Distinct maturation profiles of perisomatic and dendritic targeting GABAergic interneurons in the mouse primary visual cortex during the critical period of ocular dominance plasticity

Abstract

Lazarus MS, Huang ZJ. Distinct maturation profiles of perisomatic and dendritic targeting GABAergic interneurons in the mouse primary visual cortex during the critical period of ocular dominance plasticity. J Neurophysiol 106: 775-787, 2011. First published May 25, 2011 doi:10.1152/jn.00729.2010In the rodent primary visual cortex, maturation of GABA inhibitory circuitry is regulated by visual input and contributes to the onset and progression of ocular dominance (OD) plasticity. Cortical inhibitory circuitry consists of diverse groups of GABAergic interneurons, which display distinct physiological properties and connectivity patterns. Whether different classes of interneurons mature with similar or distinct trajectories and how their maturation profiles relate to experience dependent development are not well understood. We used green fluorescent protein reporter lines to study the maturation of two broad classes of cortical interneurons: parvalbumin-expressing (PV) cells, which are fast spiking and innervate the soma and proximal dendrites, and somatostatin-expressing (SOM) cells, which are regular spiking and target more distal dendrites. Both cell types demonstrate extensive physiological maturation, but with distinct trajectories, from eye opening to the peak of OD plasticity. Typical fast-spiking characteristics of PV cells became enhanced, and synaptic signaling from PV to pyramidal neurons became faster. SOM cells demonstrated a large increase in input resistance and a depolarization of resting membrane potential, resulting in increased excitability. While the substantial maturation of PV cells is consistent with the importance of this source of inhibition in triggering OD plasticity, the significant increase in SOM cell excitability suggests that dendrite-targeted inhibition may also play a role in OD plasticity. More generally, these results underscore the necessity of cell type-based analysis and demonstrate that distinct classes of cortical interneurons have markedly different developmental profiles, which may contribute to the progressive emergence of distinct functional properties of cortical circuits.

MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex

“…Together, these results suggest increased presynaptic vesicles and/or GABA loading, especially in PV interneurons, in MeCP2 −/y V1. During the critical period of visual cortical development (25), which spans around 3 wk after eye opening, GABA + PV interneurons undergo substantial maturation in synaptic innervation and physiological properties, concomitant with increased expression and synaptic localization of GAD67, GAD65, and PV (18,24,26). In V1 of MeCP2 −/y mice, we found that increased expression of GAD67, GAD65, vGAT, and PV persisted to at least the fifth week ( Fig.…”

“…It should be noted that, in addition to mediating cytosolic GABA synthesis, which influences cellular GABA levels, GAD67 and GAD65 form complexes that directly interact with vGAT on synaptic vesicles, thereby facilitating the coupling from GABA synthesis to vesicular packaging (51,52). The key role of GAD67, GAD65, PV, and vGAT in regulating vesicular GABA content and release (26,(51)(52)(53) suggest that alterations in their levels may impact the strength and/or dynamics of GABA transmission (54), especially during fast spiking in PV cells.…”

“…This highly connected network of fast-spiking PV cells plays a key role in the detection of temporal activity patterns within the neocortex (35) and in the generation of network oscillations (34,36). During postnatal development, substantial maturation of intrinsic and synaptic properties, including GABA transmission among PV cells, converts the PV cell network from a slow to fast signaling device for regulating cortical activity patterns (26,37). To determine the physiological impact of increased GADs and vGAT levels in PV cells in MeCP2 −/y V1, we measured a series of physiological parameters.…”

Neuroplasticity in Depressed Individuals Compared with Healthy Controls

“…Further, there is evidence that the rate-limiting enzyme for GABA synthesis (GAD67) is reduced in the cortex of individuals with bipolar disorder (Thompson et al, 2009) and hippocampus of depressed individuals (Thompson et al, 2011). Although robust changes in cortical GAD67 mRNA are not typically found in the PFC of individuals with depression (Thompson et al, 2009;Sibille et al, 2011), significant decreases in somatostatin suggest that interneuron deficits may be especially prominent in a subset of interneurons shown to directly contribute to cortical plasticity (Lazarus and Huang, 2011). As inhibitory interneuron deficits are shared among those with depression, bipolar disorder, and schizophrenia (Thompson et al, 2009(Thompson et al, , 2011Fung et al, 2010;Hashimoto et al, 2008;Daskalakis et al, 2002), cortical plasticity deficits would also be expected to be found in multiple forms of psychopathology.…”

Deprivation-Induced Strengthening of Presynaptic and Postsynaptic Inhibitory Transmission in Layer 4 of Visual Cortex during the Critical Period

“…FS interneurons have a protracted period of postnatal development in primary sensory cortex, reaching an adult-like physiological and anatomical state 3-4 weeks after birth (Okaty et al, 2009;Jiang et al, 2010;Lazarus and Huang, 2011;PangratzFuehrer and Hestrin, 2011). Interestingly, FS3 SP long-term depression (LTD), long-term potentiation (LTP), and spike timing-dependent plasticity are expressed at distinct stages along this postnatal timeline, suggesting that inhibitory plasticity is tuned to interneuron identity and age of the cortex Yazaki-Sugiyama et al, 2009;Lamsa et al, 2010;House et al, 2011;Lefort et al, 2013).…”