in sampling chamber (unteathered) Then, all females placed in homecage with 4 donor pups (replaced daily) for several days. TIME CHOICE TASK After sampling, all females were given an 8-min choice task in sampling chamber (unteathered) Then, all females placed in homecage with 4 donor pups (replaced daily) for several days. TIME CHOICE TASK After sampling, all females were given an 8-min choice task in sampling chamber (unteathered) Then, all females placed in homecage with 4 donor pups (replaced daily) for several days. Baseline sampling (no stimuli) TIME CHOICE TASK After sampling, all females were given an 8-min choice task in sampling chamber (unteathered) Then, all females placed in homecage with 4 donor pups (replaced daily) for several days. Baseline sampling (no stimuli) CHOICE TASK After sampling, all females were given an 8-min choice task in sampling chamber (unteathered) Then, all females placed in homecage with 4 donor pups (replaced daily) for several days. Baseline sampling (no stimuli) TEST 2 (2nd sampling and choice task) For postpartum and cycling females 4-5 days of homecage pup-experience. For hormone treated females, after responding maternally in homecage. For sham treated females no 2nd test was performed. TEST 2 (2nd sampling and choice task) For postpartum and cycling females 4-5 days of homecage pup-experience. For hormone treated females, after responding maternally in homecage. For sham treated females no 2nd test was performed. TEST 2 (2nd sampling and choice task) For postpartum and cycling females 4-5 days of homecage pup-experience. For hormone treated females, after responding maternally in homecage. For sham treated females no 2nd test was performed. TEST 2 (2nd sampling and choice task) For postpartum and cycling females 4-5 days of homecage pup-experience. For hormone treated females, after responding maternally in homecage. For sham treated females no 2nd test was performed. TEST 2 (2nd sampling and choice task) For postpartum and cycling females 4-5 days of homecage pup-experience. For hormone treated females, after responding maternally in homecage. For sham treated females no 2nd test was performed.

  36. Sprague-Dawley Intact Rats (N=11) Mated and have litter Lactating Cycling virgin 1. Postpartum Influence pups removed 6-12 hr prior to sampling and presented with pups (PND1). 1st pup experience at sampling. Afonso, King,Chatterjee, & Fleming, IN PREP

  37. New mother rats show sustained increased dopamine response in NAC to pup stimuli; virgins do not. Postpartum MATERNAL IN OWN CAGE, NOT IN DIALYSIS CHAMBER Cycling NOT MATERNAL IN OWN CAGE OR IN DIALYSIS CHAMBER Parity diff /baseline covariate also sig at 16 and 24

  38. DA effects are non-specific; All females show increased DA to FOOD-stimuli , however virgins show higher levels than do postpartum animals (reverse of pattern to pups) DA peaks quickly Cycling Postpartum

  39. Sprague-Dawely OVXed Rats (N=10) (P capsules removed 24 hr prior to sampling). Sham Salastic Capsules SHAM E + P Salastic Capsules HORMONE 1st Experience with pups. 2. Hormonal Influence Afonso, Burton, Novakov, & Fleming

  40. Hormonally-primed virgin rats show sustained increased dopamine response to pups in the absence of prior pup-experience; control sham animals do not. HORMONE NOT MATERNAL IN HOME CAGE OR IN CHAMBER BUT SNIFFING PUPS SHAM NOT MATERNMAL IN HOME CAGE OR IN CHANBER

  41. Sprague-Dawely Cycling Rats (N=31) Multiparous (n=11) Nulliparous (n=13) PARITY EXPERIENCE NonSensitized (n=5) Sensitized (n=8) NonSensitized (n=5) Sensitized (n=6) 3. Maternal Experience Influence PUP-SENSITIZATION EXPERIENCE Afonso, Grella, Chatterjee, & Fleming, 2008.

  42. Rats given previous mothering experience show only an initial dopamine response in NAC to pup stimuli, related to sniffing. Experience effects ARE ADDITIVE The multiparous sensitized animals showed the greatest DA response. pup Multiparous Sensitized Multiparous NonSensitized Nulliparous Sensitized Nulliparous NonSensitized Afonso, Grella, Chatterjee, & Fleming, 2008.

  43. MATERNAL CIRCUIT: Brain Areas Associated with Maternal/Associated Behaviors Here focus on the Medial Prefrontal Cortex Inhibition of Maternal Behavior Olfactory Bulb Odor of Pups MPFC NA VMH Reinforce/ Memory attention VP MPOA MAM VTA Fear system mPFC:ATTENTION, flexibility MPOA and VMH: Maternal Behavior AMYGDALA: Emotions NAcc:Stimulus Salience, Rewards Motivation

  44. Rats with Medial Prefrontal Lesions (NMDA) all Show Maternal retrievals, BUT they Show disrupted Sequencing of retrievals and reduced Licking Afonso, Lovic, et al., 2008;

  45. mPFC lesions also produce • reduced Attention • on a PPI task (attentional filtering) (Afonso et al., 2008) and • on an attention set shifting task (Birrel & Brown, 2000)

  46. fMRI Activation in the PFC (dl) occurs during Attentional Shifting • Figures show similar fMRI brain activation in macaque monkeys and humans during successful shifts in attention (Nakahara et al. 2002) Macaque Monkey Human

  47. Frontal sites associated With performance on executive And attention tasks are also Activated by infant cues Gonzalez et al., 2008

  48. THESE BEHAVIORAL AND NEUROLOGICAL SYSTEMS ARE SET UP BY EARLY NEONATAL AND PREWEANING EXPERIENCES Gonzalez & Fleming, 2001; Lovic & Fleming, 2004

  49. Pups experiencing early maternal/litter deprivation show reduced attention, reduced licking as well as structural and functional changes in NAC and MPFC ‘Anxiety’ Elevated plus maze CORT Response to stress Early Experience (prenatal+post-partum) Severity Maternal Licking/ Crouching Attention (prepulse inhibition 84) Synapse Integrity NAC and MPFC ELEVATED BASAL DA Activity Open-field test Burton, Lovic, & Fleming, 2006 See also Zhang et al., 2005 Afonso et al., 2007; 2008; in prep

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