The extracellular matrix regulates cortical layer dynamics and cross-columnar frequency integration in the auditory cortex

Abstract

In the adult vertebrate brain, enzymatic removal of the extracellular matrix (ECM) is increasingly recognized to promote learning, memory recall, and restorative plasticity. The impact of the ECM on translaminar dynamics during cortical circuit processing is still not understood. Here, we removed the ECM in the primary auditory cortex (ACx) of adult Mongolian gerbils using local injections of hyaluronidase (HYase). Using laminar current-source density (CSD) analysis, we found layer-specific changes of the spatiotemporal synaptic patterns with increased cross-columnar integration and simultaneous weakening of early local sensory input processing within infragranular layers Vb. These changes had an oscillatory fingerprint within beta-band (25–36 Hz) selectively within infragranular layers Vb. To understand the laminar interaction dynamics after ECM digestion, we used time-domain conditional Granger causality (GC) measures to identify the increased drive of supragranular layers towards deeper infragranular layers. These results showed that ECM degradation altered translaminar cortical network dynamics with a stronger supragranular lead of the columnar response profile.

Why do children with autism spectrum disorder have abnormal visual perception?

“…On the one hand, it receives information from retinal ganglion cells and transmits it to the visual cortex and, on the other hand, receives feedback information from the visual cortex and regulates the electrical activity of visual neurons through neurotransmitters to achieve a balanced effect in visual information processing ( 99 , 100 ). The balance of excitatory and inhibitory transmitters plays a fundamental role in the normal function of all levels of cells in the retina and LGN and the normal transmission of visual information ( 101 , 102 ). An imbalance between excitatory/inhibitory neurotransmission has been posited as a central characteristic of the neurobiology of autism ( 103 ).…”

Novel extracellular matrix architecture on excitatory neurons revealed by HaloTag-HAPLN1

“…Notably, the ECM regulates plasticity and behavior [4][5][6][7]. Digestion of the main sugar modification on the major protein subunits of the ECM, chondroitin sulfate on chondroitin sulfate proteoglycans (CSPGs), with chondroitinase, restores juvenile levels of plasticity in a variety of paradigms, including ocular dominance plasticity, auditory learning, and fear memory consolidation [8][9][10][11]. Also, aged animals and animals in neurodegenerative models display increased memory performance after digestion of the ECM, overexpression of chondroitin-6-transferase, or ECM component knockouts [6,7,[12][13][14].…”

Tinnitus is associated with increased extracellular matrix density in the auditory cortex

“…In the present study we aim to investigate tinnitus related adaptations in the auditory cortex (AC) after an assumed chronic manifestation of the phantom percept. Based on electrophysiological recordings in animals (Engineer et al , 2011;Tziridis et al , 2015) and e.g., imaging methods or EEG recordings in humans (Haab et al , 2009;Schoisswohl et al , 2021), it is already known that tinnitus before and after chronification has different neurophysiological manifestations within the AC of mammals. While before chronification the neurophysiology of the AC seems to undergo profound changes in, e.g., tonotopy (e.g., Eggermont, 2006), the normal processing in the AC seems to be recovered after the new percept is developed, with the addition of the phantom sound activity in the affected frequency range (Ahlfet al , 2012;Langers et al , 2012).…”