Strong Preference for Autaptic Self-connectivity of Neocortical PV Interneurons Facilitates Their Tuning to γ-oscillations

Overview

Journal PLoS Biol

Specialty Biology

Date 2019 Sep 5

PMID 31483783

Citations 23

Authors

Charlotte Deleuze

Gary S Bhumbra

Antonio Pazienti

Joana Lourenco

Caroline Mailhes

Andrea Aguirre

Marco Beato

Alberto Bacci

Affiliations

Soon will be listed here.

Abstract

Parvalbumin (PV)-positive interneurons modulate cortical activity through highly specialized connectivity patterns onto excitatory pyramidal neurons (PNs) and other inhibitory cells. PV cells are autoconnected through powerful autapses, but the contribution of this form of fast disinhibition to cortical function is unknown. We found that autaptic transmission represents the most powerful inhibitory input of PV cells in neocortical layer V. Autaptic strength was greater than synaptic strength onto PNs as a result of a larger quantal size, whereas autaptic and heterosynaptic PV-PV synapses differed in the number of release sites. Overall, single-axon autaptic transmission contributed to approximately 40% of the global inhibition (mostly perisomatic) that PV interneurons received. The strength of autaptic transmission modulated the coupling of PV-cell firing with optogenetically induced γ-oscillations, preventing high-frequency bursts of spikes. Autaptic self-inhibition represents an exceptionally large and fast disinhibitory mechanism, favoring synchronization of PV-cell firing during cognitive-relevant cortical network activity.

Citing Articles

Corticolimbic circuitry as a druggable target in schizophrenia spectrum disorders: a narrative review.

Gee A, Dazzan P, Grace A, Modinos G Transl Psychiatry. 2025; 15(1):21.

PMID: 39856031 PMC: 11760974. DOI: 10.1038/s41398-024-03221-2.

Oxidative Stress-mediated Loss of Hippocampal Parvalbumin Interneurons Contributes to Memory Precision Decline After Acute Sleep Deprivation.

Gao Y, Liu K, Wu X, Shi C, He Q, Wu H Mol Neurobiol. 2024; .

PMID: 39546120 DOI: 10.1007/s12035-024-04628-0.

Transition to seizure in focal epilepsy: From SEEG phenomenology to underlying mechanisms.

Kayabas M, Koksal Ersoz E, Yochum M, Bartolomei F, Benquet P, Wendling F Epilepsia. 2024; 65(12):3619-3630.

PMID: 39474858 PMC: 11647430. DOI: 10.1111/epi.18173.

The Pathophysiological Underpinnings of Gamma-Band Alterations in Psychiatric Disorders.

Palmisano A, Pandit S, Smeralda C, Demchenko I, Rossi S, Battelli L Life (Basel). 2024; 14(5).

PMID: 38792599 PMC: 11122172. DOI: 10.3390/life14050578.

Physiological features of parvalbumin-expressing GABAergic interneurons contributing to high-frequency oscillations in the cerebral cortex.

Milicevic K, Barbeau B, Lovic D, Patel A, Ivanova V, Antic S Curr Res Neurobiol. 2024; 6:100121.

PMID: 38616956 PMC: 11015061. DOI: 10.1016/j.crneur.2023.100121.

References

Van Der Loos H, GLASER E . Autapses in neocortex cerebri: synapses between a pyramidal cell's axon and its own dendrites. Brain Res. 1972; 48:355-60. DOI: 10.1016/0006-8993(72)90189-8. View

Deleuze C, Pazienti A, Bacci A . Autaptic self-inhibition of cortical GABAergic neurons: synaptic narcissism or useful introspection?. Curr Opin Neurobiol. 2014; 26:64-71. DOI: 10.1016/j.conb.2013.12.009. View

Isaacson J, Scanziani M . How inhibition shapes cortical activity. Neuron. 2011; 72(2):231-43. PMC: 3236361. DOI: 10.1016/j.neuron.2011.09.027. View

Freund T, Katona I . Perisomatic inhibition. Neuron. 2007; 56(1):33-42. DOI: 10.1016/j.neuron.2007.09.012. View

Kepecs A, Fishell G . Interneuron cell types are fit to function. Nature. 2014; 505(7483):318-26. PMC: 4349583. DOI: 10.1038/nature12983. View

Shao Y, Isett B, Miyashita T, Chung J, Pourzia O, Gasperini R . Plasticity of recurrent l2/3 inhibition and gamma oscillations by whisker experience. Neuron. 2013; 80(1):210-22. PMC: 3792397. DOI: 10.1016/j.neuron.2013.07.026. View

Moore N, Bhumbra G, Foster J, Beato M . Synaptic Connectivity between Renshaw Cells and Motoneurons in the Recurrent Inhibitory Circuit of the Spinal Cord. J Neurosci. 2015; 35(40):13673-86. PMC: 4595620. DOI: 10.1523/JNEUROSCI.2541-15.2015. View

Adesnik H, Scanziani M . Lateral competition for cortical space by layer-specific horizontal circuits. Nature. 2010; 464(7292):1155-60. PMC: 2908490. DOI: 10.1038/nature08935. View

Martina M, Royer S, Pare D . Cell-type-specific GABA responses and chloride homeostasis in the cortex and amygdala. J Neurophysiol. 2001; 86(6):2887-95. DOI: 10.1152/jn.2001.86.6.2887. View

10.

Bhumbra G, Beato M . Reliable evaluation of the quantal determinants of synaptic efficacy using Bayesian analysis. J Neurophysiol. 2012; 109(2):603-20. PMC: 3574980. DOI: 10.1152/jn.00528.2012. View

11.

Jiang M, Yang M, Yin L, Zhang X, Shu Y . Developmental reduction of asynchronous GABA release from neocortical fast-spiking neurons. Cereb Cortex. 2013; 25(1):258-70. DOI: 10.1093/cercor/bht236. View

12.

Bartos M, Vida I, Jonas P . Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci. 2006; 8(1):45-56. DOI: 10.1038/nrn2044. View

13.

Harris K, Shepherd G . The neocortical circuit: themes and variations. Nat Neurosci. 2015; 18(2):170-81. PMC: 4889215. DOI: 10.1038/nn.3917. View

14.

Pawelzik H, Hughes D, Thomson A . Modulation of inhibitory autapses and synapses on rat CA1 interneurones by GABA(A) receptor ligands. J Physiol. 2003; 546(Pt 3):701-16. PMC: 2342589. DOI: 10.1113/jphysiol.2002.035121. View

15.

Vida I, Bartos M, Jonas P . Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron. 2006; 49(1):107-17. DOI: 10.1016/j.neuron.2005.11.036. View

16.

Jiang M, Zhu J, Liu Y, Yang M, Tian C, Jiang S . Enhancement of asynchronous release from fast-spiking interneuron in human and rat epileptic neocortex. PLoS Biol. 2012; 10(5):e1001324. PMC: 3348166. DOI: 10.1371/journal.pbio.1001324. View

17.

Sah P, Faber E . Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol. 2002; 66(5):345-53. DOI: 10.1016/s0301-0082(02)00004-7. View

18.

Fritschy J, Panzanelli P, Tyagarajan S . Molecular and functional heterogeneity of GABAergic synapses. Cell Mol Life Sci. 2012; 69(15):2485-99. PMC: 11115047. DOI: 10.1007/s00018-012-0926-4. View

19.

Kamigaki T, Dan Y . Delay activity of specific prefrontal interneuron subtypes modulates memory-guided behavior. Nat Neurosci. 2017; 20(6):854-863. PMC: 5554301. DOI: 10.1038/nn.4554. View

20.

Tamas G, Buhl E, Somogyi P . Massive autaptic self-innervation of GABAergic neurons in cat visual cortex. J Neurosci. 1997; 17(16):6352-64. PMC: 6568358. View