Sex-dependent effects of paternal deprivation and chronic variable stress on novel object recognition in adult California mice (Peromyscus californicus)

Agarwal, Priyanka; Palin, Nicole; Walker, S.L.; Glasper, Erica R.

doi:10.1016/j.yhbeh.2019.104610

Cited by 19 publications

(11 citation statements)

References 82 publications

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“…It also relies on a rodent's natural inclination to explore its environment, and to approach and interact with objects that hold novelty value (Renner, 1990;Bevins and Besheer, 2006). A major advantage of the task is that it can be used in both rats and mice (Agarwal et al, 2020;Chang et al, 2020). Current iterations of the NOR paradigm are widely used to study memory (Cole et al, 2020), synaptic plasticity (Lee et al, 2020), impairment and/or recovery of function in brain disease (Grayson et al, 2015), TBI (Amoros-Aguilar et al, 2020), stress (Brivio et al, 2020;Glushchak et al, 2021), aging (Amirazodi et al, 2020), sleep (Shahveisi et al, 2020), autism (Batista et al, 2019;Gandhi and Lee, 2020), and epigenetics (Ellis et al, 2020;Sadat-Shirazi et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

A Sensitive Homecage-Based Novel Object Recognition Task for Rodents

Wooden

Spinetta

Nguyen

et al. 2021

Front. Behav. Neurosci.

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The recognition of novel objects is a common cognitive test for rodents, but current paradigms have limitations, such as low sensitivity, possible odor confounds and stress due to being performed outside of the homecage. We have developed a paradigm that takes place in the homecage and utilizes four stimuli per trial, to increase sensitivity. Odor confounds are eliminated because stimuli consist of inexpensive, machined wooden beads purchased in bulk, so each experimental animal has its own set of stimuli. This paradigm consists of three steps. In Step 1, the sampling phase, animals freely explore familiar objects (FO). Novel Objects (NO1 and NO2) are soiled with bedding from the homecage, to acquire odor cues identical to those of the FO. Steps 2 and 3 are test phases. Herein we report results of this paradigm from neurologically intact adult rats and mice of both sexes. Identical procedures were used for both species, except that the stimuli used for the mice were smaller. As expected in Step 2 (NO1 test phase), male and female rats and mice explored NO1 significantly more than FO. In Step 3 (NO2 test phase), rats of both sexes demonstrated a preference for NO2, while this was seen only in female mice. These results indicate robust novelty recognition during Steps 2 and 3 in rats. In mice, this was reliably seen only in Step 2, indicating that Step 3 was difficult for them under the given parameters. This paradigm provides flexibility in that length of the sampling phase, and the delay between test and sampling phases can be adjusted, to tailor task difficulty to the model being tested. In sum, this novel object recognition test is simple to perform, requires no expensive supplies or equipment, is conducted in the homecage (reducing stress), eliminates odor confounds, utilizes 4 stimuli to increase sensitivity, can be performed in both rats and mice, and is highly flexible, as sampling phase and the delay between steps can be adjusted to tailor task difficulty. Collectively, these results indicate that this paradigm can be used to quantify novel object recognition across sex and species.

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Section: Introductionmentioning

confidence: 99%

A Sensitive Homecage-Based Novel Object Recognition Task for Rodents

Wooden

Spinetta

Nguyen

et al. 2021

Front. Behav. Neurosci.

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“…According to the World Health Organization (WHO), depression is the leading cause of disability and will become the second most common disease in the world at 2025. Sex is an important factor in influencing the susceptibility to psychiatric illness ( Agarwal et al, 2020 ). Women are more likely to suffer from anxiety disorders, while men are more likely to suffer from substance-use disorders, suggesting that there are some differences in the mechanisms of depression between the sexes.…”

Section: Introductionmentioning

confidence: 99%

Latent Sex Differences in CaMKII-nNOS Signaling That Underlie Antidepressant-Like Effects of Yueju-Ganmaidazao Decoction in the Hippocampus

Yin

Qian

Chen

et al. 2021

Front. Behav. Neurosci.

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Previous studies have demonstrated that Yueju-Ganmaidazao (YG) decoction induces rapid antidepressant-like effects, and the antidepressant response is mostly dependent on the suppression of nitric oxide-cyclic guanosine monophosphate signaling in male mice. This study aimed to investigate the sex difference mediated by calcium/calmodulin-dependent protein kinase II (CaMKII)-neuronal nitric oxide synthase (nNOS) signaling involved in the antidepressant-like effect of YG in mice. We found that the immobility times in the tail suspension test (TST) were found to be decreased after the single injection of YG in male and female mice with the same dosage. Additionally, chronic administration for 4 days of subthreshold dosage of YG and escitalopram (ES) also significantly decreased the immobility time in mice of both sexes. Chronic subthreshold dosage of YG and ES in LPS-treated mice and in chronic unpredictable stress (CUS) mice both decreased the immobility time, which was increased by stress. Meanwhile, in CUS-treated mice, sucrose preference test, forced swimming test, and open field test were applied to further confirm the antidepressant-like effects of YG and ES. Moreover, CUS significantly decreased the expression of nNOS and CaMKII, and both YG and ES could enhance the expression in the hippocampus of female mice, which was opposite to that in male mice, while endothelial nitric oxide synthase expression was not affected by stress or drug treatment neither in male mice nor in female mice. Finally, subthreshold dosage of YG combined with 7-nitroindazole (nNOS inhibitor) induced the antidepressant-like effects both in female and in male mice, while the single use of YG or 7-NI did not display any effect. However, pretreatment with KN-93 (CaMKII inhibitor) only blocked the antidepressant-like effect of high-dosage YG in female mice. Meanwhile, in CUS mice, chronic stress caused NR1 overexpression and inhibited cAMP response element binding protein action, which were both reversed by YG and ES in male and female mice, implying that YG and ES produced the same antidepressant-like effect in mice of both sexes. The study revealed that chronic treatment with a subthreshold dose of YG also produced antidepressant-like effects in female mice, and these effects depended on the regulation of the CaMKII-nNOS signaling pathway.

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“…Others fail to find differences in corticosterone concentration in MON vs BPC prairie voles, 18 and variations in the neuroendocrine substrates of the hypothalamic‐pituitary‐adrenal axis are either null or suggest a more resilient phenotype in MON prairie voles 18,35 . Similarly, paternal absence does not result in increased serum corticosterone in adult California mice 43 . Early in development (ie, PND8‐14), mandarin vole pups show elevated levels of serum corticosterone and ACTH 44 ; however, findings from Jia et al 45 show that MON mandarin vole pups are attended to less that BPC pups (as also seen in prairie voles 19,27,46 ); therefore, it remains unclear whether the elevated CORT and ACTH are indicators of stress or metabolic processes related to thermoregulation.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, one might hypothesise that, in the natural habitat paternal, absence acts as an indicator of broader environmental circumstances (eg, predation, population density, resource scarcity, etc) and drives variation in social behaviour accordingly. This distinction also provides an opportunity to combine conditions of paternal absence with more salient stress paradigms in unique combinations that might be interactive rather than additive (eg, see Agarwal et al 43 ).…”

Section: Discussionmentioning

confidence: 99%

Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)

Rogers

Freeman

Anderson

et al. 2021

J Neuroendocrinology

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Paternal absence can significantly alter bio‐behavioural development in many biparental species. This effect has generally been demonstrated by comparing the development of offspring reared under biparental care with those reared by a single mother. However, studies employing this design conflate two significant modifications to early‐life experience: removal of father‐specific qualities and the general reduction of offspring‐directed care. In the socially monogamous prairie vole (Microtus ochrogaster), the experience of paternal absence without substitution during development inhibits partner preference formation in adulthood, a hallmark of social monogamy, in females and males. Employing alloparents as substitutes for fathers, our previous work demonstrated that paternal absence affects pair‐bond formation in female offspring via reduced quantity of care, although it affects pair‐bond formation in male offspring by means of a missing paternal quality (or qualities). Here, we present evidence that paternal absence (with and without alloparental substitution) may alter the ontogeny of neural oxytocin receptor (OXTR) and/or vasopressin 1a receptor (AVPR1a) distribution in male and female prairie voles. Compared to biparentally reared controls (BPC), male offspring reared in mother only (MON) and maternal‐plus‐alloparental (MPA) conditions show lower densities of OXTR in the central amygdala; and MPA males show lower densities of OXTR in the caudate putamen and nucleus accumbens. Early‐life experience was not associated with differences in AVPR1a density in males. However, MON and MPA females show greater densities of AVPR1a in the medial amygdala than BPC; and MPA females show greater densities of AVPR1a in the ventromedial nucleus of the hypothalamus. We also demonstrate with corticosterone concentrations that MON and MPA offspring are not differentially susceptible to a stressor (ie, social isolation) than BPC offspring. These findings suggest that paternal absence, although likely not a salient early‐life stressor, has neuroendocrine consequences for offspring, some of which may affect partner preference formation.

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Sex-dependent effects of paternal deprivation and chronic variable stress on novel object recognition in adult California mice (Peromyscus californicus)

Cited by 19 publications

References 82 publications

A Sensitive Homecage-Based Novel Object Recognition Task for Rodents

A Sensitive Homecage-Based Novel Object Recognition Task for Rodents

Latent Sex Differences in CaMKII-nNOS Signaling That Underlie Antidepressant-Like Effects of Yueju-Ganmaidazao Decoction in the Hippocampus

Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)

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