Selective Disruption of Perineuronal Nets in Mice Lacking Crtl1 is Sufficient to Make Fear Memories Susceptible to Erasure

Poli, Andrea; Viglione, Aurelia; Mazziotti, Raffaele; Totaro, Valentino; Morea, Silvia; Melani, Riccardo; Silingardi, Davide; Putignano, Elena; Berardi, Nicoletta; Pizzorusso, Tommaso

doi:10.1007/s12035-023-03314-x

Cited by 7 publications

(6 citation statements)

References 66 publications

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“…After the threat of the rubber paw, we observed pupil dilation that can also be observed when only the threat is applied without prior exposition to the prosthesis and tactile stimulations (Figure S1). Pupil dilation has been shown to correlate with different arousal states (Reimer et al, 2014; Turner et al, 2023), attention (Abdolrahmani et al, 2021), as well as the processing of startling stimuli (Leuchs et al, 2019) and fear conditioning (Poli et al, 2023). We interpret this increase in pupil diameter as a sign that mice were strongly engaged by the arrival of the threat in all conditions in a similar manner.…”

Section: Discussionmentioning

confidence: 99%

Embodiment of an artificial limb in the mouse model

Hayatou,

Wang,

Chaillet

et al. 2024

Preprint

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Having the ability to probe the strength of limb embodiment is a requirement to better understand body ownership disorders that are triggered both by disease and by accidental body damage. It is also an essential tool towards the development of neuroprostheses that better integrate into the user's body representation. One key way to probe limb embodiment is through the rubber hand illusion. Here we adapted this paradigm to the mouse forelimb, which is a relevant model for upper limb research thanks to its diverse and rich behavioural characteristics and unparalleled access to genetic and optogenetic research tools. We exposed head-fixed mice to a visible, static 3D printed replica of their right forelimb, while their own forelimb was removed from their sight and stimulated by brush strokes in synchrony with the replica. Following these visuo-tactile stimulations, the replica was visually threatened, and we probed the mice reaction using automated tracking of pupils and facial expression. We found that mice focused significantly more their gaze towards the forelimb replica when they received congruent tactile and visual information, compared to control conditions. This observation is consistent with the human overt response to the rubber hand illusion. In summary, these findings indicate that mice can experience forelimb embodiment, and this phenomenon can be evaluated with the method we developed.

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Section: Discussionmentioning

confidence: 99%

Embodiment of an artificial limb in the mouse model

Hayatou,

Wang,

Chaillet

et al. 2024

Preprint

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“…HAPLN1 is emerging as an important extracellular molecule implicated in memory, independent of our use as a target for genetically encoded labeling in the ECM. Disrupting PNNs in a HAPLN1 (Crtl1) mouse knock-out model rendered fear memories susceptible to erasure 44 . HAPLN1 turnover was found to be relatively rapid in PNNs and at synapses 45 , and viral-mediated HAPLN1 delivery into mouse cortex showed that HAPLN1 is both necessary for PNN maturation in mice and when overexpressed can accelerate PNN and memory engram formation 46 .…”

Section: Discussionmentioning

confidence: 99%

Perineuronal nets and the neuronal extracellular matrix can be imaged by genetically encoded labeling of HAPLN1in vitroandin vivo

Lemieux,

Lev-Ram,

Tsien

et al. 2023

Preprint

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Neuronal extracellular matrix (ECM) and a specific form of ECM called the perineuronal net (PNN) are important structures for central nervous system (CNS) integrity and synaptic plasticity. PNNs are distinctive, dense extracellular structures that surround parvalbumin (PV)-positive inhibitory interneurons with openings at mature synapses. Enzyme-mediated PNN disruption can erase established memories and re-open critical periods in animals, suggesting that PNNs are important for memory stabilization and conservation. Here, we characterized the structure and distribution of several ECM/PNN molecules around neurons in culture, brain slice, and whole mouse brain. While specific lectins are well-established as PNN markers and label a distinct, fenestrated structure around PV neurons, we show that other CNS neurons possess similar extracellular structures assembled around hyaluronic acid, suggesting a PNN-like structure of different composition that is more widespread. We additionally report that genetically encoded labeling of hyaluronan and proteoglycan link protein 1 (HAPLN1) reveals a PNN-like structure around many neuronsin vitroandin vivo. Our findings add to our understanding of neuronal extracellular structures and describe a new mouse model for monitoring live ECM dynamics.

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“…The crucial role of the cartilage link protein Crtl1 in making fear memories resistant to deletion has been shown in the experimental model of fear extinction in Crtl1-KO mice [118]. Crtl1 is upregulated during brain development and participates in PNN condensation [46,143].…”

Section: Pnn In Fear and Memorymentioning

confidence: 99%

Perineuronal Net Microscopy: From Brain Pathology to Artificial Intelligence

Paveliev,

Egorchev,

Musin

et al. 2024

IJMS

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Perineuronal nets (PNN) are a special highly structured type of extracellular matrix encapsulating synapses on large populations of CNS neurons. PNN undergo structural changes in schizophrenia, epilepsy, Alzheimer’s disease, stroke, post-traumatic conditions, and some other brain disorders. The functional role of the PNN microstructure in brain pathologies has remained largely unstudied until recently. Here, we review recent research implicating PNN microstructural changes in schizophrenia and other disorders. We further concentrate on high-resolution studies of the PNN mesh units surrounding synaptic boutons to elucidate fine structural details behind the mutual functional regulation between the ECM and the synaptic terminal. We also review some updates regarding PNN as a potential pharmacological target. Artificial intelligence (AI)-based methods are now arriving as a new tool that may have the potential to grasp the brain’s complexity through a wide range of organization levels—from synaptic molecular events to large scale tissue rearrangements and the whole-brain connectome function. This scope matches exactly the complex role of PNN in brain physiology and pathology processes, and the first AI-assisted PNN microscopy studies have been reported. To that end, we report here on a machine learning-assisted tool for PNN mesh contour tracing.

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Selective Disruption of Perineuronal Nets in Mice Lacking Crtl1 is Sufficient to Make Fear Memories Susceptible to Erasure

Cited by 7 publications

References 66 publications

Embodiment of an artificial limb in the mouse model

Embodiment of an artificial limb in the mouse model

Perineuronal nets and the neuronal extracellular matrix can be imaged by genetically encoded labeling of HAPLN1in vitroandin vivo

Perineuronal Net Microscopy: From Brain Pathology to Artificial Intelligence

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