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/lp/springer-journals/memory-and-exploratory-behavior-impairment-in-ovariectomized-wistar-MTBWO00Ynr
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- Springer Journals
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- Copyright © 2018 by The Author(s)
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- Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
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- 1744-9081
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- 10.1186/s12993-018-0146-7
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Abstract
Background: Estrogen deficiency is linked to changes in several physiological processes, but the extent to which it associates with cognitive changes in menopause context is controversial. Rationale: We evaluated the impact of ovariectomy on memory processes and normal exploratory behavior in Wistar rats. Methods: Young adult rats (4–6 months) were either ovariectomized (OVX group) (N = 10), sham operated (N = 10), or untouched (naïve controls) (N = 8). Afterwards, they were monitored for 12 weeks during which their cognitive functions were evaluated at first week (S1), second (S2), every 3 weeks (S5, S8) and then at week 12 (S12) using: (i) object recognition test to evaluate the short-term and long-term non-spatial memory; (ii) the object placement test to assess the spatial memory; and (iii) normal exploratory behavior components like locomotor and vertical activities in an open field arena. Results: Marked changes in ovariectomized rats were observed in long-term non-spatial memory (~ 40% change vs. naïve and sham, P < 0.001) and spatial memory (~ 30% change, P < 0.05) from S2. Instead, from S5 the exploratory behavior was affected, with decreases in line crossing and rearing episode numbers (~ 40% change, P < 0.01), and in the time spent in the center of open field arena (~ 60% change, P < 0.01). Conclusions: Our findings support the involvement of sex hormones in cognitive functions in female rats and sug- gest that controversy on the importance of cognitive affections in menopause context may emerge from differences between short-term and long-term memory processes. Keywords: Ovariectomy, Memory, Object recognition, Spatial memory, Ovarian hormones, Wistar rats Background of ovarian functions affects most physiological processes, Menopause is a normal component of aging in women including cognitive and motor functions, although, the accompanied by clinical signs and higher risk for devel- extent to which central nervous system functions are oping diseases such as osteoporosis, cardiovascular dis- affected in postmenopausal women is not clear. How - eases, solid cancers, and neurodegenerative diseases [1]. ever, it is widely accepted that compromised memory and Menopause and the clinical concerns it raises emerge motor functions reported in menopausal women may from definitive cessation of menstrual cycle resulting emerge mainly from declines in steroid hormones’ levels, from the cessation of ovarian functions, including the particularly estradiol [2]. Notably, brain structures like production of estrogens and progesterone. The cessation the hippocampus, a key player in learning and memory processes, need high levels of estrogens obtained partly by intrathecal production [2, 3]. In the last decades, experimental models of meno- *Correspondence: sefirin.djiogue@gmail.com Laboratory of Animal Physiology, Department of Animal Biology pause have been used for getting translationally rel- and Physiology, Faculty of Science, University of Yaounde I, P.O. Box 812, evant insights in the role of estrogens in cognitive Yaoundé, Cameroon and movement disorders [4, 5]. Ovariectomy is widely Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Djiogue et al. Behav Brain Funct (2018) 14:14 Page 2 of 8 used to induce a menopause-like status in laboratory Methods rodents. It results in definitive cessation of ovarian Animals hormones’ production [6], and mimics some features Female Wistar rats (N = 28, 4–6 months old, 190– of human menopause. There is controversy on the spe- 220 g) were obtained from the animal facility of the cific features with translational potential in this model, University of Yaoundé I (Cameroon). Rats were group which contributes to disagreements on the importance housed (N = 4 or 5) in standard cages under 12:12 h of cognitive affections in menopause context [7]. Over- light–dark cycle, with ad libitum access to food and tap all, research reports in rodents and non-human pri- water. Rats were acclimatized to the testing room envi- mates suggest that sexual hormones are key players in ronment (for 1 week), then they were randomly divided the maintenance of cognitive abilities [5, 8]. Studies in into three groups: (i) ovariectomized animals (N = 10) ovariectomized animals showed significant alterations (OVX group); (ii) sham-operated animals (N = 10); and in the structure and function of hippocampal and cor- naïve control animals (N = 8). tical circuits accompanied by poor performance in sev- All procedures were approved by institutional review eral cognitive tasks [9–12]. These observations were board. Animals were handled in accordance with Euro- confirmed in humans, as estrogen therapy improved pean Commission’s Guidelines for Laboratory Animal performances in cognitive tasks, verbal memory, and Use and Care (EEC Directive of 1986; 86/609/EEC). executive functions of perimenopausal women [13]. Many reports confirmed the beneficial effects of estro- Ovariectomy gen replacement therapy on various physiological Surgery was performed under anesthesia induced by functions in ovariectomized animals as well [10, 13]. Valium (10 mg/kg, i.p) and ketamine (50 mg/kg, i.p), However, controversy remains on the extent of altera- using standard procedures. Briefly, anesthesia was tions mediated by ovariectomy in these physiological confirmed by reduced respiratory rate and absence of functions. For instance, although various studies sug- response to gentle pinching of footpad. Ventral incision gest that ovariectomy may impair object recognition was made through the skin on the right flank. In the ability [10, 14], the importance of such affection is OVX group, the ovary, oviduct, and top of the fallopian controversial. It was hypothesized that such contro- tubes were clamped and removed. In sham-operated versy may emergence from differences in experimental rats, same surgical procedure was performed, but ova- protocols, particularly in time intervals between ova- ries were just palpated, not removed. Skins and abdom- riectomy and object recognition testing [9, 15]. inal walls of animals of both groups were sutured, and Surprisingly, considering the importance and trans- animals were returned to their cages. lational potential of information on the effects of chronic ovarian hormone deprivation on memory Memory and exploratory behavior assessment processes and other cognitive functions, data com- Procedures paring the effects of ovariectomy on short-term and After the recovery period (1 week), open field (OF), long-term memory in rodents, are scarce. Research in object recognition, and object placement tests were rodents and non-human primates’ shows that gonadals performed 1, 2, 5, 8 and 12 weeks after surgery (S1, S2, hormones are beneficial for the maintenance of cogni- S5, S8, and S12). Tests were performed during 3 con- tive abilities [5, 8]. However, it should be noted that secutive days: OF testing in day 1 (used also as animal most animal research are based on the replacement habituation phase to the arena), object recognition of gonadal hormones, usually estrogens, with ani- test in day 2, and object placement test on day 3. The mals ovariectomized (OVX). Few studies have directly apparatus consisted of a wooden box (40.5 × 40.5 cm investigated the effects of OVX on short-term or long- basis, 30-cm walls’ height), with a computerized cam- term memory [11, 14] or locomotor and exploratory era on top (45°, for capturing both vertical and hori- activity in rodents. One study conducted through- zontal activities in the arena). The monitor was placed out 7 weeks have assessed the short-term memory in an adjoining room. Throughout testing, the door of tasks (OR and OP) of ovariectomized young and the testing room was closed, and animals were video intact rats for 7 consecutive weeks. In this study, we recorded. The arena was cleaned with 70% ethanol wanted to describe the evolution of both short-term between rats. and long-term memory over a longer study period. On this basis, we assessed the effects of ovariectomy Memory evaluation on normal exploratory behavior, as well as changes in Testing procedures were based on standard proto- short-term and long-term memory in Wistar rats for cols for object recognition and object placement tests, 12 weeks. Djiogue et al. Behav Brain Funct (2018) 14:14 Page 3 of 8 whose tasks are based on the natural affinity of rats explore the arena and its objects (where applicable). Its for novelty [10, 16, 17]. Four plastic objects (~ 4–6 cm exploratory activities were video recorded for 5 min, then height and width,) were used: two identical objects (O1 scored offline. and O2) and two objects differing in color and shape (O3 and O4) were used. Memory evaluation was per- Object recognition assessment (day 2) Rats explored formed in 3 phases: habituation phase, object recogni- the same arena, but with two identical objects (O1, O2) tion evaluation phase, and object placement evaluation placed as shown in Fig. 2b). After 3-h (short-term mem- phase (Fig. 1). ory assessment) or 24-h (long-term memory assessment), the animals explored the arena again, but object O1 was Habituation phase (day 1) Rats explored an empty replaced by a novel object (O3) (Fig. 2b inset). open field arena (Fig. 1a) similar to OF test procedures [18]. In this phase and in each of the following, a rat was Object placement assessment (day 3) Rats explored the introduced in the open field arena and allowed 5-min to same arena, but object O3 was replaced by a novel object Fig. 1 Testing procedure. a Habituation phase (day 1). b Object recognition assessment (day 2): habituation to objects (b) and object recognition test (inset). c Spatial memory assessment (day 3): habituation to objects (c) and object recognition test (inset) Fig. 2 Object recognition assessment. Relative exploration time of novel objects (% of total object exploration time) throughout the first 12 weeks following surgery with 3-h inter-trial time (a) or with 24-h inter-trial time (b). Treatment groups: ovariectomized animals receiving vehicle solution (OVX) (N = 10), sham operated animals (N = 10), and naïve animals (N = 8). Dashed line indicates chance performance of task, which is the same amount of time spent exploring the old and novel object. ANOVA followed by Bonferroni test: *P < 0.05 vs. sham group; ***P < 0.001 vs. sham group. Data are mean ± SEM Djiogue et al. Behav Brain Funct (2018) 14:14 Page 4 of 8 Long‑term memory (O4) placed at the same location (Fig. 2c). After 3-h, the Figure 2b shows the effects of ovariectomy on long-term animals explored the arena again, but object O4 was object recognition ability in rats, throughout the first placed in a new location (Fig. 2c inset). 12 weeks following surgery. As observed for short-term memory assessment, all groups spent more time in the Data offline scoring Object exploration was when the exploration of the novel object than in the exploration of subject sniffed, whisked at, or looked at the object from the old one in the first week. Afterwards, sham and naïve less than 2 cm. Object relative time (exploration ratio) was animals kept novel object-old object time ratios above its exploration time expressed as a percent of total object 0.7 while OVX group ratios were lower than 0.6 (Fig. 2b). exploration time. At weeks 2 (t = 2.950, P < 0.05), 5 (t = 4.345, P < 0.001), 8 (t = 2.802, P < 0.05), and 12 (t = 2.756, P < 0.05) post- surgery, animals of the OVX group significantly failed to Exploratory behavior evaluation discriminate between the old and new objects. Analysis Habituation phase recordings (OF test) were scored of the post-surgical ratios by two-way ANOVA showed offline. Locomotor activity was evaluated by measur - a significant group effect (F = 16.33, P < 0.0001), without ing line crossing, i.e. the number of times the rat crossed significant week effects or group—week interactions. No grid lines drawn on the flour with all four paws. Other statistically significant difference was observed between exploratory behavior parameters scored included the sham and naive groups. total time spent in the central square of the open field arena (Fig. 1a) (an established indicator of anxiety), the Object placement number of rearing episodes (where rats stood on their Figure 3 shows the effects of ovariectomy on the explo - hind legs) (an established indicator of cognition: danger ration ratio of the new location, i.e. the ratio of the new assessment), and the number of grooming episodes (time location exploration time to old + new location explora- spent licking or scratching itself while stationary) (whose tion times, throughout the first 12 weeks following sur - absence is an established indicator of depression). gery in rats. In the first week post-surgery, all animals discriminated the novel location from the old one. From week 2 onward, sham and naïve groups’ exploration Statistical analysis Repeated measures ANOVA followed by Bonferroni test was used to evaluate the statistical significance of differ - ences between ovariectomized, sham, and naïve animals’ performances in the various tests. Two factors were con- sidered: the experimental group and the week Differ - ences with P ˂ 0.05 were considered significant. Data were expressed as mean ± SEM. Results Object recognition Short‑term memory Figure 2a shows the effects of ovariectomy on short- term object recognition ability in rats, throughout the first 12 weeks following surgery. In the first week, all groups spent more time in the exploration of the novel object than in the exploration of the old one. Afterwards, while the sham and naïve animals maintained their novel object-old object time ratios above 0.7, the ratios of OVX Fig. 3 Spatial memory assessment. Relative time spent in the new group were decreased from 0.8 to 0.6 at week 12. This location of the object relocated (% of total object exploration time) throughout the first 12 weeks following surgery. Treatment groups: change was not statistically significant (Fig. 2a). Analysis ovariectomized animals receiving vehicle solution (OVX) (N = 10), of the post-surgical ratios with two-way ANOVA (group sham operated animals (N = 10), and naïve animals (N = 8). Dashed vs. week) showed a significant group (F = 2.72, P < 0.05) line indicates chance performance of task, which is the same amount and week (F = 2.73, P < 0.05) effect, without a significant of time spent exploring the old and novel object. ANOVA followed group—week interaction. No statistically significant dif - by Bonferroni test: *P < 0.05 vs. sham group; P < 0.05 vs. naive group. Data are mean ± SEM ference was observed between sham and naive groups. Djiogue et al. Behav Brain Funct (2018) 14:14 Page 5 of 8 ratios increased from 0.55 to more than 0.8 at week showed significant group (F = 15.02, P < 0.0001) and week 12, while OVX group ratios remained lower than 0.5 effects (F = 25.51, P < 0.0001) and no significant group— (t = 2.971, P < 0.05 vs. the other groups). Post-surgical, week interaction. No statistically significant difference two-way ANOVA of the ratios showed significant group was observed between sham and naive groups. (F = 14.40, P < 0.001) and week (F = 3.303, P < 0.05) effects, but no significant group—week interaction. No Rearing episodes statistically significant difference was observed between Figure 4b shows the effects of ovariectomy on rearing sham and naive groups. episodes’ number in rats, throughout the first 12 weeks following surgery. In the first 7 weeks, changes in rear - OF test ing episodes’ number were comparable in all groups. Line crossing and rearing However, from week 8 onward, ovariectomized animals Figure 4a shows the effects of ovariectomy on line cross - displayed significant decreases compared to sham and ing number in rats, throughout the first 12 weeks fol - naïve groups (t = 3.380, P < 0.01) (Fig. 4b). Postsurgi- lowing surgery. In the first 2 weeks, the number of line cal analysis using two-way ANOVA showed significant crossing was comparable in all groups. However, from group (F = 7.481, P < 0.0001) and week effects (F = 28.90, week 5 onward, line crossing number increased markedly P < 0.0001) and a significant group—week interaction in sham and naïve groups (t = 3.373, P < 0.01 vs. base- (F = 2.509, P < 0.05). No statistically significant difference line values), but not in OVX group (t = 3.214, P < 0.01) was observed between sham and naive groups. (Fig. 4a). Postsurgical analysis using two-way ANOVA Central OF arena time Figure 5 shows effects of ovariectomy on the time spent at the center of the OF arena in rats, throughout the first 12 weeks following surgery. In the first 7 weeks, chang - ing in the time spent at the center were comparable in all groups. However, from week 8 onward, ovariecto- mized animals displayed significant decreases compared to sham group (t = 2.940, P < 0.05) (Fig. 5). Postsurgi- cal analysis using two-way ANOVA showed significant group (F = 5.745, P < 0.01) and week effects (F = 24.12, P < 0.001) and no significant group—week interaction. No statistically significant difference was observed between sham and naïve groups. Fig. 4 Locomotor and vertical activities. Number of line crossing (a) and rearing episodes (b) throughout the first 12 weeks following Fig. 5 Time in the center of the OF arena. Time spent at the center surgery. Treatment groups: ovariectomized animals receiving throughout the first 12 weeks following surgery. Treatment groups: vehicle solution (OVX) (N = 10), sham operated animals (N = 10), ovariectomized animals receiving vehicle solution (OVX) (N = 10), and naïve animals (N = 8). ANOVA followed by Bonferroni test: sham operated animals (N = 10), and naïve animals (N = 8). ANOVA ## *P < 0.05, **P < 0.01 vs. sham group; P < 0.01 vs. naive group. Data are followed by Bonferroni test: *P < 0.05 vs. naive group. Data are mean ± SEM mean ± SEM Djiogue et al. Behav Brain Funct (2018) 14:14 Page 6 of 8 Discussion estrogens’ importance is area-specific in the brain, due to Our results showed declines of performances in cognitive area-specific repartition of subtypes and expressions of and motor tasks, and affections of components of normal estrogen receptors [9, 13, 27–30]. exploratory behavior in ovariectomized rats. Short-term These findings support the hypothesis that contro - (3-h inter-trial delay) and long-term (24-h inter-trial versy on the importance and effects of sustained estro - delay) non-spatial memory (object recognition) and spa- gen depletion on memory and other cognitive processes tial memory (object placement) started to decline as early may emerge from differences in time intervals between as 2 weeks after surgery. Similarly, the numbers of line ovariectomy and object recognition testing, among other crossing and rearing episodes were significantly reduced parameters differing between the experimental protocols from the 8th week post-surgery. Altogether, these obser- used in the available reports [10, 16]. Thus, future studies vations suggest that ovarian hormones play a key role attempting to confirm the available data should consider in the preservation of cognitive and motor functions harmonizing the experimental protocols with protocols in female rats. Our findings corroborate the previous used in the studies that produced them. reports suggesting that ovariectomy affects significantly Our results revealed an alteration of the spatial and the cognitive processes [10, 18, 19]. The decrease in line nonspatial memory processes, both short and long term, crossing (indicator of rodent natural drive to explore of intact rats, compared to OVX rats observed from a novel environment) and rearing episodes numbers week 2–12 post OVX. Knowing that OR and OP are hip- (assessment of the presence of potential environmental pocampal-dependent tasks [31], our results suggest that dangers) observed in ovariectomized rats in this study estradiol would act as a regulator of cellular processes in also indicate cognitive impairment [20, 21], as well as the hippocampus. The mechanisms underlying the rapid mood affections [22]. Decreases in the time spent in the effects of estrogen also remain to be elucidated. However, center of the open field arena, a well-established indicator it has been suggested that E2 may produce its effects by of anxiety in rodents [22–25], also suggested an increased binding to its ERα and ERβ intracellular canonical recep- anxiety in ovariectomized rats in this study. tors located in the dendritic spines, dendrites, axons The analysis of the relative time spent exploring the and nucleus of the pyramidal neurons of the hippocam- novel object in short-term memory evaluation with pus [28]. The classical mechanism by which E2 exert his two-way ANOVA showed significant group and week effects involve the formation of an E2-ER complex in the effects, without significant group-week interactions. This cytoplasm, its translocation into the nucleus, followed observation suggests that ovariectomy was associated by its attachment to the estrogen response element. with a decline in performance in object recognition test (ERE) which then initiates transcription. However, since whose severity increased with time. On the same hand, this mechanism is too slow and insufficient to explain the evaluation of short-term spatial memory revealed by itself the multiple effects of E2 on the hippocampus, an increasing trend in the time spent exploring the new other mechanisms have also been suggested. E2 may also location in sham and naïve animals, which was lost in influence neuronal function through the rapid activa - ovariectomized animals, where the novel area explora- tion of cell signalling cascades such as phosphatidylino- tion remained constant. These findings indicate a direct sitol 3-kinase (PI3 K) and extracellular signal-regulated link between estrogen bioavailability and processes driv- kinase (ERK) [10], by induction of post-translational ing the plasticity of short-term memory in rats. Instead, epigenetic modifications (histone acetylation and DNA the analysis of the relative time spent exploring the novel methylation) [30] or by initiating the synthesis of mTOR object in long term memory evaluation with two-way proteins (mammalian Target Of Rapamycin). Moreo- ANOVA showed a significant group effect, but without ver, it is currently accepted that E2 may influence the significant week effect or group—week interactions. This hippocampus via the interaction between ERs and neu- finding also suggests that ovariectomy was associated rotransmitter receptors (NMDA receptors for exam- with a decline in object recognition, but it indicates an ple) and/or by attachment to new estrogen receptors indirect link between estrogen depletion and long-term located in the plasma membrane and/or synaptic termi- memory affections. Thus, overall, long-term memory nals (GPR30) [32]. It has been proposed that perirhinal, affections were more severe but unpredictable in this entorhinal and medial prefrontal cortical areas are crucial study, while short-term memory affections were mild for for object memory, whereas spatial recognition involves a long time but increased in severity. This is not surpris - hippocampal pathways in rats [27]. Thus, this suggests ing considering that short-term memory depends more that, effects of reduction of the ability to recognize the on perirhinal, entorhinal and medial prefrontal cortical object in OVX rats in our study are not limited to, or spe- areas while long-term memory relies heavily on the hip- cific to, hippocampus pathways, but rather extend to sev - pocampal formation in mammals [26, 27], and given that eral other brain structures. Djiogue et al. Behav Brain Funct (2018) 14:14 Page 7 of 8 Ethics approval and consent to participate Few studies have investigated the mechanisms by All experiments were carried out in accordance with the Cameroon National which E2 promotes the exploratory behaviour of rats. Ethic Committee for animal experiments, which adopted all procedures The hypothesis currently accepted is that E2 would act recommended by the European Union on the protection of animals used for scientific purposes (CEE Council 86/609; Reg. No. FWA-IRD 0001954). mainly via ERα, ERβ being little or not at all involved [33, 34]. However, the mechanisms by which ERα influ - Funding ences locomotor activity are unclear. ERα may still act We received no funding support for the present study. by modulating the activity of many neurotransmitters, including dopamine and/or serotonin [35]. Indeed, Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub- estrogens are able to regulate different stages of dopa - lished maps and institutional affiliations. minergic functioning, including the release of dopa- mine, its metabolism and the functioning of its pre- and Received: 23 April 2018 Accepted: 10 July 2018 postsynaptic proteins [36, 37]. In addition, E2 may also acts on the dopaminergic system via non-genomic mechanisms of action, not involving ERα or ERβ [38]. References 1. Sherwin BB. Estrogen and memory in women: how can we reconcile the findings? Horm Behav. 2005;47(3):371–5. Conclusions 2. Hogervorst E, Bandelow S. Brain and cognition. Is there any case for improving cognitive function in menopausal women using estrogen Our data suggest that memory and locomotor activity treatment? Minerva Ginecol. 2009;61(6):499–515. may be impaired by ovariectomy in female rats, indi- 3. Hojo Y, et al. 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Journal
Behavioral and Brain Functions – Springer Journals
Published: Jul 16, 2018