Regular Spiking and Intrinsic Bursting Pyramidal Cells Show Orthogonal Forms of Experience-Dependent Plasticity in Layer V of Barrel Cortex

Jacob, Vincent; Petreanu, Leopoldo; Wright, Nicholas Fraser; Svoboda, Karel; Fox, Kevin

doi:10.1016/j.neuron.2011.11.034

Cited by 76 publications

(97 citation statements)

References 70 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Of these 11 proteins, only three were altered by more than 1.2-fold, the cutoff used in our study, and all three were altered in the same direction in deprived tissue from both studies, thereby suggesting partial overlap in synaptic proteins that are affected by deprived sensory experience. However, it is possible that the tissue and cell heterogeneity in our whole barrel cortex samples may mask or dilute changes in any particular protein (95).…”

Section: Discussionmentioning

confidence: 99%

In vivo quantitative proteomics of somatosensory cortical synapses shows which protein levels are modulated by sensory deprivation

Butko¹,

Savas

Friedman³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Postnatal bilateral whisker trimming was used as a model system to test how synaptic proteomes are altered in barrel cortex by sensory deprivation during synaptogenesis. Using quantitative mass spectrometry, we quantified more than 7,000 synaptic proteins and identified 89 significantly reduced and 161 significantly elevated proteins in sensory-deprived synapses, 22 of which were validated by immunoblotting. More than 95% of quantified proteins, including abundant synaptic proteins such as PSD-95 and gephyrin, exhibited no significant difference under high-and low-activity rearing conditions, suggesting no tissue-wide changes in excitatory or inhibitory synaptic density. In contrast, several proteins that promote mature spine morphology and synaptic strength, such as excitatory glutamate receptors and known accessory factors, were reduced significantly in deprived synapses. Immunohistochemistry revealed that the reduction in SynGAP1, a postsynaptic scaffolding protein, was restricted largely to layer I of barrel cortex in sensorydeprived rats. In addition, protein-degradation machinery such as proteasome subunits, E2 ligases, and E3 ligases, accumulated significantly in deprived synapses, suggesting targeted synaptic protein degradation under sensory deprivation. Importantly, this screen identified synaptic proteins whose levels were affected by sensory deprivation but whose synaptic roles have not yet been characterized in mammalian neurons. These data demonstrate the feasibility of defining synaptic proteomes under different sensory rearing conditions and could be applied to elucidate further molecular mechanisms of sensory development. mass spectrometric proteomics | somatosensory cortex | experience-dependent plasticity | synaptic protein dynamics S ensory information is encoded in the brain by activation of specific neuronal circuits that operate via chemical synapses. Important sensory experiences are stored by strengthening activated synapses in the circuit, a process known as "experience-dependent plasticity" (1). When animals are deprived of sensory experience during development, for example, by trimming rodent whiskers from birth to 30 d after birth, synaptic strength and mature synaptic morphology are attenuated, suggesting that the low activity in the deprived circuits interferes with normal development (2-7). However, the molecular changes that alter these synaptic properties in response to experience remain unclear. Synaptic activation has been shown to promote regulated and highly localized effects on synaptic proteins such as local translation, recruitment, and targeted degradation (8-11), and this spatiotemporal control of protein availability is required for long-term plasticity and synaptic maturation, which are fundamental in memory formation and storage and ultimately for an organism's survival (12-14). The need for highly controlled protein availability is highlighted in studies of neurological diseases, which often result from the disruption of protein availability at the synapse (15-17). ...

show abstract

Section: Discussionmentioning

confidence: 99%

In vivo quantitative proteomics of somatosensory cortical synapses shows which protein levels are modulated by sensory deprivation

Butko¹,

Savas

Friedman³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…We used our previously described methods for photostimulation to identify inputs connected to each recorded neuron (Covic and Sherman 2011;Sherman 2011, 2012;Lam and Sherman 2005). Data acquisition and photostimulation were controlled by a program written in MATLAB (The MathWorks, Natick, MA).…”

Section: Laser Uncaging Of Glutamatementioning

confidence: 99%

“…It should be noted that cortical cells that fire at roughly 130 Hz or more (the tetanus frequency we used) exist, including bursting cells (Brumberg et al 2000;DeBusk et al 1997;Jacob et al 2012;Llano and Sherman 2009;Tateno et al 2004). Furthermore, a recent study showed that activation of mGluRs via Class 2 inputs (as in this study) can be achieved with brief trains activated at lower frequencies (e.g., Ն10 -15 Hz) and that although higher frequency stimulation increases the amplitude of the mGluR response, it is not necessary to initially evoke it (Viaene et al 2013).…”

Section: Activation Of Inputs To Layer 4 Of V1 From the White Mattermentioning

confidence: 99%

A modulatory effect of the feedback from higher visual areas to V1 in the mouse

Pasquale

Sherman

2013

Journal of Neurophysiology

View full text Add to dashboard Cite

show abstract

“…Experience-dependent potentiation of neuronal responses has been well characterized in somatosensory cortex (S1), where synaptic potentiation, the addition of new synaptic contacts, and a reduction in local inhibition all play a role in transforming the output of neural circuits (Finnerty et al 1999;Knott et al 2002;Barth et al 2004;Clem and Barth 2006;Jiao et al 2006;Cheetham et al 2007;Wen and Barth 2011;Jacob et al 2012). During postnatal development, experience-dependent plasticity is enhanced, and there has been great interest in understanding the cellular and molecular mechanisms that regulate this phenomenon in order to facilitate learning in other training paradigms as well as to restore plasticity in adults (Feldman et al 1998;Pizzorusso et al 2002;Hensch 2005;Di Cristo et al 2007;Morishita et al 2010;Gu et al 2013;Kuhlman et al 2013).…”

mentioning

confidence: 99%

Experience-dependent regulation of presynaptic NMDARs enhances neurotransmitter release at neocortical synapses

et al. 2014

View full text Add to dashboard Cite

Sensory experience can selectively alter excitatory synaptic strength at neocortical synapses. The rapid increase in synaptic strength induced by selective whisker stimulation (single-row experience/SRE, where all but one row of whiskers has been removed from the mouse face) is due, at least in part, to the trafficking of AMPA receptors (AMPARs) to the post-synaptic membrane, and is developmentally regulated. How enhanced sensory experience can alter presynaptic release properties in the developing neocortex has not been investigated. Using paired-pulse stimulation at layer 4-2/3 synapses in acute brain slices, we found that presynaptic release probability progressively increases in the spared-whisker barrel column over the first 24 h of SRE. Enhanced release probability can be at least partly attributed to presynaptic NMDA receptors (NMDARs). We find that the influence of presynaptic NMDARs in enhancing EPSC amplitude markedly increases during SRE. This occurs at the same time when recently potentiated synapses become highly susceptible to a NMDAR-dependent form of synaptic depression, during the labile phase of plasticity. Thus, these data show that augmented sensory stimulation can enhance release probability at layer 4-2/3 synapses and enhance the function of presynaptic NMDARs. Because presynaptic NMDARs have been linked to synaptic depression at layer 4-2/3 synapses, we propose that SRE-dependent up-regulation of presynaptic NMDARs is responsible for enhanced synaptic depression during the labile stage of plasticity.

show abstract

Regular Spiking and Intrinsic Bursting Pyramidal Cells Show Orthogonal Forms of Experience-Dependent Plasticity in Layer V of Barrel Cortex

Cited by 76 publications

References 70 publications

In vivo quantitative proteomics of somatosensory cortical synapses shows which protein levels are modulated by sensory deprivation

In vivo quantitative proteomics of somatosensory cortical synapses shows which protein levels are modulated by sensory deprivation

A modulatory effect of the feedback from higher visual areas to V1 in the mouse

Experience-dependent regulation of presynaptic NMDARs enhances neurotransmitter release at neocortical synapses

Contact Info

Product

Resources

About