Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus

Abstract

Theodosis, Dionysia T., Andrei Trailin, and Dominique A. Poulain. Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus. Am J Physiol Regul Integr Comp Physiol 290: R1175-R1182, 2006; doi:10.1152/ajpregu.00755.2005.-Neurons, including their synapses, are generally ensheathed by fine processes of astrocytes, but this glial coverage can be altered under different physiological conditions that modify neuronal activity. Changes in synaptic connectivity accompany astrocytic transformations so that an increased number of synapses are associated with reduced astrocytic coverage of postsynaptic elements, whereas synaptic numbers are reduced on reestablishment of glial coverage. A system that exemplifies activity-dependent structural synaptic plasticity in the adult brain is the hypothalamo-neurohypophysial system, and in particular, its oxytocin component. Under strong, prolonged activation (parturition, lactation, chronic dehydration), extensive portions of somatic and dendritic surfaces of magnocellular oxytocin neurons are freed of intervening astrocytic processes and become directly juxtaposed. Concurrently, they are contacted by an increased number of inhibitory and excitatory synapses. Once stimulation is over, astrocytic processes again cover oxytocinergic surfaces and synaptic numbers return to baseline levels. Such observations indicate that glial ensheathment of neurons is of consequence to neuronal function, not only directly, for example by modifying synaptic transmission, but indirectly as well, by preparing neuronal surfaces for synapse turnover.NEURONS, GLIA, AND SYNAPTIC inputs are not static elements because they undergo dynamic transformations. This can take place under normal physiological conditions and highlights the adult nervous system's remarkable capacity to undergo restructuring to meet particular functional requirements. A change in the morphology of neurons, and especially of afferent inputs controlling their activity, can have important consequences on their respective functions. These modifications are often accompanied by remodeling of adjacent glia, which has further impact on neuronal activity by modifying the immediate extracellular microenvironment, thereby influencing synaptic and volume transmission.The hypothalamo-neurohypophysial system (HNS), and in particular, its oxytocinergic component, is a familiar model for this kind of morphological neuronal and glial plasticity (57,76). Oxytocin (OT) neurons accumulate in well-defined regions in the hypothalamus, the supraoptic (SON), and paraventricular (PVN) nuclei, and release OT mainly from axon terminals in the neurohypophysis to act as a neurohormone in vital functions like parturition, lactation, and osmotic regulation. Critical for this systemic secretion is the concomitant exocytotic release of the peptide from somata and dendrites of OT neurons themselves in the SON and PVN. This central release facilitates the synchronous high-frequency activity of...

Expression of the embryonal isoform (0N/3R) of the microtubule‐associated protein tau in the adult rat central nervous system

“…As referenced in Nacher et al (2000Nacher et al ( , 2001 and Bonfanti et al (1992), these cells show neuronal plasticity in the adult, e.g., changes of dendrites and synapse formation. For instance, in the supraoptic nucleus, stimulation by lactation or dehydration leads to dendritic and synaptic plasticity (review: Theodosis et al, 2006). The semilunar-transition type layer II neurons are located preferentially in the associative areas of the neocortex (Luzzati et al, 2009) and have a plastic phenotype with expression of DCX, PSA-NCAM, and CRMP-4 (Gómez-Climent et al, 2008).…”

H3 Receptor Antagonism Enhances NCAM PSA-Mediated Plasticity and Improves Memory Consolidation in Odor Discrimination and Delayed Match-to-Position Paradigms

“…Many of the NCAM PSA-immunopositive cells located at the infragranular zone of the dentate gyrus have been identified as newly generated granule cells that remain available for integration into the neuronal architecture and before their natural loss by apoptosis (Ge et al, 2007;Dupret et al, 2007;Toni et al, 2008). Similarly, the activitydependent modifications to hypothalamic synapse and astrocytic coverage of oxytocinergic neurons, which occur in response to physiological stimuli arising during parturition, lactation, or chronic dehydration, are dependent on NCAM PSA, as these are prevented by infusions of endoneuraminidase-N (Hoyk et al, 2001;Monlezun et al, 2005;Catheline et al, 2006;Theodosis et al, 2006).…”

The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output

“…The glial cells express receptors for neurotransmitters and release several substances that act as gliotransmitters and may influence glia-to-glia and gliato-neuron communication as well as neuronal differentiation and plasticity. In addition, modifications in glial cell morphology affect the formation and maintenance of synaptic contacts (Garcia-Segura et al 1994, Hatton 1997, Theodosis et al 2006. Therefore, a substantial modification in the interpretation of the function of glial cells has emerged.…”