Cocaine-induced plasticity in the cerebellum of sensitised mice

Vázquez-Sanromán, Dolores; Carbó-Gas, Maria; Leto, Ketty; Cerezo-Garcia, Miguel; Gil‐Miravet, Isis; Sanchis‐Segura, Carles; Carulli, Daniela; Rossi, Ferdinando; Miquel, Marta

doi:10.1007/s00213-015-4072-1

Cited by 31 publications

(18 citation statements)

References 57 publications

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“…PNNs are modified by a variety of stimuli, including cocaine exposure [34,59], cocaine-CPP acquisition [21], alcohol [60,61], nicotine self-administration [62], heroin self-administration [63], sleep deprivation [40],environmental enrichment [64], and consumption of high fat diets [32]. A majority of PV FSIs within the PL PFC are surrounded by PNNs, and previous work by our group has shown that the amount of cocaine exposure differentially affected PNN and PV expression [34].…”

Section: Discussionmentioning

confidence: 99%

Cocaine memory reactivation induces functional adaptations of fast-spiking interneurons in the rat medial prefrontal cortex

Jorgensen

Gonzalez

Harkness

et al. 2019

Preprint

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Perineuronal nets (PNNs) are specialized extracellular matrix structures that ensheathe parvalbumin-containing fast-spiking interneurons (PV FSIs) and play a key role in neuroplasticity. We previously showed that PNNs within the prelimbic prefrontal cortex (PL PFC) are required for the maintenance of cocaine-associated memories following cocaine memory reactivation. However, how cocaine memory reactivation affects PNNs, PV, and corresponding changes in PV FSI function are unknown. In this study, we characterized the electrophysiological properties of PV FSIs and corresponding changes in PNN and PV intensity within the PL PFC prior to and after cocaine memory reactivation. Adult male Sprague-Dawley rats were trained to acquire cocaine-conditioned place preference (CPP) and, following cocaine-CPP memory reactivation (30 m, 2 h, and 24 h post-reactivation), we measured PNN intensity (determined by Wisteria floribunda agglutinin [WFA] staining) as well as PV intensity using immunohistochemistry. The intensity of PV staining was reduced at all time points following memory reactivation with no changes in WFA intensity. Using whole-cell electrophysiology we found a reduction in the number of action potentials at 30 m and 2 h that returned to control levels by 24 h. The attenuation in firing was accompanied by a presumed compensatory increase in excitatory synaptic transmission, which was corroborated by an increase in VGluT1 puncta apposing PV/PNN neurons. Collectively, our results indicate that cocaine memory reactivation decreases PV intensity, which may play a role in decreasing excitation of PV FSIs. Thus, the inhibitory tone onto pyramidal neurons may be decreased following memory reactivation, resulting in an increase in PFC output to promote cocaine-seeking behaviors.

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Section: Discussionmentioning

confidence: 99%

Cocaine memory reactivation induces functional adaptations of fast-spiking interneurons in the rat medial prefrontal cortex

Jorgensen

Gonzalez

Harkness

et al. 2019

Preprint

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“…We examined 8–15 sum-slice images from each brain area to compare three methods of quantification: “Point”, “ROI”, and PIPSQUEAK; the latter is the automated version of “ROI” (see below). The Point method has been used in previous studies (Foscarin et al, 2011, Carulli et al, 2013, Vazquez-Sanroman et al, 2015a). For the Point method, an experimenter blind to the treatment conditions randomly selected 15 points (pixels) within a PNN.…”

Section: Methodsmentioning

confidence: 99%

“…An increasing number of studies examining the contribution of PNNs to various behaviors and types of plasticity have analyzed the fluorescence intensity of WFA as an indirect measure of the maturity of PNNs – with mature PNNs labeled with more intense WFA stain and immature PNNs labeled with less intense WFA stain (Foscarin et al, 2011, Cabungcal et al, 2013a, Cabungcal et al, 2013b, Carulli et al, 2013, Happel et al, 2014, Chen et al, 2015, Slaker et al, 2015, Vazquez-Sanroman et al, 2015a, Vazquez-Sanroman et al, 2015b). While WFA intensity is important for formulating experiments and interpreting the findings, the method by which WFA intensity is measured and analyzed has been inconsistent across studies.…”

Section: Introductionmentioning

confidence: 99%

“…Some studies have used semi-quantitative methods to examine relative intensity changes, but these studies lack measures of individual PNNs (Wang et al, 2011, Deak et al, 2012, Yamada and Jinno, 2013, Racz et al, 2014, Kecskes et al, 2015). Other studies examine changes in individual PNNs by averaging the intensity of 15 pixels within a given PNN around the soma (Foscarin et al, 2011, Carulli et al, 2013, Vazquez-Sanroman et al, 2015a), and others have not included details in the methodology (Chen et al, 2015). The diversity of analyses within this relatively young, but rapidly growing area of study makes it difficult to compare analyses across studies that have identified important changes in PNN staining intensity.…”

Section: Introductionmentioning

confidence: 99%

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A standardized and automated method of perineuronal net analysis using Wisteria floribunda agglutinin staining intensity

2016

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Perineuronal nets (PNNs) are aggregations of extracellular matrix molecules that are critical for plasticity. Their altered development or changes during adulthood appear to contribute to a wide range of diseases/disorders of the brain. An increasing number of studies examining the contribution of PNN to various behaviors and types of plasticity have analyzed the fluorescence intensity of Wisteria floribunda agglutinin (WFA) as an indirect measure of the maturity of PNNs, with brighter WFA staining corresponding to a more mature PNN and dim WFA staining corresponding to an immature PNN. However, a clearly-defined and unified method for assessing the intensity of PNNs is critical to allow us to make comparisons across studies and to advance our understanding of how PNN plasticity contributes to normal brain function and brain disease states. Here we examined methods of PNN intensity quantification and demonstrate that creating a region of interest around each PNN and subtracting appropriate background is a viable method for PNN intensity quantification that can be automated. This method produces less variability and bias across experiments compared to other published analyses, and this method increases reproducibility and reliability of PNN intensity measures, which is critical for comparisons across studies in this emerging field.

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“…The intensity of the PNN marker WFA is altered after cocaine, ethanol, and nicotine exposure throughout the brain [34, 37–39]. More specifically, cocaine has been shown to both increase and decrease WFA intensity in the cerebellum, which is dependent on the time course, stage of withdrawal, and a cocaine challenge [34, 37]. Collectively, these findings suggest that exposure to drugs of abuse changes PNN expression in a time dependent manner within multiple brain regions.…”

Section: Discussionmentioning

confidence: 99%

Role of perineuronal nets in the anterior dorsal lateral hypothalamic area in the acquisition of cocaine-induced conditioned place preference and self-administration

2017

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Addiction involves drug-induced neuroplasticity in the circuitry of motivated behavior, which includes the medial forebrain bundle and the lateral hypothalamic area. Emerging at the forefront of neuroplasticity regulation are specialized extracellular matrix (ECM) structures that form perineuronal nets (PNNs) around certain neurons, mainly parvalbumin positive (PV+), fast-spiking interneurons (FSINs), making them a promising target for the regulation of drug-induced neuroplasticity. Despite the emerging significance of PNNs in drug-induced neuroplasticity and the well-established role of the lateral hypothalamic area (LHA) in reward, reinforcement, and motivation, very little is known about how PNN-expressing neurons control drug-seeking behavior. We found that a discrete region of the anterior dorsal LHA (LHAad) exhibited robust PNN and dense ECM expression. Approximately 87% of parvalbumin positive (PV+) neurons co-expressed the PNN marker Wisteria floribunda agglutinin (WFA), while 62% of WFA positive (WFA+) neurons co-expressed PV in the LHAad of drug naïve rats. Removal of PNNs within this brain region via chrondroitinase ABC (Ch-ABC) administration abolished acquisition of cocaine-induced CPP and significantly attenuated the acquisition of cocaine self-administration (SA). Removal of LHAad PNNs did not affect locomotor activity, sucrose intake, sucrose-induced CPP, or acquisition of sucrose SA in separate groups of cocaine naïve animals. These data suggest that PNN-dependent neuroplasticity within the LHAad is critical for the acquisition of both cocaine-induced CPP and SA but is not general to all rewards, and that PNN degradation may have utility for the management of drug-associated behavioral plasticity and memory in cocaine addicts.

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Cocaine-induced plasticity in the cerebellum of sensitised mice

Cited by 31 publications

References 57 publications

Cocaine memory reactivation induces functional adaptations of fast-spiking interneurons in the rat medial prefrontal cortex

Cocaine memory reactivation induces functional adaptations of fast-spiking interneurons in the rat medial prefrontal cortex

A standardized and automated method of perineuronal net analysis using Wisteria floribunda agglutinin staining intensity

Role of perineuronal nets in the anterior dorsal lateral hypothalamic area in the acquisition of cocaine-induced conditioned place preference and self-administration

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