Nursing-Induced Somatosensory Cortex Plasticity: Temporally Decoupled Changes in Neuronal Receptive Field Properties Are Accompanied by Modifications in Activity-Dependent Protein Expression

Abstract

This study is an attempt to gain insight into the malleability of representational maps in the primary somatosensory cortex in relation to the expression of proteins involved in inhibitory and excitatory neurotransmitter systems that contribute to maintain these maps in a dynamic state. Malleability of somatosensory maps is characterized by changes in the sizes of neuron receptive fields (RFs) affecting the representational grain and in the locations and submodalities of these RFs modifying the map extent. The concomitance of these alterations remains so far hypothetical. We used nursing as an evolving source of ethologically significant cutaneous stimulation. This cyclic behavior is particularly suited to investigating the time course of experience-dependent cortical changes. Electrophysiological maps of the ventrum skin were recorded twice in the same lactating rats between nursing initiation and several weeks after nursing. We found that reduction in RF size occurred earlier than map expansion. As nursing time declined, the map expansion was maintained longer than the RF sharpening. Based on this difference in time course, we compared the expression patterns of several activity-dependent proteins in relation to the RF plasticity. Western blot analysis showed an increase in glutamic acid decarboxylase expression that was concomitant with RF contraction. In contrast, NR2A subunit of NMDA and ␣ calcium/calmodulin kinase type II were upregulated at times when map expansion was observed. We propose that inhibitory and excitatory plasticity mechanisms operating with different time courses may contribute to the temporal dissociation of nursing-induced RF reshaping and map expansion.

Hypergravity within a critical period impacts on the maturation of somatosensory cortical maps and their potential for use-dependent plasticity in the adult

“…The cutaneous RF enlargement found in HG rats is consistent with the decrease in GABA immunoreactivity recorded in the limb representation of the rats S1 cortex after 14 days of exposure to HG (D'Amelio et al 1998). Furthermore, an expansion of cutaneous RFs in the S1 cortex was found when GABA-mediated local inhibition was antagonized (Alloway et al 1989 regation of inputs converging onto neuronal targets was reshaped on a timescale closely dependent on behaviorally driven changes in somatosensory inputs (Rosselet et al 2006). The reversibility vs. retention of different neuronal response properties, after the animals were exposed to NG, shows that the use-dependent synaptic mechanisms leading to masking/ unmasking of less/more effective inputs or to synaptogenesis at maturity are expressed within limits of representational malleability stabilized by somatosensory experience during a critical developmental period.…”

“…The enduring effects of early HG rearing are at variance with the reversibility of alteration found in adult somatosensory maps following various manipulations (see for reviews Barnes and Finnerty 2010;Buonomano and Merzenich 1998;Xerri 2008), such as experimental syndactyly (Clark et al 1988), limb immobilization (Coq and Xerri 1999), or natural episodic behavior (nursing; Rosselet et al 2006). These HG-induced sustained alterations provide an additional argument in favor of a critical period in the maturation of somatosensory maps, previously shown for the development of the whisker-barrel system (see Erzurumlu and Gaspar 2012 for review).…”

Excitation and Inhibition Jointly Regulate Cortical Reorganization in Adult Rats

“…Experimental work on a timescale of days to weeks reveals that cortical map expansion and RF sharpening/contraction induced by the repetitive cutaneous stimulation during nursing is associated with changes in the inhibitory and excitatory system (Rosselet et al, 2006). The authors show that, at different time points, only one of the systems is changed.…”

“…Based on theoretical and experimental work, it has been suggested that the maintenance of cortical maps and RFs arises from a meticulous balance of both local and global mechanisms based on feedforward and recurrent inputs (Stratford et al, 1996;Miller et al, 2001;Kalarickal and Marshall, 2002), on alterations of both excitatory and inhibitory mechanisms (Heizmann, 1993;Jones, 2000;Kalarickal and Marshall, 2002;Rosselet et al, 2006), and on a continues protein synthesis (Kleim et al, 2003).…”

Specific knock-down of GAD67 in the striatum using naked small interfering RNAs

“…Western blot analysis was performed as described in Rosselet et al (2006). In brief, tissue samples were homogenized and denatured in Tris-Cl buffer.…”