Experience-dependent modulation of extracellular matrix integrity supports perceptual skill learning and memory

Area of Science:

• Neuroscience
• Cell Biology

Background:

• Perceptual learning enhances sensory skills but demands extensive training.
• Neural mechanisms of learning, particularly the extracellular matrix (ECM), are key to accelerating skill acquisition.
• The ECM's proposed role in learning involves degradation for plasticity and reaccumulation for stabilization, but its timescale conflicts with perceptual learning dynamics.

Purpose of the Study:

• To investigate the temporal dynamics of ECM changes during auditory perceptual learning.
• To determine the ECM's role in regulating skill acquisition and memory consolidation.
• To resolve the discrepancy between the ECM's traditional time course and perceptual learning's rapid daily gains.

Main Methods:

• Tracking and manipulating auditory cortical ECM integrity in Mongolian gerbils during perceptual learning.
• Utilizing enzymatic digestion with chondroitinase ABC (chABC) to alter ECM composition.
• Assessing the impact of ECM manipulation on learning performance and memory stability.

Main Results:

• The ECM exhibits rapid, training-induced degradation and recovery within 24 hours per session.
• The ECM's degradation-recovery cycle diminished with training and disappeared upon performance plateau.
• Enzymatic ECM digestion impaired perceptual learning and destabilized acquired memories.

Conclusions:

• The ECM is a critical regulator of perceptual learning, with rapid, experience-dependent changes.
• A decrease in ECM degradation with training limits further plasticity, preserving learned representations.
• This study reframes the ECM's role in learning, aligning its dynamics with rapid skill acquisition and consolidation.