Sexually dimorphic organization of open field behavior following moderate prenatal alcohol exposure

Abstract

Background Prenatal alcohol exposure (PAE) can produce deficits in a wide range of cognitive functions but is especially detrimental to behaviors requiring accurate spatial information processing. In open field environments, spatial behavior is organized such that animals establish “home bases” marked by long stops focused around one location. Progressions away from the home base are circuitous and slow, while progressions directed toward the home base are non‐circuitous and fast. The impact of PAE on the organization of open field behavior has not been experimentally investigated. Methods In the present study, adult female and male rats with moderate PAE or saccharin exposure locomoted a circular high walled open field for 30 minutes under lighted conditions. Results The findings indicate that PAE and sex influence the organization of open field behavior. Consistent with previous literature, PAE rats exhibited greater locomotion in the open field. Novel findings from the current study indicate that PAE and sex also impact open field measures specific to spatial orientation. While all rats established a home base on the periphery of the open field, PAE rats, particularly males, exhibited significantly less clustered home base stopping with smaller changes in heading between stops. PAE also impaired progression measures specific to distance estimation, while sex alone impacted progression measures specific to direction estimation. Conclusions These findings support the conclusion that adult male rats have an increased susceptibility to the effects of PAE on the organization of open field behavior.

Organization of spontaneous spatial behaviors under dark conditions is unaffected in adult male and female long–Evans rats after moderate prenatal alcohol exposure.

“…In the present study, mPAE and SACC rats were given a single 30-min exposure to an open field in a testing room that was made completely dark. Consistent with previous reports (Donaldson et al, 2019;Osterlund Oltmanns et al, 2022), we found that general locomotion decreased across the test session as measured by a reduction in travel distance, an increased stop duration, and a progressive increase in stops located along the edge of the maze environment. As expected, progression features (path directness) also varied with the length of the trip such that shorter trips were associated with more direct progressions and a more consistent topography relationship between progression peak speeds.…”

“…PAE (moderate or high doses) can also alter the expression of anxiety-like behaviors in open environments (Osborn et al, 1998;Staples et al, 2013;Wang et al, 2023). It is important to note, however, that in our previous work using a lighted open field (Osterlund Oltmanns et al, 2022), we failed to detect group differences in the percentage of stops localized along the edge of the open field (a putative anxiety-like phenotype). Additional work is therefore needed to investigate this possibility using a battery of tests for anxiety-like behavior (e.g., elevated plus maze).…”

“…Female adult rat breeders (Harlan Industries, Indianapolis, Indiana, United States) were exposed to a voluntary ethanol drinking paradigm using previously described procedures (Davies et al, 2023; Osterlund Oltmanns et al, 2022). Prepregnancy ethanol consumption was monitored daily during a 4-hr period for at least 2 weeks, and mean daily ethanol consumption was determined for each female rat.…”

“…Furthermore, damage to the hippocampal formation can disrupt the organization of stopping, progression, and home base behaviors (Clark et al, 2005; Gorny et al, 2002; Hines & Whishaw, 2005; Lehmann et al, 2007; Wallace et al, 2002; Whishaw et al, 1994). In a previous study, we found moderate PAE (mPAE) rats exhibited alterations in their open-field behavior under lighted conditions in adulthood (Osterlund Oltmanns et al, 2022), with a sex-specific decrease in the stability of home base behavior, and organization of progression behaviors in male mPAE rats. It is unknown whether this pattern of behavior would generalize, or possibly expand, to include both sexes when animals are more reliant on self-motion cues to guide behavior.…”

“…Subjects included eight female and eight male Long-Evans rats from each of the two prenatal treatment groups obtained from the University of New Mexico Health Sciences Animal Resource Facility (see the Breeding Colony and Ethanol Consumption Procedure section). The sample size in the present study is based on the sample size used in our previous work demonstrating significant spatial behavior impairments after mPAE in a lighted open field (Osterlund Oltmanns et al, 2022). A similar sample size has also been used in other studies observing spatial behavior and hippocampal place cell impairments after mPAE (Harvey et al, 2020;Sanchez et al, 2019) and in other animal models in open-field tests (Banovetz et al, 2021;Blankenship et al, 2016Blankenship et al, , 2017Donaldson et al, 2018).…”