Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex

Harkness, John H.; Gonzalez, Angela E.; Bushana, Priyanka N.; Jorgensen, Emily T.; Hegarty, Deborah M.; Nardo, Ariel A. Di; Prochiantz, Alain; Wisor, Jonathan P.; Aicher, Sue A.; Brown, Travis E.; Sorg, Barbara A.

doi:10.1101/2020.10.25.354134

Cited by 3 publications

(12 citation statements)

References 114 publications

(42 reference statements)

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“…We interpret our results as altered PNN composition rather than fluctuating numbers of PNNs. Similar diurnal rhythms in PNN composition were reported recently in the rat medial prefrontal cortex (Harkness et al, 2020). Decreased PNN composition during sleep (Pantazopoulos et al, 2020a) coincides with reduced LTP amplitude during the light phase in the hippocampus (Chaudhury et al, 2005).…”

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationsupporting

confidence: 84%

“…Diurnal and circadian fluctuations in excitatory/inhibitory balance have also been reported in rodents and humans (Chellappa et al, 2016;Bridi et al, 2020). Circadian rhythms in PNN composition may contribute to daily rhythms in excitatory/inhibitory balance through regulation of PVB neuron firing as well as regulation of excitatory and inhibitory synapses on PVB soma (Carceller et al, 2020;Harkness et al, 2020). Taken together, these data suggest that PNN composition changes during sleep may in part contribute to synaptic downscaling by allowing increased inhibitory inhibition for synapse depotentiation by PVB neurons.…”

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationmentioning

confidence: 64%

“…Day/night differences in the AMPA/NMDA ratio were reported recently in the rat medial prefrontal cortex, with increased AMPA/NMDA ratio during the night (ZT18) compared to the day (ZT6). This was accompanied by increased vGlut1 glutamatergic synapses on PVB neurons at ZT18 and increased PNN intensity (Harkness et al, 2020).…”

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationmentioning

confidence: 93%

“…Circadian rhythms of PNN composition (Harkness et al, 2020;Pantazopoulos et al, 2020a) may also contribute to memory consolidation through the regulation of PVB neuron firing properties. GABAergic inhibition of excitatory neurons is proposed to contribute to synaptic downscaling by promoting long term depression (LTD) (Niethard et al, 2016), in agreement with reported decreased LTP amplitude during the light phase (Chaudhury et al, 2005).…”

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationmentioning

confidence: 99%

“…Several studies point to multiple pathways in which neurons and microglia may modify PNN composition (Bertocchi et al, 2020;Harkness et al, 2020;Nguyen et al, 2020;Pantazopoulos et al, 2020a). Neurons signal to microglia through IL-33 to promote experience dependent synaptic plasticity in part by stimulating engulfment of ECMs (Nguyen et al, 2020).…”

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationmentioning

confidence: 99%

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Sleep and Memory Consolidation Dysfunction in Psychiatric Disorders: Evidence for the Involvement of Extracellular Matrix Molecules

et al. 2021

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Sleep disturbances and memory dysfunction are key characteristics across psychiatric disorders. Recent advances have revealed insight into the role of sleep in memory consolidation, pointing to key overlap between memory consolidation processes and structural and molecular abnormalities in psychiatric disorders. Ongoing research regarding the molecular mechanisms involved in memory consolidation has the potential to identify therapeutic targets for memory dysfunction in psychiatric disorders and aging. Recent evidence from our group and others points to extracellular matrix molecules, including chondroitin sulfate proteoglycans and their endogenous proteases, as molecules that may underlie synaptic dysfunction in psychiatric disorders and memory consolidation during sleep. These molecules may provide a therapeutic targets for decreasing strength of reward memories in addiction and traumatic memories in PTSD, as well as restoring deficits in memory consolidation in schizophrenia and aging. We review the evidence for sleep and memory consolidation dysfunction in psychiatric disorders and aging in the context of current evidence pointing to the involvement of extracellular matrix molecules in these processes.

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Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationsupporting

confidence: 84%

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationmentioning

confidence: 64%

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationmentioning

confidence: 93%

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationmentioning

confidence: 99%

Section: Extracellular Matrix: Evidence For Involvement In Memory Consolidationmentioning

confidence: 99%

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Sleep and Memory Consolidation Dysfunction in Psychiatric Disorders: Evidence for the Involvement of Extracellular Matrix Molecules

et al. 2021

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Circadian desynchronization attenuates information throughput of prefrontal cortex pyramidal neurons in mice

Roberts

Karatsoreos

2022

Preprint

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Circadian rhythms are ubiquitous in biology, from the molecular to behavioral levels. There is growing interest in understanding the functional implications of circadian oscillations in different cells and systems, including the brain. The prefrontal cortex (PFC) is heavily involved in myriad processes, including working memory, cognition, stress responses, and fear associated behaviors. Many PFC associated behaviors are time-of-day dependent, yet how time-of-day impacts the basic function of neurons in the PFC is not known. Here we use patch-clamp electrophysiology to record from layer 2/3 pyramidal neurons in the prelimbic (pl) PFC of male and female C57BL/6J mice at 4 separate bins of zeitgeber time (ZT): 0-4, 6-10, 12-16, and 18-22. We measured changes in membrane properties, inhibitory and excitatory inputs, ion channel function, and action potential kinetics. We demonstrate that the activity of plPFC neurons, their inhibitory inputs, and action potential dynamics are regulated by time-of-day. Further, we show that in males postsynaptic K+ channels play a central role in mediating these rhythms, suggesting the potential for an intrinsic gating mechanism mediating information throughput. These key discoveries in PFC physiology demonstrate the importance of understanding how daily rhythms contribute to the mechanisms underlying the basic functions of PFC circuitry.

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Perineuronal nets in the rat medial prefrontal cortex alter hippocampal-prefrontal oscillations and reshape cocaine self-administration memories

Wingert,

Ramos,

Reynolds

et al. 2024

Preprint

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The medial prefrontal cortex (mPFC) is a major contributor to relapse to cocaine in humans and to reinstatement behavior in rodent models of cocaine use disorder. Output from the mPFC is modulated by parvalbumin (PV)-containing fast-spiking interneurons, the majority of which are surrounded by perineuronal nets (PNNs). Here we tested whether chondroitinase ABC (ABC)- mediated removal of PNNs prevented the acquisition or reconsolidation of a cocaine self-administration memory. ABC injections into the dorsal mPFC prior to training attenuated the acquisition of cocaine self-administration. Also, ABC given 3 days prior to but not 1 hr after memory reactivation blocked cue-induced reinstatement. However, reduced reinstatement was present only in rats given anovelreactivation contingency, suggesting that PNNs are required for the updating of a familiar memory. In naive rats, ABC injections into mPFC did not alter excitatory or inhibitory puncta on PV cells but reduced PV intensity. Whole-cell recordings revealed a greater inter-spike interval 1 hr after ABC, but not 3 days later.In vivorecordings from the mPFC and dorsal hippocampus (dHIP) during novel memory reactivation revealed that ABC in the mPFC prevented reward-associated increases in beta and gamma activity as well as phase-amplitude coupling between the dHIP and mPFC. Together, our findings show that PNN removal attenuates the acquisition of cocaine self-administration memories and disrupts reconsolidation of the original memory when combined with a novel reactivation session. Further, reduced dHIP/mPFC coupling after PNN removal may serve as a key biomarker for how to disrupt reconsolidation of cocaine memories and reduce relapse.

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Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex

Cited by 3 publications

References 114 publications

Sleep and Memory Consolidation Dysfunction in Psychiatric Disorders: Evidence for the Involvement of Extracellular Matrix Molecules

Sleep and Memory Consolidation Dysfunction in Psychiatric Disorders: Evidence for the Involvement of Extracellular Matrix Molecules

Circadian desynchronization attenuates information throughput of prefrontal cortex pyramidal neurons in mice

Perineuronal nets in the rat medial prefrontal cortex alter hippocampal-prefrontal oscillations and reshape cocaine self-administration memories

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