The Relationship Between Synchronization Among Neuronal Populations and Their Mean Activity Levels
Abstract
In the past decade the importance of synchronized dynamics in the brain has emerged from both empirical and theoretical perspectives. Fast dynamic synchronous interactions of an oscillatory or nonoscillatory nature may constitute a form of temporal coding that underlies feature binding and perceptual synthesis. The relationship between synchronization among neuronal populations and the population firing rates addresses two important issues: the distinction between rate coding and synchronization coding models of neuronal interactions and the degree to which empirical measurements of population activity, such as those employed by neuroimaging, are sensitive to changes in synchronization. We examined the relationship between mean population activity and synchronization using biologically plausible simulations. In this article, we focus on continuous stationary dynamics. (In a companion article, Chawla (forth-coming), we address the same issue using stimulus-evoked transients.) By manipulating parameters such as extrinsic input, intrinsic noise, synaptic efficacy, density of extrinsic connections, the voltage-sensitive nature of postsynaptic mechanisms, the number of neurons, and the laminar structure within the populations, we were able to introduce variations in both mean activity and synchronization under a variety of simulated neuronal architectures. Analyses of the simulated spike trains and local field potentials showed that in nearly every domain of the model's parameter space, mean activity and synchronization were tightly coupled. This coupling appears to be mediated by an increase in synchronous gain when effective membrane time constants are lowered by increased activity. These observations show that under the assumptions implicit in our models, rate coding and synchrony coding in neural systems with reciprocal interconnections are two perspectives on the same underlying dynamic. This suggests that in the absence of specific mechanisms decoupling changes in synchronization from firing levels, indexes of brain activity that are based purely on synaptic activity (e.g., functional magnetic resonance imaging) may also be sensitive to changes in synchronous coupling.
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Synaptic gain is determined by network dynamics, like synchronization of fast oscillations in the 40-100 Hz or gamma frequencies.
“Synaptic gain is not just determined by receptor activity but also by network dynamics, like the synchronization of fast oscillations, especially in the 40–100 Hz or gamma frequencies (c.f., synchronous gain: Chawla et al., 1999).”
From The Computational Anatomy of Psychosis (2013) · cites this paper as Chawla et al., 1999
The Discussion (pp. 15–16) links network activity, synchronization, and increased synchronous gain: neurons become more responsive to coincident synaptic inputs. The paper discusses fast oscillatory dynamics, but the passages do not establish the claimed 40–100 Hz gamma range or show that synchronization determines synaptic gain generally. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe encoding of salience or precision can also be understood in terms of synchronous gain and fast oscillatory dynamics associated with binding, attention and dynamic coordination.
“As noted above, the encoding of salience or precision can also be understood in terms of synchronous gain [30] and fast (oscillatory) dynamics associated with binding, attention and dynamic coordination [4,5].”
From Cerebral hierarchies: predictive processing, precision and the pulvinar (2015) · cites this paper as [30]
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Cites
Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex
Hubel, D. H., & Wiesel, T. N. (1962) · The Journal of Physiology · doi:10.1113/jphysiol.1962.sp006837 · Cited by 13,680 · see citing works
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783 · see citing works
Gray, C. M., König, P., Engel, A. K., & Singer, W. (1989) · Nature · doi:10.1038/338334a0 · Cited by 4,183 · see citing works
Functional and effective connectivity in neuroimaging: a synthesis
Friston, K. J. (1994) · Human Brain Mapping · doi:10.1002/hbm.460020107 · Cited by 2,452 · see citing works
Self-citationStochastic resonance and the benefits of noise: from ice ages to crayfish and SQUIDs
Wiesenfeld, K., & Moss, F. (1995) · Nature · doi:10.1038/373033a0 · Cited by 1,830 · see citing works
Visuomotor integration is associated with zero time-lag synchronization among cortical areas
Roelfsema, P. R., Engel, A. K., König, P., & Singer, W. (1997) · Nature · doi:10.1038/385157a0 · Cited by 1,136 · see citing works
Frostig, R. D., Lieke, E. E., Ts’o, D. Y., & Grinvald, A. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6082 · Cited by 948 · see citing works
Interhemispheric Synchronization of Oscillatory Neuronal Responses in Cat Visual Cortex
Engel, A. K., Peter König, B., Kreiter, A. K., & Singer, W. (1991) · Science · doi:10.1126/science.252.5009.1177 · Cited by 914 · see citing works
Segev, I., & Bradford, A. (1988) · Cited by 911 · see citing works
Traub, R. D., Wong, R. K. S., Miles, R., & Michelson, H. B. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.2.635 · Cited by 715 · see citing works
A model for visual shape recognition.
Milner, P. M. (1974) · Psychological Review · doi:10.1037/h0037149 · Cited by 598 · see citing works
Primary cortical representation of sounds by the coordination of action-potential timing
deCharms, R. C., & Merzenich, M. M. (1996) · Nature · doi:10.1038/381610a0 · Cited by 541 · see citing works
Kawaguchi, Y. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02638.1995 · Cited by 533 · see citing works
Synaptic background activity influences spatiotemporal integration in single pyramidal cells.
Bernander, Ö., Douglas, R. J., Martin, K. A. C., & Koch, C. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.24.11569 · Cited by 518 · see citing works
Fries, P., Roelfsema, P. R., Engel, A. K., Peter König, B., & Singer, W. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12699 · Cited by 505 · see citing works
Condé, F., Lund, J. S., Jacobowitz, D. M., Baimbridge, K. G., & Lewis, D. A. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410109 · Cited by 500 · see citing works
Imaging Brain Plasticity: Conceptual and Methodological Issues— A Theoretical Review
Poldrack, R. A. (2000) · NeuroImage · doi:10.1006/nimg.2000.0596 · Cited by 409 · see citing works
Role of the cortical neuron: integrator or coincidence detector?
Abeles, M. (1982) · PubMed · Cited by 356 · see citing works
Polyneuronal innervation of spiny stellate neurons in cat visual cortex
Ahmed, B., Anderson, J. C., Douglas, R. J., Martin, K. A. C., & Nelson, J. C. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410105 · Cited by 338 · see citing works
Cortical activations during paced finger-tapping applying visual and auditory pacing stimuli
Jäncke, L., Loose, R., Lutz, K., Specht, K., & Shah, N. J. (2000) · Cognitive Brain Research · doi:10.1016/s0926-6410(00)00022-7 · Cited by 332 · see citing works
Relation between oscillatory activity and long-range synchronization in cat visual cortex.
Peter König, B., Engel, A. K., & Singer, W. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.1.290 · Cited by 283 · see citing works
Transients, Metastability, and Neuronal Dynamics
Friston, K. J. (1997) · NeuroImage · doi:10.1006/nimg.1997.0259 · Cited by 269 · see citing works
Self-citationBeaulieu, C., Kisvarday, Z., Somogyi, P., Cynader, M., & Cowey, A. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.4.295 · Cited by 269 · see citing works
Stern, P., Edwards, F. A., & Sakmann, B. J. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019085 · Cited by 260 · see citing works
Multiple channels and calcium dynamics
Yamada, W. M., Koch, C., & Adams, P. R. (1989) · Cited by 242 · see citing works
Beaulieu, C., & Colonnier, M. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902310206 · Cited by 239 · see citing works
Otis, T. S., Koninck, Y. D., & Módy, I. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019600 · Cited by 230 · see citing works
Reduced Synchronization in the Visual Cortex of Cats with Strabismic Amblyopia
Roelfsema, P. R., Peter König, B., Engel, A. K., Sireteanu, R., & Singer, W. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00556.x · Cited by 228 · see citing works
Lumer, E. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.3.207 · Cited by 186 · see citing works
Self-citationStructural basis of cortical synchronization. I. Three types of interhemispheric coupling
Nowak, L. G., Munk, M., Nelson, J. I., James, A. C., & Bullier, J. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.6.2379 · Cited by 169 · see citing works
Calabresi, P., Mercuri, N. B., Stefani, A., et al. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.4.651 · Cited by 163 · see citing works
Differential activation of GABAA and GABAB receptors by spontaneously released transmitter
Otis, T. S., & Módy, I. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.227 · Cited by 160 · see citing works
Dynamics of activity and connectivity in physiological neuronal networks
Aertsen, A. M. H. J., & Preissl, H. T. (1991) · MPG.PuRe (Max Planck Society) · Cited by 148 · see citing works
Neural modeling and functional brain imaging: an overview
Horwitz, B., Friston, K. J., & Taylor, J. G. (2000) · Neural Networks · doi:10.1016/s0893-6080(00)00062-9 · Cited by 146 · see citing works
Self-citationRelationship between repetitive firing and afterhyperpolarizations in human neocortical neurons
Lorenzon, N. M., & Foehring, R. C. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.2.350 · Cited by 145 · cited 1× · see citing works
“…feature of neocortical cell behavior, and it has been observed consistently that repetitive cell stimulation produces a progressive and reversible decrease of spontaneous depolarizations and a decrease in firing rate (Calabresi, Mercuri, Stefani, & Bernardi, 1990; Lorenzon & Foehring, 1992).”
BackgroundSynapse restructuring associated with the maintenance phase of hippocampal long-term potentiation
Geinisman, Y., deToledo‐Morrell, L., Morrell, F., Persina, I. S., & Beatty, M. A. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960506)368:3 · Cited by 140 · see citing works
Arthurs, O. J., Williams, E. J., Carpenter, T. A., Pickard, J. D., & Boniface, S. J. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00511-x · Cited by 135 · see citing works
Beaulieu, C., & Colonnier, M. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902170308 · Cited by 124 · see citing works
Lumer, E. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.3.228 · Cited by 103 · see citing works
Self-citationStimulus dependent intercolumnar synchronization of single unit responses in cat area 17
Freiwald, W. A., Kreiter, A. K., & Singer, W. (1995) · Neuroreport · doi:10.1097/00001756-199511270-00018 · Cited by 94 · see citing works
Sukov, W. R., & Barth, D. S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.6.2875 · Cited by 80 · see citing works
Patterns of synaptic activity in forward and feedback pathways within rat visual cortex
Domenici, L., Harding, G. W., & Burkhalter, A. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.6.2649 · Cited by 50 · see citing works
Relating Macroscopic Measures of Brain Activity to Fast, Dynamic Neuronal Interactions
Chawla, D., Lumer, E. D., & Friston, K. J. (2000) · Neural Computation · doi:10.1162/089976600300014737 · Cited by 50 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 3
- Engel, A. K., Konig, P., Kreiter, A. K., Gray, C. M., & Singer, W., (1990). Temporal coding bycoherent oscillations as a potential solution to the binding problem. in H. G. Schuster (Ed.), Nonlinear dynamics and neural networks . New York : VCH Publishers.
- Gray, C. M., Engel, A. K., Konig, P., & Singer, W. (1990). Temporal properties of synchronous oscillatory neuronal interactions in cat striate cortex, In W. G. Schuster (Ed.), Nonlinear dynamics and neural networks . New York : VCH Publishers.
- Sporns, O., Tononi, G., & Edelman, G. M. (1990). Dynamic interactions of neuronal groups and the problem of cortical integration. In W. G. Schuster (Ed.), Nonlinear dynamics and neural networks . New York : VCH Publishers.
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Friston, K. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2787 · Cited by 8,120 · see citing works
Self-citationRepetition and the brain: neural models of stimulus-specific effects
Grill-Spector, K., Henson, R., & Martin, A. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.11.006 · Cited by 2,256 · see citing works
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Deco, G., Jirsa, V. K., & McIntosh, A. R. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn2961 · Cited by 1,798 · see citing works
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Adams, R. A., Stephan, K. E., Brown, H. R., Frith, C. D., & Friston, K. J. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00047 · Cited by 850 · see citing works
“Synaptic gain is not just determined by receptor activity but also by network dynamics, like the synchronization of fast oscillations, especially in the 40–100 Hz or gamma frequencies (c.f., synchronous gain: Chawla et al., 1999).”
BackgroundMethodSelf-citationCerebral hierarchies: predictive processing, precision and the pulvinar
Kanai, R., Komura, Y., Shipp, S., & Friston, K. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0169 · Cited by 432 · see citing works
Self-citationHillebrand, A., Barnes, G. R., Bosboom, J. L., Berendse, H. W., & Stam, C. J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.11.005 · Cited by 416 · see citing works
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Self-citation
- Authors
- Chawla, D., Lumer, E. D., & Friston, K. J.
- Affiliations
- UCL Queen Square Institute of Neurology (GB)
- ORCID
- Friston, K. J.
- Venue
- Neural Computation
- Publisher
- MIT Press - Journals
- Published
- 1999-08-01
- Volume
- 11
- Issue
- 6
- Pages
- 1389-1411
- ISSN
- 0899-7667 (ISSN-L)
- 1530-888X
- OpenAlex
- W2147782383
- Cited by
- 125
- References
- 43
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 3 · 2020: 1 · 2019: 5 · 2018: 3 · 2017: 7 · 2016: 10 · 2015: 6 · 2014: 10 · 2013: 1 · 2012: 5
- FWCI
- 3.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neural Computation (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Physical Sciences › Computer Science › Computer Networks and Communications › Nonlinear Dynamics and Pattern Formation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- neuronal synchronization, population firing rate, rate coding, neural oscillations, local field potentials, spike trains, membrane time constant, intrinsic noise, synaptic efficacy, laminar structure, feature binding, temporal coding
- MeSH terms
- Brain, Computer Simulation, Models, Neurological, Neurons, Time Factors, Neural Networks, Computer
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