Rapid inhibitory circuit plasticity as a homeostatic mechanism in cerebral cortex

NIH RePORTER · NIH · R01 · $344,055 · view on reporter.nih.gov ↗

Abstract

Experience robustly regulates the development and function of GABAergic inhibitory circuits in cerebral cortex, but the purpose of this inhibitory circuit plasticity is unclear. Recent findings in rodent somatosensory (S1) and visual cortex suggest that inhibitory plasticity may contribute to homeostatic stabilization of firing rate in cortical networks. We recently discovered that during competitive map plasticity in S1, sensory deprivation weakens parvalbumin (PV) inhibitory circuits very rapidly (< 1 day). This is faster than classical homeostatic mechanisms like synaptic scaling, and promotes firing rate stability in the S1 network. We propose that PV circuit plasticity functions as a rapid, bidirectional homeostat, operating on the time scale of hours, and that its role is to stabilize cortical firing rate. We propose that it accomplishes this by adaptively altering PV circuit gain and excitation-inhibition (E-I) ratio in local pyramidal cells as a function of the recent history of network activity. This rapid inhibitory plasticity may be a major contributor to controlling firing rate in cerebral cortex. Here, we test this hypothesis, using L2/3 of mouse whisker S1 cortex as a model system. In Aim 1, we use slice physiology and layer-specific optogenetics to measure how whisker deprivation alters the gain of L4-L2/3 feedforward and L2/3-L2/3 recurrent inhibitory circuits, and quantify the dynamics of this plasticity. We test whether direct chemogenetic modulation of pyramidal cell firing rate induces inhibitory circuit plasticity, whether this is bidirectional, and whether it is general across cortical areas. In Aim 2, we use dual whole-cell recording to identify the specific synaptic and cellular changes that mediate rapid inhibitory plasticity in PV and Somatostatin (SOM) circuits. In Aim 3, we use 2-photon calcium imaging and chronic extracellular unit recording to characterize firing rate homeostasis in L2/3, determine its magnitude and dynamics across age, and measure its relationship to inhibitory circuit plasticity. Breakdown of inhibitory homeostasis could contribute to circuit dysfunction in autism, schizophrenia, and other disorders. In Aim 4, we test this hypothesis by asking whether inhibition or inhibitory homeostasis is disrupted in cortex in several transgenic mouse models of autism. Preliminary data show that excitation-inhibition ratio is disrupted in common across four genetically unrelated mouse models. This provides key support for the long-held E-I ratio model of autism. Overall, this project will reveal whether inhibitory circuit plasticity is an important mechanism for rapid homeostasis of cortical firing rate, and whether its disruption may contribute to neurological disease.

Key facts

NIH application ID
10063590
Project number
5R01NS105333-04
Recipient
UNIVERSITY OF CALIFORNIA BERKELEY
Principal Investigator
Daniel Feldman
Activity code
R01
Funding institute
NIH
Fiscal year
2021
Award amount
$344,055
Award type
5
Project period
2017-12-15 → 2022-11-30