Rearing in enriched environment increases parvalbumin-positive small neurons in the amygdala and decreases anxiety-like behavior of male rats

Abstract

BackgroundEarly life experiences including physical exercise, sensory stimulation, and social interaction can modulate development of the inhibitory neuronal network and modify various behaviors. In particular, alteration of parvalbumin-expressing neurons, a gamma-aminobutyric acid (GABA)ergic neuronal subpopulation, has been suggested to be associated with psychiatric disorders. Here we investigated whether rearing in enriched environment could modify the expression of parvalbumin-positive neurons in the basolateral amygdala and anxiety-like behavior.ResultsThree-week-old male rats were divided into two groups: those reared in an enriched environment (EE rats) and those reared in standard cages (SE rats). After 5 weeks of rearing, the EE rats showed decreased anxiety-like behavior in an open field than the SE rats. Under another anxiogenic situation, in a beam walking test, the EE rats more quickly traversed an elevated narrow beam. Anxiety-like behavior in the open field was significantly and negatively correlated with walking time in the beam-walking test. Immunohistochemical tests revealed that the number of parvalbumin-positive neurons significantly increased in the basolateral amygdala of the EE rats than that of the SE rats, while the number of calbindin-D28k-positive neurons did not change. These parvalbumin-positive neurons had small, rounded soma and co-expressed the glutamate decarboxylase (GAD67). Furthermore, the number of parvalbumin-positive small cells in the basolateral amygdala tended to positively correlate with emergence in the center arena of the open field and negatively correlated with walking time in the beam walking test.ConclusionRearing in the enriched environment augmented the number of parvalbumin-containing specific inhibitory neuron in the basolateral amygdala, but not that of calbindin-containing neuronal phenotype. Furthermore, the number of parvalbumin-positive small neurons in the basolateral amygdala was negatively correlated with walking time in the beam walking test and tended to be positively correlated with activity in the center arena in the open field test. The results suggest that rearing in the enriched environment augmented parvalbumin-positive specific neurons in the basolateral amygdala, which induced behavioral plasticity that was reflected by a decrease in anxiety-like behavior in anxiogenic situations.

Adult Neurogenesis and Mental Illness

“…One study reported that housing pregnant dams in an enriched environment led to decreased anxiety-like behavior in adult offspring (Friske and Gammie, 2005). However, environmental enrichment for neonates and juvenile rodents had anxiolytic-and antidepressant-like effects on adult behavior in some studies (Baldini et al, 2013;Benaroya-Milshtein et al, 2004;Urakawa et al, 2013;Workman et al, 2011) but not others (Ishihama et al, 2010;Workman et al, 2011;Yildirim et al, 2012). Early-life wheel running also appears to have little effect on adult anxiety-like behavior (Ishikawa et al, 2014).…”

Developmental Age Differentially Mediates the Calcium-Binding Protein Parvalbumin in the Rat: Evidence for a Selective Decrease in Hippocampal Parvalbumin Cell Counts

“…Rather than an overall loss of PV+ GABAergic neurons, there appears to be a dysregulation in the expression of a number of enzymatic pathways, including PV [22,26]. Recently, alterations in PV levels have been observed as a function of experience and/or training [27,28,29,30], suggesting that PV may be dynamically regulated by both external and internal factors. Additional evidence suggests a key role of PV, either directly or as a correlative marker, in neural plasticity in relation to both development and cognition [15,17,31,32].…”

Extinction of Contextual Fear with Timed Exposure to Enriched Environment: A Differential Effect

“…However, our understanding of the effect of EE on connectivity between brain regions is rudimentary. Studies have shown that EE can influence brain plasticity in the hippocampus [19] , amygdala [20], and prefrontal cortex [21] . However, these studies have failed to provide information about neuronal oscillations which have functional relevance to the behavior of animals.…”