Whisker Deprivation Drives Two Phases of Inhibitory Synapse Weakening in Layer 4 of Rat Somatosensory Cortex

Gainey, Melanie; Wolfe, Renna; Pourzia, Olivia; Feldman, Daniel E.

doi:10.1371/journal.pone.0148227

Cited by 12 publications

(10 citation statements)

References 47 publications

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“…5G; 17.25 +/-2.44 vs. 17.13 +/-1.86 spines/10 microns). Taken together, our data confirm that whisker deprivation induced a homeostatic response in the contralateral hemisphere 48 hours after trimming, as previously reported (Gainey et al, 2016(Gainey et al, , 2018Knott et al, 2002;Li et al, 2014).…”

Section: Sensory Deprivation Induces a Homeostatic Response In The Basupporting

confidence: 92%

“…Sensory deprivation of the visual cortex, for example, reduces cortical inhibition, which increases spontaneous activity and lowers the threshold for LTP (Benevento et al, 1992;Bridi et al, 2018;Kirkwood et al, 1996;Kuhlman et al, 2013). Similarly, whisker trimming, an established model for sensory deprivation of somatosensory (barrel) cortex (Gainey et al, 2016(Gainey et al, , 2018Gray et al, 2006), has been shown to increase the ratio of excitation to inhibition (E/I): while both excitation and inhibition decrease after whisker trimming, inhibition decreases more (Gainey et al, 2018;Li et al, 2014). Given the evidence that sensory deprivation alters both excitation and inhibition, we asked whether whisker trimming induces an upscaling or downscaling-like homeostatic PIN response.…”

Section: Sensory Deprivation Induces a Homeostatic Response In The Bamentioning

confidence: 99%

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Homeostatic Plasticity Requires Remodeling of the Homer-Shank Interactome

We¹,

Speed²,

Jd³

et al. 2020

Preprint

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Neurons maintain constant levels of excitability using homeostatic scaling, which adjusts relative synaptic strength in response to large changes in overall activity. While previous studies have catalogued the transcriptomic and proteomic changes associated with scaling, the resulting alterations in synaptic protein interaction networks (PINs) are less well understood. Here, we monitor a glutamatergic synapse PIN composed of 380 binary interactions among 21 protein members to identify protein complexes altered by synaptic scaling. In cultured cortical neurons, we observe widespread bidirectional PIN alterations with up-versus downscaling. In the barrel cortex, the PIN response to 48 hours of sensory deprivation exhibits characteristics of both upscaling and downscaling, consistent with emerging models of excitatory/inhibitory balance in cortical plasticity. Mice lacking Homer1 or Shank3B do not undergo normal PIN rearrangements, suggesting that these Autism Spectrum Disorder (ASD)-linked proteins serve as structural hubs for synaptic homeostasis. Our approach demonstrates how previously identified RNA and protein-level changes induced during homeostatic scaling translate into functional PIN alterations.

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Section: Sensory Deprivation Induces a Homeostatic Response In The Basupporting

confidence: 92%

Section: Sensory Deprivation Induces a Homeostatic Response In The Bamentioning

confidence: 99%

Homeostatic Plasticity Requires Remodeling of the Homer-Shank Interactome

We¹,

Speed²,

Jd³

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…We also measured the miniature inhibitory postsynaptic currents (mIPSC) to test whether the increase in inhibitory synaptic density (Sarma et al, 2011) could also reflects an increase in local number of sites of GABAergic synapses. Moreover, as development of inhibitory circuit in neocortex can be driven by sensory experience, and the sensory‐deprived animals often show a weaker inhibition and persistence of immature synaptic phenotypes (Jiao et al, 2006; Kreczko et al, 2009; Gainey et al, 2016), we also studied the GABAergic synaptic transmission after early postnatal olfactory deprivation. Therefore, considering that the inhibitory cortical circuits in the aPC can be formed via combination of intrinsic neuronal and environmental changes during the maturation process, we evaluated the sIPSC and mIPSC in aPC of both hemispheres of unilateral naris‐occluded rats.…”

Section: Introductionmentioning

confidence: 99%

Postnatal development of inhibitory synaptic transmission in the anterior piriform cortex

Pardo

Lucion

Calcagnotto

2018

Intl J of Devlp Neuroscience

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The morphological and functional development of inhibitory circuit in the anterior piriform cortex (aPC) during the first three postnatal weeks may be crucial for the development of odor preference learning in infant rodents. As first step toward testing this hypothesis, we examined the normal development of GABAergic synaptic transmission in the aPC of rat pups during the postnatal days (P) 5-8 and 14-17. Whole cell patch-clamp recordings of layer 2/3 (L2/3) aPC pyramidal cells revealed a significant increase in spontaneous (sIPSC) and miniature (mIPSC) inhibitory postsynaptic current frequencies and a decrease in mIPSC rise and decay-time constant at P14-P17. Moreover, as the development of neocortical inhibitory circuit can be driven by sensory experience, we recorded sIPSC and mIPSC onto L2/3 aPC pyramidal cells from unilateral naris-occluded animals. Early partial olfactory deprivation caused by naris occlusion do not affected the course of age-dependent increase IPSC frequency onto L2/3 aPC pyramidal cell. However, this age-dependent increase of sIPSC and mIPSC frequencies were lower on aPC pyramidal cells ipsilateral to the occlusion side. In addition, the age-dependent increase in sIPSC frequency and amplitude were more pronounced on aPC pyramidal cells contralateral to the occlusion. While mIPSC kinetics were not affected by age or olfactory deprivation, at P5-P8, the sIPSC decay-time constant on aPC pyramidal cells of both hemispheres of naris-occluded animals were significantly higher when compared to sham. These results demonstrated that the GABAergic synaptic transmission on the aPC changed during postnatal development by increasing inhibitory inputs on L2/3 pyramidal cells, with increment in frequency of both sIPSC and mIPSC and faster kinetics of mIPSC. Our data suggested that the maturation of GABAergic synaptic transmission was little affected by early partial olfactory deprivation. These results could contribute to unravel the mechanisms underlying the development of odor processing and olfactory preference learning.

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“…It is important to note that our protocol of partial sensory deprivation (whisker trimming) was applied to adult mice only (3–4 months old) and did not include follicle removal or cauterization. Moreover, considering the short duration of the deprivation (7 days), we do not believe that the results of this study are a consequence of cortical map plasticity, widely described in neurodevelopmental and plasticity studies using the barrel-cortex system model (Van der Loos and Woolsey, 1973 ; Woolsey and Wann, 1976 ; Levin and Dunn-Meynell, 1991 ; Dunn-Meynell et al, 1992 ; Siucinska and Kossut, 1994 ; Melzer and Smith, 1996 ; Kossut and Juliano, 1999 ; Fox, 2002 ; Allen et al, 2003 ; Rema et al, 2003 ; Schierloh et al, 2003 ; Shepherd et al, 2003 ; Dubroff et al, 2005 ; Fox and Wong, 2005 ; Shoykhet et al, 2005 ; Frostig, 2006 ; Lee et al, 2007 ; Schubert et al, 2007 ; Drew and Feldman, 2009 ; Wu et al, 2011 ; Gainey et al, 2016 ; Jacob et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

In Vivo Visualization of Active Polysynaptic Circuits With Longitudinal Manganese-Enhanced MRI (MEMRI)

Almeida-Corrêa

Czisch

Wotjak

2018

Front. Neural Circuits

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Manganese-enhanced magnetic resonance imaging (MEMRI) is a powerful tool for in vivo non-invasive whole-brain mapping of neuronal activity. Mn2+ enters active neurons via voltage-gated calcium channels and increases local contrast in T1-weighted images. Given the property of Mn2+ of axonal transport, this technique can also be used for tract tracing after local administration of the contrast agent. However, MEMRI is still not widely employed in basic research due to the lack of a complete description of the Mn2+ dynamics in the brain. Here, we sought to investigate how the activity state of neurons modulates interneuronal Mn2+ transport. To this end, we injected mice with low dose MnCl2 2. (i.p., 20 mg/kg; repeatedly for 8 days) followed by two MEMRI scans at an interval of 1 week without further MnCl2 injections. We assessed changes in T1 contrast intensity before (scan 1) and after (scan 2) partial sensory deprivation (unilateral whisker trimming), while keeping the animals in a sensory enriched environment. After correcting for the general decay in Mn2+ content, whole brain analysis revealed a single cluster with higher signal in scan 1 compared to scan 2: the left barrel cortex corresponding to the right untrimmed whiskers. In the inverse contrast (scan 2 > scan 1), a number of brain structures, including many efferents of the left barrel cortex were observed. These results suggest that continuous neuronal activity elicited by ongoing sensory stimulation accelerates Mn2+ transport from the uptake site to its projection terminals, while the blockage of sensory-input and the resulting decrease in neuronal activity attenuates Mn2+ transport. The description of this critical property of Mn2+ dynamics in the brain allows a better understanding of MEMRI functional mechanisms, which will lead to more carefully designed experiments and clearer interpretation of the results.

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Whisker Deprivation Drives Two Phases of Inhibitory Synapse Weakening in Layer 4 of Rat Somatosensory Cortex

Cited by 12 publications

References 47 publications

Homeostatic Plasticity Requires Remodeling of the Homer-Shank Interactome

Homeostatic Plasticity Requires Remodeling of the Homer-Shank Interactome

Postnatal development of inhibitory synaptic transmission in the anterior piriform cortex

In Vivo Visualization of Active Polysynaptic Circuits With Longitudinal Manganese-Enhanced MRI (MEMRI)

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