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. Author manuscript; available in PMC: 2013 Oct 1.
Published in final edited form as: Neurosci Biobehav Rev. 2012 Jul 20;36(9):1985–2006. doi: 10.1016/j.neubiorev.2012.07.003

Table 3.

Summary of results of studies on early life stress and spatial/relational memory in the adult

Procedure Early Life Manipulation Strain Sex Age Result Reference
Morris Water Maze (MWM) Handling (15-min; PN1-22) Long-E male aged decreased aging impairments Meaney et al. 1988
Handling (10-min * 2/day; PN1-21) Roman both? aged enhanced RHA (path length) Escorihuela et al 1995
Handling (10-min; PN1-22) SD male adult enhance w/stress Pham et al. 1997
Handling (15-min; PN1-21) SD male adult n.s. Vallee et al. 1997
Handling (15-min; PN1-21) SD male adult n.s. Vallee et al. 1999
Handling (15-min; PN1-21) SD male aged n.s. Vallee et al. 1999
Handling + stroking (3-min; PN1-21) Long-E both adult enhanced (latency; improvement score) Tang et al 2001
Handling (10-min; PN1-10) Wistar both adult Impaired females Noschang et al 2010
Handling. (15-min; PN2-14) Long-E male adult n.s. Hout et al 2002
Handling (15-min; PN1-22) Wistar male aged enhanced (latency) Lehmann et al. 2002
Handling (15-min; PN2-9) SD male adult enhanced (latency) Fenoglio et al 2005
Handling (15-min*3/day; PN4-21) Long-E both adult n.s. Gibb & Kolb 2005
Handling (15-min; PN1-21) Wistar male adult enhanced w/stress Garoflos et al 2005
Handling (15-min; PN1-22) Wistar both adult enhanced w/stress males Stamatakis et al 2008
Neonatal isolation (3-min; PN1-PN21) Roman both? aged enhanced Fernandez-Teruel et al 1997
Neonatal isolation (15-min; PN1-21) Wistar both adult n.s. Pryce et al 2003
Novel environment (3-min; PN1-21) Long-E male 7-mon enhanced Tang et al 2006
Mat. Sep. (24-hr; PN3) Wistar both adult impaired Oomen et al 2010
Mat. Sep. (24-hr; PN3) Wistar female adult n.s. Oomen et al 2011
Mat. Sep. (24-hr; PN4) Wistar both adult enhanced reversal learning Lehmann et al 1999
Mat. Sep. (24-hr; PN9) Wistar both adult enhanced reversal learning Lehmann et al 1999
Mat. Sep. (24-hr; PN18) Wistar both adult enhanced reversal learning Lehmann et al 1999
Mat. Sep. (24-hr; PN3) Brn Norw male adult impaired (latency, distance acq, rev) Oitzel et al. 2000
Mat. Sep. (24-hr; PN3) Brn Norw male aged n.s. Oitzel et al. 2000
Mat. Sep. (3-hr; PN2-14) Long-E male adult impaired (latency; distance) Hout et al 2002
Mat. Sep. (3-hr; PN2-21) Wistar male adult Impaired Aisa et al 2009
Mat. Sep. (3-hr; PN2-21) Wistar male adult impaired Aisa et al 2009
Mat. Sep. (3-hr; PN2-21) Wistar male adult impaired Solas et al 2010
Mat. Sep. (3-hr; PN2-21) Wistar male aged impaired Solas et al 2010
Mat. Sep. (6-hr; PN12, 14, 16,&18) Wistar male aged trend enhance (latency) Lehmann et al. 2002
Mat. Sep (12-hr; PN9 and PN11) Wistar male adult impaired (path length; latency) Garner et al 2007
Mat. Sep. (3-hr; PN2-14) SD both adult Impaired (quadrant time) Hui et al 2011
Mat. Sep. (3-hr; PN2-21) Wistar both? adult impaired retention; n.s. acq Aisa et al 2007
Mat. Sep. (24-hr; PN9) Wistar male adult n.s. Choy et al 2008
Neonatal isolation (6-hr/day; PN15-21) Long-E both adult enhanced Frisone et al 2002
Neonatal isolation (1-hr/day; PN2-9) SD male adult impaired (latency) Huang et al. 2002
Neonatal isolation (4-hr; PN1-21) Wistar both adult enhanced (distance) Pryce et al 2003
Neonatal isolation (1-hr/day; PN2-9) SD male adult n.s. Lai et al 2006
Limited nesting (PN2-PN9) SD male adult trend impairment Brunson et al 2005
Limited nesting (PN2-PN9) SD male aged impaired Brunson et al 2005
Limited nesting (PN2-PN9) SD male aged impaired (quadrant time; latency) Ivy et al 2010
CRH (PN10) SD male adult trend impairment Brunson et al 2001
CRH (PN10) SD male adult impaired Brunson et al 2001
CRH (PN10) SD male aged impaired Brunson et al 2001
CRH antagonist (PN10-17) SD male adult enhanced (latency) Fenoglio et al 2005
CRH antagonist (PN10-17) SD male aged n.s. (quadrant time; latency) Ivy et al 2010
Cort (PN1-21) Wistar male adult enhanced Catalani et al 1993
Cort (PN1-21) Wistar female adult enhanced Catalani et al 2002
Artificial rearing SD female adult some enhancements in retention Levy et al 2003

Radial arm maze (RAM) Handling (PN1-21; 15-min) SD male aged decrease aging impair(<work mem err) Vallee et al. 1999
Neonatal isolation (6-hr; PN15-21) Long-E both adult >working errors in males; n.s. females Sandstrom 2005
Neonatal isolation (6-hr; PN15-21) Long-E males adult > working errors; n.s. ref memory Sandstrom & Hart 2005
CORT (PN1-PN12) Wistar both? adult initial better working memory Roskoden et al 2005a
Artificial rearing SD female adult decrease latency during initial sessions Levy et al 2003

Circular maze (CM) Neonatal isolation (15-min; PN1-21) SD both adult n.s. Kosten et al 2007a

Can test (CT) Neonatal isolation (15-min; PN2-21) Wistar male aged enhanced correct responses Cannizzaro et al 2005
Neonatal isolation (15-min; PN2-21) Wistar male adult enhanced ref mem & correct responses Cannizzaro et al 2006

Active avoidance (AA) Handling (2-min; PN1-21) Maudsley female adult enhanced Powell & North-Jones 1974
Handling (15-min; PN1-21) SD female adult enhanced Nunez et al 1995
Neonatal isolation (3-min; PN2-15) SD & L-E both adult impaired (cort response) Weinberg & Levine 1977
Neonatal isolation (15-min; PN1-21) Wistar both adult enhanced Pryce et al 2003
Mat. Sep. (24-hr; PN4) Wistar both adult impaired males Lehmann et al 1999
Mat. Sep. (24-hr; PN9) Wistar both adult enhanced males Lehmann et al 1999
Mat. Sep. (24-hr; PN18) Wistar both adult n.s Lehmann et al 1999
Mat. Sep. (6-hr; PN12, 14, 16,&18) Wistar both adult enhanced acquisition Lehmann et al., 2000
Mat. Sep. (4-hr/day; PN1-21) SD both adult impaired Weiss et al., 2001
Mat. Sep. (3-hr; PN1-16) Wistar female adult increased avoidance responses Day 1 Schable et al 2007
Neonatal isolation (4-hr; PN1-21) Wistar both adult enhanced Pryce et al 2003
Neonatal isolation (4-hr; PN5-11) SD male adult n.s (2-way shuttle) Toth et al. 2008
Cort (PN1-21) Wistar male aged enhanced Catalani et al 2000
Cort (PN1-21) Wistar female aged enhanced Catalani et al 2002

T-maze (TM) Neonatal isolation (PN1-22; 3-min) Long-E both adult enhanced reversal learning Wong & Judd 1973
Tact stim/neo iso (<5-min; PN2-9) Wistar male adult enhanced delayed alternation Zhang & Cai 2008
Tact stim/neo iso (<5-min; PN10-17) Wistar male adult enhanced delayed alternation Zhang & Cai 2008
Tact stim/neo iso (1-hr; PN2-9) Wistar male adult enhanced delayed alternation Zhang & Cai 2008
Tact stim/neo iso (1-hr; PN10-17) Wistar male adult enhanced delayed alternation Zhang & Cai 2008
Mat. Sep (12-hr; PN9 and PN11) Wistar male adult n.s. Garner et al 2007
Mat. Sep. (24-hr; PN9) Wistar male adult no effect on working memory Choy et al 2008

Y-maze (YM) Handling (PN1-21; 15-min) SD male adult n.s. (4,6,8,24-hr ITI) Vallee et al. 1997
Handling (PN1-21; 15-min) SD male adult n.s. Vallee et al. 1999
Handling (PN1-21; 15-min) SD male aged decrease aging impairment 24- not 8-hr Vallee et al. 1999
Tact stim+novel envt (Pn1-21; 15-min) Wistar both adult enhance males; n.s. females Daskalakis et al 2009
Tact stim (PN1-21; 15-min) Wistar both adult enhance males; impair females Daskalakis et al 2009
Mat. Sep. (24-hr; PN9) Wistar male adult n.s. Choy et al 2008

Object recognition (OR) Handling (15-min; PN2-9) SD male adult enhanced 24-hr Fenoglio et al 2005
Neonatal isolation (15-min; PN1-21) SD both adult enhanced both sexes 3- and 24-hr test Kosten et al 2007a
Mat. Sep. (3-hr; PN2-21) Wistar male adult impaired 1-hr Aisa et al 2007
Mat. Sep. (3-hr; PN1-10) Wistar male adult impaired 24-hr Benetti et al 2009
Neonatal isolation (1-hr/day; PN2-9) SD both adult impaired 24-hr but not 3-hr Kosten et al 2007b
Mat. Sep. (3-hr; PN1-15) Wistar male adult impaired 24-hr but not 1.5-hr Martins de Lima et al 2011
Mat. Sep. (3-hr; PN2-21) Wistar male adult impaired Solas et al 2010
Mat. Sep. (3-hr; PN2-21) Wistar male aged impaired Solas et al 2010
Limited nesting (PN2-PN9) SD male adult impaired 24-hr Brunson et al 2005
Limited nesting (PN2-PN9) SD male aged impaired 24-hr Ivy et al 2010
CRH (PN10) SD male aged impaired 24-hr Brunson et al 2001
CRH antagonist (PN10-17) SD male adult enhanced 24-hr Fenoglio et al 2005
CRH antagonist (PN10-17) SD male aged n.s. 24-hr Ivy et al 2010

Social memory (SM) Handling (1-min; PN1-10) Wistar both adult n.s. Todeschin et al 2009
Novel environment (3-min; PN1-21) Long-E male adult enhanced 24-hr Reeb-Sutherland & Tang 2011
Mat. Sep. (3-hr; PN1-10) Wistar male adult impaired 24-hr Benetti et al 2009
Mat. Sep. (3-hr; PN1-14) Wistar male adult impaired 1-hr Lukas et al 2011
Artificial rearing SD female adult Impaired 24-hr Levy et al 2003