Hemispheric differences in basilar dendrites and spines of pyramidal neurons in the rat prelimbic cortex: activity‐ and stress‐induced changes

Claudia Perez‐Cruz,Mária Simon,Eberhard Fuchs,Boldizsár Czéh,Gabriele Flügge

doi:10.1111/j.1460-9568.2009.06622.x

Abstract

Pyramidal neurons of the rat medial prefrontal cortex have been shown to react to chronic stress by retracting their apical dendrites and by spine loss. We extended these findings by focusing on the basilar dendritic tree of layer III pyramidal neurons in both hemispheres of the rat prelimbic cortex. Animals were subjected to daily restraint stress for 1 week (6 h/day), during either the resting or the activity period. The morphology of basilar dendrites and spines of Golgi–Cox-stained neurons in the left and right hemispheres was digitally reconstructed and analyzed. We observed the following: (i) there was an inherent hemispheric asymmetry in control rats during the resting period: the number of spines on proximal dendrites was higher in the left than in the right hemisphere; (ii) basal dendrites in controls displayed a diurnal variation: there was more dendritic material during the resting period than in the activity period; (iii) chronic stress reduced the length of basal dendrites in only the right prelimbic cortex; (iv) chronic stress reduced spine density on proximal basal dendrites; (v) restraint stress during the activity period had more pronounced effects on the physiological stress parameters than restraint stress during the resting period. Our results show dynamic hemisphere-dependent structural changes in pyramidal neurons of the rat prelimbic cortex that are tightly linked to periods of resting and activity. These morphological alterations reflect the capacity of the neurons to react to external stimuli and mirror presumptive changes in neuronal communication.

Highlights

Chronic stress-induced perturbations of the central nervous system have the potential to lead to depressive disorders (McEwen, 1998; Kendler et al, 1999), and the medial prefrontal cortex is intimately involved in emotional processes related to such psychopathologies (Drevets et al, 1997; Cardinal et al, 2002; Sullivan, 2004)
It has been proposed that the function of the prefrontal cortex is lateralized and that the right medial prefrontal cortex (mPFC) plays a special role in integrating emotional and physiological responses to stress (Thiel & Schwarting, 2001; Sullivan, 2004)
We report three novel findings: (i) an intrinsic hemispheric asymmetry in the number of spines on proximal basal dendrites; (ii) a diurnal variation in the amount of dendritic material and in spine number in relation to the normal activity cycle; and (iii) a pronounced selective effect of stress on basal dendrites of neurons in the right prelimbic cortex (PL)

Summary

Introduction

Chronic stress-induced perturbations of the central nervous system have the potential to lead to depressive disorders (McEwen, 1998; Kendler et al, 1999), and the medial prefrontal cortex (mPFC) is intimately involved in emotional processes related to such psychopathologies (Drevets et al, 1997; Cardinal et al, 2002; Sullivan, 2004). Studies in rats have shown that stress changes apical dendrites of pyramidal neurons in mPFC layers II–III, inducing retraction of distal dendritic branches and spine loss (Cook & Wellman, 2004; Radley et al, 2004, 2006; Brown et al, 2005). Repeated mild restraint stress reduces the length of apical dendrites and spine density of neurons in layer V of the mPFC (Liu & Aghajanian, 2008). To date no report has indicated a significant impact of stress on basal dendrites, even though the majority of synapses of neocortical pyramidal neurons are on the basal dendrites (Gordon et al, 2006).

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Conclusion