Dendrites of the dorsal and ventral hippocampal CA1 pyramidal neurons of singly housed female rats exhibit lamina‐specific growths and retractions during adolescence that are responsive to pair housing

Abstract

Adolescence is accompanied by increased vulnerability to psychiatric illnesses, including anxiety, depression, schizophrenia, and eating disorders. The hippocampus is important for regulating emotional state through its ventral compartment and spatial cognition through its dorsal compartment. Previous animal studies have examined hippocampal development at stages before, after or at single time points during adolescence. However, only one study has investigated morphological changes at multiple time points during adolescence, and no study has yet compared developmental changes of dorsal versus ventral hippocampi. We analyzed the dorsal and ventral hippocampi of rats to determine the developmental trajectory of Golgi-stained hippocampal CA1 neurons by sampling at five time points, ranging from postnatal day (P) 35 (puberty) to 55 (end of adolescence). We show that the dorsal hippocampus undergoes transient dendritic retractions in stratum radiatum (SR), while the ventral hippocampus undergoes transient dendritic growths in SR. During adulthood, stress and hormonal fluctuations have been shown to alter the physiology and morphology of hippocampal neurons, but studies of the impact of these factors upon adolescent hippocampi are scarce. In addition, we show that female-female pair housing from P 36-44 significantly increases branching in the dorsal SR and reduces branching in the ventral SR. Taken together with data on spine density, these results indicate that pyramidal cells in the dorsal and ventral CA1 of female adolescents are remodeled differently following single housing. Social housing during adolescence elicits pathway-specific changes in the hippocampus that may underlie behavioral benefits, including stability of emotion regulation and superior cognition.

Effects of adolescent experience of food restriction and exercise on spatial learning and open field exploration of female rats

“…These behavioral data indicate that the precocious dendritic arbors and spine maturity that was detected previously in the ventral hippocampus of another cohort of the EX + FR group or the retraction of dendritic arbors detected between P51-55 for another cohort of CON animals (Chen et al, 2018;Chowdhury et al, 2014) do not translate to alterations in anxiety-like behavior at P47-48 or P54-55.…”

“…One aspect of research that is relatively unexplored is the impact of voluntary physical exercise and food restriction specifically during adolescence. Previous work showed that pyramidal neurons in this brain region exhibit robust extensions and retraction of dendritic arbors during adolescence (Chen, Akad, Aderogba, Chowdhury, & Aoki, 2018;Chowdhury et al, 2014). These changes are accompanied by spinogenesis, spine pruning (Chen et al, 2018;Chowdhury et al, 2014), and restructuring of GABAergic synapses on pyramidal neurons (Aoki et al, 2012).…”

“…Previous work showed that pyramidal neurons in this brain region exhibit robust extensions and retraction of dendritic arbors during adolescence (Chen, Akad, Aderogba, Chowdhury, & Aoki, 2018;Chowdhury et al, 2014). These changes are accompanied by spinogenesis, spine pruning (Chen et al, 2018;Chowdhury et al, 2014), and restructuring of GABAergic synapses on pyramidal neurons (Aoki et al, 2012). Moreover, these changes of dendritic morphology and GABAergic synapses are influenced significantly by voluntary exercise, food restriction, and the combination of the two during adolescence (Aoki et al, 2012;Chowdhury, Wable, Sabaliauskas, & Aoki, 2013).…”

Caffeine consumption during development alters spine density and recovery from repetitive mild traumatic brain injury in young adult rats

“…Overall, caffeine increased spine density in the NAc, mPFC, and the OFC apical dendrites while RmTBI increased spine density in the NAc, mPFC apical dendrites, OFC apical dendrites in caffeinated males, and OFC basilar dendrites in caffeinated females. Although increased dendritic spine density is commonly perceived as beneficial (Chen, ), it can often be maladaptive, particularly in the context of early adulthood neurological development. For example, a study by Kolb et al (2003) found that while exposure to amphetamine or cocaine increased spine density in the mPFC and NAc, these changes also limited the brain's ability to respond to subsequent experiences (Kolb, ).…”

Synaptic changes in the hippocampus of adolescent female rodents associated with resilience to anxiety and suppression of food restriction-evoked hyperactivity in an animal model for anorexia nervosa

“…2). Conversely, dendritic branches of pyramidal neurons in the dorsal CA1 hippocampus exhibit a transient 50% retraction during adolescence (Chen et al, 2015a). The changes in both the dorsal and ventral hippocampus are transient, returning to pre-pubertal levels by the time animals reach late adolescence.…”