Effects of drugs of abuse on hippocampal plasticity and hippocampus-dependent learning and memory: contributions to development and maintenance of addiction

Kutlu, Munir Gunes; Gould, Thomas J.

doi:10.1101/lm.042192.116

Cited by 255 publications

(176 citation statements)

References 420 publications

(438 reference statements)

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“…Interestingly, abnormal RC connectivity was found in the hippocampus, caudate, and pallidum (Figure 3D), regions of dense distribution of CB1 receptors in the brain (Svizenska, et al, 2008). In addition, the hippocampus and dorsal striatum play important roles in contextual learning and habit formation that maintain addictive behaviors (Koob and Volkow, 2016; Kutlu and Gould, 2016). In the present data, the hippocampus of CB users showed higher regional SC-FC coupling, while the caudate of users had a reduced coupling level (Figure 3E).…”

Section: Discussionmentioning

confidence: 99%

Aberrant structural–functional coupling in adult cannabis users

Kim

Martin

Shin³

et al. 2018

Human Brain Mapping

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Cellular studies indicate that endocannabinoid type-1 retrograde signaling plays a major role in synaptic plasticity. Disruption of these processes by delta-9-tetrahydrocannabinol (THC) could produce alterations either in structural and functional brain connectivity or in their association in cannabis (CB) users. Graph theoretic structural and functional networks were generated with diffusion tensor imaging and resting-state functional imaging in 37 current CB users and 31 healthy non-users. The primary outcome measures were coupling between structural and functional connectivity, global network characteristics, association between the coupling and network properties, and measures of rich-club organization. Structural-functional (SC-FC) coupling was globally preserved showing a positive association in current CB users. However, the users had disrupted associations between SC-FC coupling and network topological characteristics, most perturbed for shorter connections implying region-specific disruption by CB use. Rich-club analysis revealed impaired SC-FC coupling in the hippocampus and caudate of users. This study provides evidence of the abnormal SC-FC association in CB users. The effect was predominant in shorter connections of the brain network, suggesting that the impact of CB use or predispositional factors may be most apparent in local interconnections. Notably, the hippocampus and caudate specifically showed aberrant structural and functional coupling. These structures have high CB1 receptor density and may also be associated with changes in learning and habit formation that occur with chronic cannabis use.

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Section: Discussionmentioning

confidence: 99%

Aberrant structural–functional coupling in adult cannabis users

Kim

Martin

Shin³

et al. 2018

Human Brain Mapping

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“…The mechanisms underlying the causes of drug addiction are not entirely known, but it is thought that the processes of learning and memory are essential and that the hippocampus plays a key role in contextual conditioning and cocaine addiction 1,2 . In fact, addiction has been considered as a type of nonadaptive learning 3 .…”

Section: Introductionmentioning

confidence: 99%

3d Synaptic Organization of the Rat Ca1 and Alterations Induced by Cocaine Self-Administration

Blázquez-Llorca

Miguéns

Montero-Crespo

et al. 2020

Preprint

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The hippocampus plays a key role in contextual conditioning and has been proposed as an important component of the cocaine addiction brain circuit.To gain knowledge about cocaine-induced alterations in this circuit, we used Focused Ion Beam milling/Scanning Electron Microscopy (FIB/SEM) to reveal and quantify the 3D synaptic organization of the stratum radiatum of rat CA1, under normal circumstances and after cocaine-self administration (SA). Most synapses are asymmetric (excitatory), macular-shaped, and in contact with spine heads. After cocaine-SA, the size and complexity of both asymmetric and symmetric (inhibitory) synapses increased but no changes were observed in the synaptic density.This work constitutes the first detailed report on the 3D synaptic organization in the stratum radiatum of the CA1 field of cocaine-SA rats. Our data contribute to the elucidation of the normal and altered synaptic organization of the hippocampus, which is crucial for better understanding the neurobiological mechanisms underlying cocaine addiction.

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“…We also assessed CA1 spine motility for comparison. Like the BLA, the dorsal HPC is a critical component of the neural circuit supporting drug-associated memories and we have reported spine density increases in CA1 with METH learning, as in the BLA (31,43). However, METH memories do not bear the same vulnerability to disruption when NMII is specifically inhibited in CA1 and, unlike BLA spines, METH-induced CA1 spine density increases remain intact after systemic Blebb treatment (31).…”

mentioning

confidence: 67%

Methamphetamine learning induces persistent nonmuscle myosin II-dependent spine motility in the basolateral amygdala

Young

Hua²,

Kamenecka³

et al. 2019

Preprint

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Nonmuscle myosin II inhibition (NMIIi) in the basolateral amygdala (BLA) selectively disrupts memories associated with methamphetamine (METH) days after learning, without retrieval.However, the molecular mechanisms underlying this selective vulnerability remain poorly understood. A known function of NMII is to transiently activate dendritic spine actin dynamics with learning. Therefore, we hypothesized that METH-associated learning perpetuates NMIIdriven actin dynamics in dendritic spines, leading to an extended window of vulnerability for memory disruption. Two-photon imaging of actin-mediated spine motility in neurons from memory-related structures, BLA and CA1, revealed a persistent increase in spine motility after METH-associated learning that was restricted to BLA neurons. METH-induced changes to BLA spine dynamics were reversed by a single systemic injection of an NMII inhibitor. Thus, a perpetual form of NMII-driven spine actin dynamics in BLA neurons may contribute to the unique susceptibility of METH-associated memories.Dendritic spines are small, actin-rich structures lining dendrites of excitatory neurons.These postsynaptic compartments are dynamic and enable input-specific biochemical and electrical isolation of synapses to facilitate signal transduction and information storage (1-3).During learning, dendritic spines undergo both structural and functional changes to stabilize synapses and, ultimately, memory (4, 5). Consistent with this, there is a tight connection between the physical geometry of spines and the ability to transform experiences into long-term memory (6-8). Polymerization of actin, the elongation and complex branching of filamentous actin (F-actin), drives the spine structural plasticity that is required for functional plasticity and learning (9-14).Interestingly, long-term potentiation (LTP) and newly formed memories become impervious to actin depolymerization shortly after the underlying synaptic plasticity occurs (15)(16)(17). This is attributed to rapid stabilization of the actin cytoskeleton through the cessation of polymerization and recruitment of actin capping and stabilizing proteins (18). However, we recently made the unexpected discovery that memories associated with the commonly abused stimulant, methamphetamine (METH), remain uniquely susceptible to actin depolymerization many days after learning (19). Indeed, a single infusion of the actin depolymerizer, Latrunculin A (LatA) into the basolateral amygdala (BLA) results in an immediate, long-lasting and retrievalindependent loss of the METH-associated memory and associated drug seeking behavior.Furthermore, this memory loss is accompanied by a return of BLA spine density to pre-METH conditioning levels. LatA works by sequestering actin monomers, removing them from the pool available for addition to F-actin during polymerization (20,21). In this way, LatA influences populations of dynamic, but not stable, actin. Thus the susceptibility of a METH-associated memory days after learning suggests that METH may interfere with the ...

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Effects of drugs of abuse on hippocampal plasticity and hippocampus-dependent learning and memory: contributions to development and maintenance of addiction

Cited by 255 publications

References 420 publications

Aberrant structural–functional coupling in adult cannabis users

Aberrant structural–functional coupling in adult cannabis users

3d Synaptic Organization of the Rat Ca1 and Alterations Induced by Cocaine Self-Administration

Methamphetamine learning induces persistent nonmuscle myosin II-dependent spine motility in the basolateral amygdala

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