Correlation between neural spike trains increases with firing rate
Abstract
Populations of neurons in the retina, olfactory system, visual and somatosensory thalamus, and several cortical regions show temporal correlation between the discharge times of their action potentials (spike trains). Correlated firing has been linked to stimulus encoding, attention, stimulus discrimination, and motor behaviour. Nevertheless, the mechanisms underlying correlated spiking are poorly understood, and its coding implications are still debated. It is not clear, for instance, whether correlations between the discharges of two neurons are determined solely by the correlation between their afferent currents, or whether they also depend on the mean and variance of the input. We addressed this question by computing the spike train correlation coefficient of unconnected pairs of in vitro cortical neurons receiving correlated inputs. Notably, even when the input correlation remained fixed, the spike train output correlation increased with the firing rate, but was largely independent of spike train variability. With a combination of analytical techniques and numerical simulations using 'integrate-and-fire' neuron models we show that this relationship between output correlation and firing rate is robust to input heterogeneities. Finally, this overlooked relationship is replicated by a standard threshold-linear model, demonstrating the universality of the result. This connection between the rate and correlation of spiking activity links two fundamental features of the neural code.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The degree to which the synaptic input underlying Vm fluctuations is temporally correlated can vary with overall drive to a network or with firing rates and is regulated by behavioural state transitions during wakefulness.
“The degree to which the synaptic input underlying Vm fluctuations is temporally correlated can vary with overall drive to a network or with firing rates70 and is regulated by behavioural state transitions during wakefulness29,71–74.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [70]
Cites
Shadlen, M. N., & Newsome, W. T. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-10-03870.1998 · Cited by 2,178 · see citing works
Neural correlations, population coding and computation
Averbeck, B. B., Latham, P. E., & Pouget, A. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1888 · Cited by 1,743 · see citing works
Weak pairwise correlations imply strongly correlated network states in a neural population
Schneidman, E., Berry, M. J., Segev, R., & Bialek, W. (2006) · Nature · doi:10.1038/nature04701 · Cited by 1,701 · see citing works
Tsodyks, M. V., & Markram, H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.2.719 · Cited by 1,607 · see citing works
Abeles, M. (1991) · Cambridge University Press eBooks · doi:10.1017/cbo9780511574566 · Cited by 1,380 · see citing works
Correlated neuronal activity and the flow of neural information
Salinas, E., & Sejnowski, T. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35086012 · Cited by 1,333 · see citing works
Correlated neuronal discharge rate and its implications for psychophysical performance
Zohary, E., Shadlen, M. N., & Newsome, W. T. (1994) · Nature · doi:10.1038/370140a0 · Cited by 1,237 · see citing works
The high-conductance state of neocortical neurons in vivo
Alain Destexhe, A., Rudolph, M., & Paré, D. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1198 · Cited by 1,077 · see citing works
Impaired odour discrimination on desynchronization of odour-encoding neural assemblies
Stopfer, M., Bhagavan, S., Smith, B. H., & Laurent, G. (1997) · Nature · doi:10.1038/36335 · Cited by 927 · see citing works
Computational subunits in thin dendrites of pyramidal cells
Polsky, A., Mel, B. W., & Schiller, J. (2004) · Nature Neuroscience · doi:10.1038/nn1253 · Cited by 817 · see citing works
Dynamics of neuronal interactions in monkey cortex in relation to behavioural events
Vaadia, E., Haalman, I., Abeles, M., Bergman, H., Prut, Y., Slovin, H., & Aertsen, A. (1995) · Nature · doi:10.1038/373515a0 · Cited by 802 · see citing works
Attention modulates synchronized neuronal firing in primate somatosensory cortex
Steinmetz, P. N., Roy, A., Fitzgerald, P. J., Hsiao, S. S., Johnson, K. O., & Niebur, E. (2000) · Nature · doi:10.1038/35004588 · Cited by 725 · see citing works
Cortex is driven by weak but synchronously active thalamocortical synapses
Bruno, R. M., & Sakmann, B. (2006) · Science · doi:10.1126/science.1124593 · Cited by 714 · 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
Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque
Kohn, A., & Smith, M. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5106-04.2005 · Cited by 521 · see citing works
Correlated Firing in Macaque Visual Area MT: Time Scales and Relationship to Behavior
Bair, W., Zohary, E., & Newsome, W. T. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01676.2001 · Cited by 515 · see citing works
Precisely correlated firing in cells of the lateral geniculate nucleus
Alonso, J., Usrey, W. M., & Reid, R. C. (1996) · Nature · doi:10.1038/383815a0 · Cited by 514 · see citing works
The Structure of Multi-Neuron Firing Patterns in Primate Retina
Shlens, J., Field, G. D., Gauthier, J. L., Grivich, M. I., Petrusca, D., Sher, A., Litke, A. M., & Chichilnisky, E. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1282-06.2006 · Cited by 471 · see citing works
Synchronous Membrane Potential Fluctuations in Neurons of the Cat Visual Cortex
Lampl, I., Reichova, I., & Ferster, D. (1999) · Neuron · doi:10.1016/s0896-6273(00)81096-x · Cited by 434 · see citing works
Diffusion Processes and Related Topics in Biology
Ricciardi, L. M. (1977) · Lecture notes in biomathematics · doi:10.1007/978-3-642-93059-1 · Cited by 407 · see citing works
Top-down Dendritic Input Increases the Gain of Layer 5 Pyramidal Neurons
Larkum, M. E. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh065 · Cited by 366 · see citing works
Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro
Reyes, A. D. (2003) · Nature Neuroscience · doi:10.1038/nn1056 · Cited by 296 · see citing works
Self-citationCorrelated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells
Mastronarde, D. N. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.49.2.303 · Cited by 260 · see citing works
Correlation-Induced Synchronization of Oscillations in Olfactory Bulb Neurons
Galán, R. F., Fourcaud‐Trocmé, N., Ermentrout, B., & Urban, N. N. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4605-05.2006 · Cited by 198 · see citing works
Lau, D., de Miera, E. V., Contreras, D., Ozaita, A., Harvey, M., Chow, A., Noebels, J. L., Paylor, R. E., Morgan, J. I., Leonard, C. S., et al. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09071.2000 · Cited by 175 · see citing works
Theory of oscillatory firing induced by spatially correlated noise and delayed inhibitory feedback
Lindner, B., Doiron, B., & Longtin, A. (2005) · Physical Review E · doi:10.1103/physreve.72.061919 · Cited by 175 · see citing works
Self-citationBinder, M. D., & Powers, R. K. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.5.2266 · Cited by 78 · see citing works
Stochastic synchronization in finite size spiking networks
Doiron, B., Rinzel, J., & Reyes, A. D. (2006) · Physical Review E · doi:10.1103/physreve.74.030903 · Cited by 39 · see citing works
Self-citationEstimating Membrane Voltage Correlations From Extracellular Spike Trains
Dorn, J. D., & Ringach, D. L. (2003) · Journal of Neurophysiology · doi:10.1152/jn.000889.2002 · Cited by 35 · see citing works
Influence of membrane properties on spike synchronization in neurons: theory and experiments
Svirskis, G., & Hounsgaard, J. (2003) · Network Computation in Neural Systems · doi:10.1088/0954-898x_14_4_307 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Ray, S., Crone, N. E., Niebur, E., Franaszczuk, P. J., & Hsiao, S. S. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2848-08.2008 · Cited by 722 · see citing works
Decorrelated neuronal firing in cortical microcircuits
Ecker, A. S., Berens, P., Keliris, G. A., Bethge, M., Logothetis, N. K., & Tolias, A. S. (2010) · Science · doi:10.1126/science.1179867 · Cited by 640 · see citing works
Partitioning neuronal variability
Goris, R. L. T., Movshon, J. A., & Simoncelli, E. P. (2014) · Nature Neuroscience · doi:10.1038/nn.3711 · Cited by 528 · see citing works
Mechanisms underlying gain modulation in the cortex
Ferguson, K. A., & Cardin, J. A. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0253-y · Cited by 327 · see citing works
An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity
Chen, N., Sugihara, H., & Sur, M. (2015) · Nature Neuroscience · doi:10.1038/nn.4002 · Cited by 210 · see citing works
Attention stabilizes the shared gain of V4 populations
Rabinowitz, N. C., Goris, R. L., Cohen, M., & Simoncelli, E. P. (2015) · eLife · doi:10.7554/elife.08998 · Cited by 194 · see citing works
Hug, F., Avrillon, S., Ibáñez, J., & Farina, D. (2023) · The Journal of Physiology · doi:10.1113/jp283698 · Cited by 154 · see citing works
Shea-Brown, E., Josić, K., de la Rocha, J., & Doiron, B. (2008) · Physical Review Letters · doi:10.1103/physrevlett.100.108102 · Cited by 131 · see citing works
Self-citationLaminar dependence of neuronal correlations in visual cortex
Smith, M. A., Jia, X., Zandvakili, A., & Kohn, A. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00846.2012 · Cited by 129 · see citing works
Homeostatic mechanisms regulate distinct aspects of cortical circuit dynamics
Wu, Y. K., Hengen, K. B., Turrigiano, G. G., & Gjorgjieva, J. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1918368117 · Cited by 86 · see citing works
On the Structure of Neuronal Population Activity under Fluctuations in Attentional State
Ecker, A. S., Denfield, G. H., Bethge, M., & Tolias, A. S. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2044-15.2016 · Cited by 88 · see citing works
Joshi, S., & Gold, J. I. (2022) · eLife · doi:10.7554/elife.63490 · Cited by 71 · see citing works
Single Neuron Firing Properties Impact Correlation-Based Population Coding
Hong, S., Ratté, S., Prescott, S. A., & De Schutter, E. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3735-11.2012 · Cited by 72 · see citing works
Balanced Synaptic Input Shapes the Correlation between Neural Spike Trains
Litwin-Kumar, A., Oswald, A.-M. M., Urban, N. N., & Doiron, B. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002305 · Cited by 46 · see citing works
Self-citationRepresentation of Dynamical Stimuli in Populations of Threshold Neurons
Tchumatchenko, T., & Wolf, F. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002239 · Cited by 21 · see citing works
Membrane potential and spike train statistics depend distinctly on input statistics
Rosenbaum, R., & Josić, K. (2011) · Physical Review E · doi:10.1103/physreve.84.051902 · Cited by 5 · see citing works
Self-citationA survey on neuro-mimetic deep learning via predictive coding
Salvatori, T., Mali, A., Buckley, C. L., Lukasiewicz, T., Rao, R. P. N., Friston, K., & Ororbia, A. (2026) · Neural Networks · doi:10.1016/j.neunet.2025.108161 · Cited by 2 · see citing works
- Authors
- de la Rocha, J., Doiron, B., Shea-Brown, E., Josić, K., & Reyes, A.
- Affiliations
- University of Pittsburgh (US)
- New York University (US)
- Corresponding author
- Doiron, Brent
- Venue
- Nature
- Published
- 2007-08-16
- Volume
- 448
- Issue
- 7155
- Pages
- 802-806
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2131423842
- Cited by
- 644
- References
- 30
- Citations by year
- 2026: 16 · 2025: 34 · 2024: 25 · 2023: 21 · 2022: 25 · 2021: 23 · 2020: 26 · 2019: 28 · 2018: 18 · 2017: 43 · 2016: 47 · 2015: 54 · 2014: 52 · 2013: 47 · 2012: 42
- FWCI
- 17.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › stochastic dynamics and bifurcation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- spike train correlations, firing rate, neural coding, correlated firing, integrate-and-fire neuron model, spike train variability, population coding
- MeSH terms
- Action Potentials, Animals, Auditory Cortex, Models, Neurological, Neurons, Somatosensory Cortex, Time Factors, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review