Predator odor exposure of rat pups has opposite effects on play by juvenile males and females

Abstract

Juvenile social play behavior is one of the earliest sexually differentiated behaviors to emerge. In rats, as with most other species that play, males engage in more rough-and-tumble play compared to females. Exposure to early life adversity is a major driver of adult health and can manifest differently in males and females. However, the effects of adverse early life exposure on play behavior in the juvenile period are poorly understood. To address this, male and female neonatal rats were exposed to predator odor (PO), for 5 min/day on PN1-PN3. At the time of exposure to PO, both male and female pups suppressed ultrasonic vocalization and displayed more freezing behavior. Circulating corticosterone increased in males immediately following PO exposure but not in females. The enduring effects of PO exposure were opposite in males compared to females in that PO exposed males decreased social play, while PO exposed females increased play behavior compared to same sex controls. PO exposure did not significantly affect cell genesis in the neonatal dentate gyrus of either sex. PO exposure did not affect anxiety-like behavior assessed in the juvenile period or in adulthood, nor did it affect social interactions in adulthood. This work provides new insight into how sex may interact with adverse early life events to contribute to development of the social consequences of such exposures.

Sex differences in juvenile play behavior differ among rat strains

“…We were surprised to find a lack of sex differences among Sprague‐Dawley subjects in either test, as almost all published studies have documented sex differences in this strain (Argue & McCarthy, ; Argue et al, ; Casto et al, ; Edelmann et al, ; Hotchkiss et al, ; Jessen et al, ; Krebs‐Kraft et al, ; Kurian et al, ; Olesen et al, ; Olioff & Stewart, ; Stockman & McCarthy, ; Wood et al, ), with the exception of Himmler et al () and those that found female‐biased sex differences (Field et al, ; Madden & Zup, ; Mychasiuk et al, ; Wood et al, ). However, the context in which our rats played differed in at least one way from that used in any of these previous studies.…”

“…However, the context in which our rats played differed in at least one way from that used in any of these previous studies. Many tested play in larger groups (Argue et al, ; Casto et al, ; Edelmann et al, ; Jessen et al, ; Krebs‐Kraft et al, ; Kurian et al, ; Olesen et al, ), some tested subjects in a novel environment (Argue & McCarthy, ; Argue et al, ; Krebs‐Kraft et al, ; Olioff & Stewart, ; Stockman & McCarthy, ; Wood et al, ), and others isolated subjects prior to testing (Hotchkiss et al, ; Wood et al, ). Therefore, Sprague‐Dawley males may be particularly sensitive to those environmental factors.…”

“…Among studies using Long‐Evans rats, approximately half report sex differences; although all of these sex differences are male‐biased, they range from males playing slightly more to about twice as much as females (Meaney & McEwen, ; Meaney, Dodge, & Beatty, ; Meaney, Stewart, Poulin, & McEwen, ; Parent & Meaney, ; Pellis & Pellis, ; Thor & Holloway, ). In contrast, most studies in Sprague‐Dawley rats have reported sex differences, at least in the summed frequency of all play behaviors (Argue & McCarthy, ; Argue et al, ; Casto, Ward, & Bartke, ; Edelmann, Demers, & Auger, ; Hotchkiss, Ostby, Vandenbergh, & Gray, ; Jessen, Kolodkin, Bychowski, Auger, & Auger, ; Krebs‐Kraft, Hill, Hillard, & McCarthy, ; Kurian, Bychowski, Forbes‐Lorman, Auger, & Auger, ; Olesen, Jessen, Auger, & Auger, ; Olioff & Stewart, ; Stockman & McCarthy, ; Wood, Bannoura, & Johanson, ), even when 24 hr isolation periods are used and subjects are tested with only one stimulus animal (Hotchkiss et al, ; Wood et al, ). Sprague‐Dawley rats seem to have more dramatic sex differences, with many finding that males play more than three times than females (Casto et al, ; Hotchkiss et al, ; Jessen et al, ; Kurian et al, ; Olesen et al, ; Stockman & McCarthy, ).…”

“…In contrast, most studies in Sprague‐Dawley rats have reported sex differences, at least in the summed frequency of all play behaviors (Argue & McCarthy, ; Argue et al, ; Casto, Ward, & Bartke, ; Edelmann, Demers, & Auger, ; Hotchkiss, Ostby, Vandenbergh, & Gray, ; Jessen, Kolodkin, Bychowski, Auger, & Auger, ; Krebs‐Kraft, Hill, Hillard, & McCarthy, ; Kurian, Bychowski, Forbes‐Lorman, Auger, & Auger, ; Olesen, Jessen, Auger, & Auger, ; Olioff & Stewart, ; Stockman & McCarthy, ; Wood, Bannoura, & Johanson, ), even when 24 hr isolation periods are used and subjects are tested with only one stimulus animal (Hotchkiss et al, ; Wood et al, ). Sprague‐Dawley rats seem to have more dramatic sex differences, with many finding that males play more than three times than females (Casto et al, ; Hotchkiss et al, ; Jessen et al, ; Kurian et al, ; Olesen et al, ; Stockman & McCarthy, ). However, four studies have reported some female‐biased sex differences in this strain (Field, Whishaw, Pellis, & Watson, ; Madden & Zup, ; Mychasiuk, Hehar, Farran, & Esser, ; Wood, Molina, Wagner, & Spear, ).…”

“…2003; Hotchkiss et al, 2003;Jessen et al, 2010;Kurian et al, 2008;Olesen et al, 2005;Stockman & McCarthy, 2017). However, four studies have reported some female-biased sex differences in this strain (Field, Whishaw, Pellis, & Watson, 2006;Madden & Zup, 2014;Mychasiuk, Hehar, Farran, & Esser, 2014;Wood, Molina, Wagner, & Spear, 1995).…”