Perineuronal Nets in the Adult Sensory Cortex Are Necessary for Fear Learning

• Published in: Neuron (Cambridge, Mass.) Mass.), 2017-07, Vol.95 (1), p.169-179.e3
• Main Authors: Banerjee, Sunayana B., Gutzeit, Vanessa A., Baman, Justin, Aoued, Hadj S., Doshi, Nandini K., Liu, Robert C., Ressler, Kerry J.
• Format: Article
• Language: English
• Subjects: Adults; Animals; auditory cortex; Auditory Cortex - drug effects; Auditory Cortex - metabolism; Auditory Cortex - physiology; Auditory plasticity; Aversion learning; Chondroitinase ABC; Conditioning; Conditioning (Psychology) - drug effects; Conditioning (Psychology) - physiology; Consolidation; Cortex (auditory); Cortex (somatosensory); Electrochemical machining; Extracellular matrix; Extracellular Matrix - metabolism; Extracellular Matrix - physiology; Fear & phobias; Fear - drug effects; Fear - physiology; Fear conditioning; GABA-A Receptor Agonists - pharmacology; hearing; Learning; Learning - drug effects; Learning - physiology; Memory; Memory Consolidation - drug effects; Memory Consolidation - physiology; Mice; mRNA; Muscimol - pharmacology; Nets; Neurons; Observational learning; perceptual learning; Perineuronal nets; plasticity; Proteoglycans - genetics; Proteoglycans - metabolism; PTSD; RNA, Messenger - metabolism; Rodents; Serial learning
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2017.06.007

Lattice-like structures known as perineuronal nets (PNNs) are key components of the extracellular matrix (ECM). Once fully crystallized by adulthood, they are largely stable throughout life. Contrary to previous reports that PNNs inhibit processes involving plasticity, here we report that the dynamic regulation of PNN expression in the adult auditory cortex is vital for fear learning and consolidation in response to pure tones. Specifically, after first confirming the necessity of auditory cortical activity for fear learning and consolidation, we observed that mRNA levels of key proteoglycan components of PNNs were enhanced 4 hr after fear conditioning but were no longer different from the control groups 24 hr later. A similar pattern of regulation was observed in numbers of cells surrounded by PNNs and area occupied by them in the auditory cortex. Finally, the removal of auditory cortex PNNs resulted in a deficit in fear learning and consolidation. •Auditory cortex activity after auditory fear conditioning is necessary for learning•Removal of PNNs from the auditory cortex of adult mice decreases fear learning•Regrowth of PNNs restores the ability to learn new memories•Temporal regulation of PNNs occurs in response to fear learning Banerjee et al., 2017 show that key components of the extracellular matrix, perineuronal nets (PNNs) in the auditory cortex of adult mice, are necessary for consolidation of fear learning in response to Pavlovian fear conditioning.