Sex and Time-of-Day Impact on Anxiety and Passive Avoidance Memory Strategies in Mice.

Antonia Alonso,Miroljub Popović,Ana Belén Meseguer Henarejos,María Caballero Bleda,Nicanor Morales-Delgado,Natalija Popović,Dubravko Bokonjić

doi:10.3389/fnbeh.2020.00068

Abstract

In humans, anxiety and cognitive processes are age, gender, and time of day dependent. The purpose of the present study was to assess whether the time of day and sex have an influence on anxiety and emotional memory in adult mice. Light-dark and passive avoidance (PA) tests were performed at the beginning and at the end of the light cycle, defined as Zeitgeber time (ZT) ZT0–2.5 and ZT9.5–12, respectively. A baseline difference in anxiety was not found, but on the 24 h retention trial of the PA test, females presented longer latencies to enter into the dark compartment at the ZT0–2.5 time point of the day. The data from the second test day (PA reversal trial) indicated that some animals associated the dark compartment with an aversive stimulus (shock), while others associated the aversive stimulus with crossing from one compartment to another. At the ZT9.5–12, female mice mainly related the aversive stimulus to transferring from one compartment to another, while male mice associated darkness with the aversive stimulus. There was a negative correlation between the frequency of light-dark transitions in the light-dark test and the PA latency on the 24 h retention trial in males tested at ZT0–2.5. The PA latency on the reversal and 24 h retention trials negatively correlated with a risk assessment behavior in male mice tested on ZT0–2.5 and ZT9.5–12, respectively. In conclusion, our data reveal that the impact of motor activity and risk assessment behavior on PA memory formation and applied behavioral strategies are time of day and sex dependent.

Highlights

The circadian rhythm is a 24-h internal regulator that coordinates physiological and behavioral activities with diurnal environmental variation
In the group of male mice tested at the ZT0–2.5, there existed a significant negative correlation between the latency to enter into the dark compartment and the risk assessment of both dark and light compartments
In male mice tested at the ZT9.5–12, a negative correlation was found between the latency to re-enter into the light compartment and the number of light-dark transitions

Summary

Introduction

The circadian rhythm is a 24-h internal regulator that coordinates physiological and behavioral activities with diurnal environmental variation. Studies based on morningness-eveningness individual preferences indicated the existence of three circadian typologies in humans (morning-, intermediate-, and evening-type; Kerkhof, 1985). Adan and Natale (2002) demonstrated gender differences in circadian typology, indicating that women present a more pronounced morningness preference than men. Passive Avoidance: Sex and Time-of-Day. Eveningness is generally negatively related to academic achievement (Preckel et al, 2011; Fabbian et al, 2016) and gender studies have indicated that female secondary school pupils and undergraduate students had better grade point averages (GPA) than male students (Chee et al, 2005; Freudenthaler et al, 2008). The timing of examination negatively affected the obtained scores if the exam was performed in a period of the day that did not coincide with individual circadian typology (van der Vinne et al, 2015). This study suggests that exam schedules should be adjusted to the period between 12:45 h and 15:00 h, since this interval gives equal academic opportunities to all chronobiological types

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