Synaptic Effects on the Intermittent Synchronization of Gamma Rhythms

Overview

Journal Cogn Neurodyn

Publisher Springer

Specialty Neurology

Date 2024 Dec 23

PMID 39712142

Authors

Quynh-Anh Nguyen

Leonid L Rubchinsky

Affiliations

Soon will be listed here.

Abstract

Synchronization of neural activity in the gamma frequency band is associated with various cognitive phenomena. Abnormalities of gamma synchronization may underlie symptoms of several neurological and psychiatric disorders such as schizophrenia and autism spectrum disorder. Properties of neural oscillations in the gamma band depend critically on the synaptic properties of the underlying circuits. This study explores how synaptic properties in pyramidal-interneuronal circuits affect not only the average synchronization strength but also the fine temporal patterning of neural synchrony. If two signals show only moderate synchrony strength, it may be possible to consider these dynamics as alternating between synchronized and desynchronized states. We use a model of connected circuits that produces pyramidal-interneuronal gamma oscillations to explore the temporal patterning of synchronized and desynchronized intervals. Changes in synaptic strength may alter the temporal patterning of synchronized dynamics (even if the average synchrony strength is not changed). Larger values of local synaptic connections promote longer desynchronization durations, while larger values of long-range synaptic connections promote shorter desynchronization durations. Furthermore, we show that circuits with different temporal patterning of synchronization may have different sensitivity to synaptic input. Thus, the alterations of synaptic strength may mediate physiological properties of neural circuits not only through change in the average synchrony level of gamma oscillations, but also through change in how synchrony is patterned in time over very short time scales.

References

Zirkle J, Rubchinsky L . Spike-Timing Dependent Plasticity Effect on the Temporal Patterning of Neural Synchronization. Front Comput Neurosci. 2020; 14:52. PMC: 7303326. DOI: 10.3389/fncom.2020.00052. View

Uhlhaas P, Singer W . Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci. 2010; 11(2):100-13. DOI: 10.1038/nrn2774. View

Ahn S, Rubchinsky L, Lapish C . Dynamical reorganization of synchronous activity patterns in prefrontal cortex-hippocampus networks during behavioral sensitization. Cereb Cortex. 2013; 24(10):2553-61. DOI: 10.1093/cercor/bht110. View

Borgers C, Talei Franzesi G, LeBeau F, Boyden E, Kopell N . Minimal size of cell assemblies coordinated by gamma oscillations. PLoS Comput Biol. 2012; 8(2):e1002362. PMC: 3276541. DOI: 10.1371/journal.pcbi.1002362. View

Vierling-Claassen D, Siekmeier P, Stufflebeam S, Kopell N . Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment. J Neurophysiol. 2008; 99(5):2656-71. PMC: 2679675. DOI: 10.1152/jn.00870.2007. View

Pittman-Polletta B, Kocsis B, Vijayan S, Whittington M, Kopell N . Brain rhythms connect impaired inhibition to altered cognition in schizophrenia. Biol Psychiatry. 2015; 77(12):1020-30. PMC: 4444389. DOI: 10.1016/j.biopsych.2015.02.005. View

Ermentrout G, Kopell N . Fine structure of neural spiking and synchronization in the presence of conduction delays. Proc Natl Acad Sci U S A. 1998; 95(3):1259-64. PMC: 18738. DOI: 10.1073/pnas.95.3.1259. View

Ratnadurai-Giridharan S, Zauber S, Worth R, Witt T, Ahn S, Rubchinsky L . Temporal patterning of neural synchrony in the basal ganglia in Parkinson's disease. Clin Neurophysiol. 2015; 127(2):1743-1745. DOI: 10.1016/j.clinph.2015.09.005. View

Dos Santos Lima G, Targa A, de Freitas Cavalcante S, Rodrigues L, Fontenele-Araujo J, Torterolo P . Disruption of neocortical synchronisation during slow-wave sleep in the rotenone model of Parkinson's disease. J Sleep Res. 2020; 30(3):e13170. DOI: 10.1111/jsr.13170. View

10.

Uhlhaas P, Singer W . Oscillations and neuronal dynamics in schizophrenia: the search for basic symptoms and translational opportunities. Biol Psychiatry. 2015; 77(12):1001-9. DOI: 10.1016/j.biopsych.2014.11.019. View

11.

Fell J, Axmacher N . The role of phase synchronization in memory processes. Nat Rev Neurosci. 2011; 12(2):105-18. DOI: 10.1038/nrn2979. View

12.

Somers D, Kopell N . Rapid synchronization through fast threshold modulation. Biol Cybern. 1993; 68(5):393-407. DOI: 10.1007/BF00198772. View

13.

Bansal K, Garcia J, Tompson S, Verstynen T, Vettel J, Muldoon S . Cognitive chimera states in human brain networks. Sci Adv. 2019; 5(4):eaau8535. PMC: 6447382. DOI: 10.1126/sciadv.aau8535. View

14.

Park C, Worth R, Rubchinsky L . Fine temporal structure of beta oscillations synchronization in subthalamic nucleus in Parkinson's disease. J Neurophysiol. 2010; 103(5):2707-16. PMC: 2867579. DOI: 10.1152/jn.00724.2009. View

15.

Lisman J . Excitation, inhibition, local oscillations, or large-scale loops: what causes the symptoms of schizophrenia?. Curr Opin Neurobiol. 2011; 22(3):537-44. PMC: 3302967. DOI: 10.1016/j.conb.2011.10.018. View

16.

Ahn S, Rubchinsky L . Short desynchronization episodes prevail in synchronous dynamics of human brain rhythms. Chaos. 2013; 23(1):013138. PMC: 3606233. DOI: 10.1063/1.4794793. View

17.

Zirkle J, Rubchinsky L . Noise effect on the temporal patterns of neural synchrony. Neural Netw. 2021; 141:30-39. DOI: 10.1016/j.neunet.2021.03.032. View

18.

Wang X, Buzsaki G . Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci. 1996; 16(20):6402-13. PMC: 6578902. View

19.

Sahara S, Yanagawa Y, OLeary D, Stevens C . The fraction of cortical GABAergic neurons is constant from near the start of cortical neurogenesis to adulthood. J Neurosci. 2012; 32(14):4755-61. PMC: 3325497. DOI: 10.1523/JNEUROSCI.6412-11.2012. View

20.

Salkoff D, Zagha E, Yuzgec O, McCormick D . Synaptic Mechanisms of Tight Spike Synchrony at Gamma Frequency in Cerebral Cortex. J Neurosci. 2015; 35(28):10236-51. PMC: 4502264. DOI: 10.1523/JNEUROSCI.0828-15.2015. View