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A general method to generate artificial spike train populations matching recorded neurons

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Abstract

We developed a general method to generate populations of artificial spike trains (ASTs) that match the statistics of recorded neurons. The method is based on computing a Gaussian local rate function of the recorded spike trains, which results in rate templates from which ASTs are drawn as gamma distributed processes with a refractory period. Multiple instances of spike trains can be sampled from the same rate templates. Importantly, we can manipulate rate-covariances between spike trains by performing simple algorithmic transformations on the rate templates, such as filtering or amplifying specific frequency bands, and adding behavior related rate modulations. The method was examined for accuracy and limitations using surrogate data such as sine wave rate templates, and was then verified for recorded spike trains from cerebellum and cerebral cortex. We found that ASTs generated with this method can closely follow the firing rate and local as well as global spike time variance and power spectrum. The method is primarily intended to generate well-controlled spike train populations as inputs for dynamic clamp studies or biophysically realistic multicompartmental models. Such inputs are essential to study detailed properties of synaptic integration with well-controlled input patterns that mimic the in vivo situation while allowing manipulation of input rate covariances at different time scales.

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Abbreviations

aGLR:

Adaptive Gaussian Local Rate template

saGLR:

Rate scaled adaptive Local Rate template

AST:

Artificial Spike Train

CV:

Coefficient of Variation

u:

u-fold increase of aGLR rate within single computed ISI (real valued number)

ISI:

Inter-spike Interval

LV:

Local Variation

MF:

Mossy fiber

MT:

Middle temporal area pyramidal neuron

PC:

Purkinje cell

PETH:

Peri Event Time Histogram

SF:

Shift Fraction

sGLR:

Slow Gaussian Local Rate template

References

  • Abbasi, S., Hudson, A. E., Maran, S. K., Cao, Y., Abbasi, A., Heck, D. H., & Jaeger, D. (2017). Robust transmission of rate coding in the inhibitory Purkinje cell to cerebellar nuclei pathway in awake mice. PLoS Computational Biology, 13.

  • Abeles, M. (1983). The quantification and graphic display of correlations among three spike trains. IEEE Transactions on Biomedical Engineering, BME-30, 235–239.

    Article  Google Scholar 

  • Aertsen, A., Diesmann, M., & Gewaltig, M. O. (1996). Propagation of synchronous spiking activity in feedforward neural networks. Journal of Physiology (Paris), 90, 243–247.

    Article  CAS  Google Scholar 

  • Allers, K. A., Ruskin, D. N., Bergstrom, D. A., Freeman, L. E., Ghazi, L. J., Tierney, P. L., & Walters, J. R. (2002). Multisecond periodicities in basal ganglia firing rates correlate with theta bursts in transcortical and hippocampal EEG. J.Neurophysiol., 87, 1118–1122.

    Article  PubMed  Google Scholar 

  • Bobier, B., Stewart, T. C., & Eliasmith, C. (2014). A unifying mechanistic model of selective attention in spiking neurons. PLoS Computational Biology, 10.

  • Brette, R. (2009). Generation of correlated spike trains. Neural Computation, 21, 188–215.

    Article  PubMed  Google Scholar 

  • Brown, J., Pan, W. X., & Dudman, J. T. (2014). The inhibitory microcircuit of the substantia nigra provides feedback gain control of the basal ganglia output. Elife, 3, e02397.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao, Y., Liu, Y., Jaeger, D., & Heck, D. H. (2017). Cerebellar Purkinje cells generate highly correlated spontaneous slow-rate fluctuations. Frontiers in Neural Circuits, 11, 67.

  • Cui, Y., Liu, L. D., Khawaja, F. A., Pack, C. C., & Butts, D. A. (2013). Diverse suppressive influences in area MT and selectivity to complex motion features. The Journal of Neuroscience, 33, 16715–16728.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diesmann, M., Gewaltig, M. O., & Aertsen, A. (1999). Stable propagation of synchronous spiking in cortical neural networks. Nature, 402, 529–533.

    Article  CAS  PubMed  Google Scholar 

  • Edgerton, J. R., Hanson, J. E., Gunay, C., & Jaeger, D. (2010). Dendritic sodium channels regulate network integration in Globus Pallidus neurons: A modeling study. The Journal of Neuroscience, 30, 15146–15159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eliasmith, C., Stewart, T. C., Choo, X., Bekolay, T., DeWolf, T., Tang, Y., & Rasmussen, D. (2012). A large-scale model of the functioning brain. Science, 338, 1202–1205.

    Article  CAS  PubMed  Google Scholar 

  • Gerstein, G. L., & Perkel, D. H. (1969). Simultaneously recorded trains of action potentials: Analysis and functional interpretation. Science, 164, 828–830.

    Article  CAS  PubMed  Google Scholar 

  • Gerstein, G. L., & Perkel, D. H. (1972). Mutual temporal relationships among neuronal spike trains statistical techniques for display and analysis. Biophys.J., 12, 453–473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grammont, F., & Riehle, A. (1999). Precise spike synchronization in monkey motor cortex involved in preparation for movement. Experimental Brain Research, 128, 118–122.

    Article  CAS  PubMed  Google Scholar 

  • Gutnisky, D. A., & Josic, K. (2010). Generation of spatiotemporally correlated spike trains and local field potentials using a multivariate autoregressive process. Journal of Neurophysiology, 103, 2912–2930.

    Article  PubMed  Google Scholar 

  • Hutcheon, B., & Yarom, Y. (2000). Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends in Neurosciences, 23, 216–222.

    Article  CAS  PubMed  Google Scholar 

  • Izhikevich, E. M. (2006). Polychronization: Computation with spikes. Neural Computation, 18, 245–282.

    Article  PubMed  Google Scholar 

  • Izhikevich, E. M., & Hoppensteadt, F. C. (2009). Polychronous wavefront computations. International Journal of Bifurcation and Chaos, 19, 1733–1739.

    Article  Google Scholar 

  • Jaeger, D., & Bower, J. M. (1999). Synaptic control of spiking in cerebellar Purkinje cells: Dynamic current clamp based on model conductances. The Journal of Neuroscience, 19, 6090–6101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaeger, D., DeSchutter, E., & Bower, J. M. (1997). The role of synaptic and voltage-gated currents in the control of Purkinje cell spiking: A modeling study. The Journal of Neuroscience, 17, 91–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jun, J. J., Steinmetz, N. A., Siegle, J. H., Denman, D. J., Bauza, M., Barbarits, B., Lee, A. K., Anastassiou, C. A., Andrei, A., Aydin, C., et al. (2017). Fully integrated silicon probes for high-density recording of neural activity. Nature, 551, 232–236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krumin, M., & Shoham, S. (2009). Generation of spike trains with controlled auto- and cross-correlation functions. Neural Computation, 21, 1642–1664.

    Article  PubMed  Google Scholar 

  • Lang, E. J., Sugihara, I., Welsh, J. P., & Llinas, R. (1999). Patterns of spontaneous Purkinje cell complex spike activity in the awake rat. The Journal of Neuroscience, 19, 2728–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ledergerber, D., & Larkum, M. E. (2010). Properties of layer 6 pyramidal neuron apical dendrites. The Journal of Neuroscience, 30, 13031–13044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis, T. J., & Rinzel, J. (2003). Dynamics of spiking neurons connected by both inhibitory and electrical coupling. Journal of Computational Neuroscience, 14, 283–309.

    Article  PubMed  Google Scholar 

  • Lin, R. J., & Jaeger, D. (2011). Using computer simulations to determine the limitations of dynamic clamp stimuli applied at the soma in mimicking distributed conductance sources. Journal of Neurophysiology, 105, 2610–2624.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lyamzin, D. R., Macke, J. H., & Lesica, N. A. (2010). Modeling population spike trains with specified time-varying spike rates, trial-to-trial variability, and pairwise signal and noise correlations. Frontiers in Computational Neuroscience, 4, 144.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lyamzin, D. R., Barnes, S. J., Donato, R., Garcia-Lazaro, J. A., Keck, T., & Lesica, N. A. (2015). Nonlinear transfer of signal and noise correlations in cortical networks. The Journal of Neuroscience, 35, 8065–8080.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macke, J. H., Berens, P., Ecker, A. S., Tolias, A. S., & Bethge, M. (2009). Generating spike trains with specified correlation coefficients. Neural Computation, 21, 397–423.

    Article  PubMed  Google Scholar 

  • Major, G., Larkum, M. E., & Schiller, J. (2013). Active properties of neocortical pyramidal neuron dendrites. Annual Review of Neuroscience, 36, 1–24.

    Article  CAS  PubMed  Google Scholar 

  • Marre, O., El Boustani, S., Frégnac, Y., & Destexhe, A. (2009). Prediction of spatiotemporal patterns of neural activity from pairwise correlations. Physical Review Letters, 102.

  • Mel, B. W. (1993). Synaptic integration in an excitable dendritic tree. Journal of Neurophysiology, 70, 1086–1101.

    Article  CAS  PubMed  Google Scholar 

  • Miura, K., Okada, M., & Amari, S. I. (2006). Estimating spiking irregularities under changing environments. Neural Computation, 18, 2359–2386.

    Article  PubMed  Google Scholar 

  • Murphy, B. K., & Miller, K. D. (2003). Multiplicative gain changes are induced by excitation or inhibition alone. The Journal of Neuroscience, 23, 10040–10051.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy, P. R., O'Connell, R. G., O'Sullivan, M., Robertson, I. H., & Balsters, J. H. (2014). Pupil diameter Covaries with BOLD activity in human locus Coeruleus. Human Brain Mapping, 35, 4140–4154.

    Article  PubMed  PubMed Central  Google Scholar 

  • Niebur, E. (2007). Generation of synthetic spike trains with defined pairwise correlations. Neural Computation, 19, 1720–1738.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ozden, I., Sullivan, M. R., Lee, H. M., & Wang, S. S. H. (2009). Reliable coding emerges from Coactivation of climbing fibers in microbands of cerebellar Purkinje neurons. The Journal of Neuroscience, 29, 10463–10473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paulin, M. G., & Hoffman, L. F. (2001). Optimal firing rate estimation. Neural Networks, 14, 877–881.

    Article  CAS  PubMed  Google Scholar 

  • Pillow, J. W., Shlens, J., Paninski, L., Sher, A., Litke, A. M., Chichilnisky, E. J., & Simoncelli, E. P. (2008). Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature, 454, 995–999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pipa, G., Grün, S., & van Vreeswijk, C. (2013). Impact of spike train autostructure on probability distribution of joint spike events. Neural Computation, 25, 1123–1163.

    Article  PubMed  Google Scholar 

  • Pisauro, M. A., Benucci, A., & Carandini, M. (2016). Local and global contributions to hemodynamic activity in mouse cortex. Journal of Neurophysiology, 115, 2931–2936.

    Article  PubMed  PubMed Central  Google Scholar 

  • Poirazi, P., Brannon, T., & Mel, B. W. (2003). Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron, 37, 977–987.

    Article  CAS  PubMed  Google Scholar 

  • Polsky, A., Mel, B., & Schiller, J. (2009). Encoding and decoding bursts by NMDA spikes in basal dendrites of layer 5 pyramidal neurons. The Journal of Neuroscience, 29, 11891–11903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prinz, A. A., Bucher, D., & Marder, E. (2004). Similar network activity from disparate circuit parameters. Nature Neuroscience, 7, 1345–1352.

    Article  CAS  PubMed  Google Scholar 

  • Reimer, J., McGinley, M. J., Liu, Y., Rodenkirch, C., Wang, Q., McCormick, D. A., & Tolias, A. S. (2016). Pupil fluctuations track rapid changes in adrenergic and cholinergic activity in cortex. Nature Communications, 7, 13289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson, H. P. C., & Kawai, N. (1993). Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. Journal of Neuroscience Methods, 49, 157–165.

    Article  CAS  PubMed  Google Scholar 

  • Ruskin, D. N., Bergstrom, D. A., Kaneoke, Y., Patel, B. N., Twery, M. J., & Walters, J. R. (1999a). Multisecond oscillations in firing rate in the basal ganglia: Robust modulation by dopamine receptor activation and anesthesia. Journal of Neurophysiology, 81, 2046–2055.

    Article  CAS  PubMed  Google Scholar 

  • Ruskin, D. N., Bergstrom, D. A., & Walters, J. R. (1999b). Multisecond oscillations in firing rate in the globus pallidus: Synergistic modulation by D1 and D2 dopamine receptors. The Journal of Pharmacology and Experimental Therapeutics, 290, 1493–1501.

    CAS  PubMed  Google Scholar 

  • Ruskin, D. N., Bergstrom, D. A., Tierney, P. L., & Walters, J. R. (2003). Correlated multisecond oscillations in firing rate in the basal ganglia: Modulation by dopamine and the subthalamic nucleus. Neuroscience, 117, 427–438.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, M., Hathway, P., Leuchs, L., Samann, P. G., Czisch, M., & Spoormaker, V. I. (2016). Spontaneous pupil dilations during the resting state are associated with activation of the salience network. Neuroimage, 139, 189–201.

    Article  PubMed  Google Scholar 

  • Sharp, A. A., Oneil, M. B., Abbott, L. F., & Marder, E. (1993). Dynamic clamp - computer-generated Conductances in real neurons. Journal of Neurophysiology, 69, 992–995.

    Article  CAS  PubMed  Google Scholar 

  • Shimaoka, D., Harris, K. D., & Carandini, M. (2018). Effects of arousal on mouse sensory cortex depend on modality. Cell Reports, 22, 3160–3167.

    Article  CAS  PubMed  Google Scholar 

  • Shimaoka, D., Steinmetz, N. A., Harris, K. D., & Carandini, M. (2019). The impact of bilateral ongoing activity on evoked responses in mouse cortex. Elife, 8.

  • Shinomoto, S., Shima, K., & Tanji, J. (2003). Differences in spiking patterns among cortical neurons. Neural Computation, 15, 2823–2842.

    Article  PubMed  Google Scholar 

  • Shinomoto, S., Miura, K., & Koyama, S. (2005). A measure of local variation of inter-spike intervals. Biosystems, 79, 67–72.

    Article  PubMed  Google Scholar 

  • Silver, R. A. (2010). Neuronal arithmetic. Nature Reviews Neuroscience, 11, 474–489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steuber, V., Schultheiss, N. W., Silver, R. A., De Schutter, E., & Jaeger, D. (2011). Determinants of synaptic integration and heterogeneity in rebound firing explored with data driven models of deep cerebellar nucleus cells. Journal of Computational Neuroscience, 30, 633–658.

    Article  PubMed  Google Scholar 

  • Stewart, T. C., Bekolay, T., & Eliasmith, C. (2012). Learning to select actions with spiking neurons in the basal ganglia. Frontiers in Neuroscience, 6, 2.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stringer, C., Pachitariu, M., Steinmetz, N., Bai Reddy, C., Carandini, M., & Harris, K. D. (2018). Spontaneous behaviors drive multidimensional, brain-wide population activity. bioRxiv.

  • Stringer, C., Pachitariu, M., Steinmetz, N., Reddy, C. B., Carandini, M., & Harris, K. D. (2019). Spontaneous behaviors drive multidimensional, brainwide activity. Science, 364, 255.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Traub, R. D., Kopell, N., Bibbig, A., Buhl, E. H., LeBeau, F. E., & Whittington, M. A. (2001). Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. The Journal of Neuroscience, 21, 9478–9486.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner, H., Takahashi, T., & Konishi, M. (1987). Representation of interaural time difference in the central nucleus of the barn owl's inferior colliculus. J.Neurosci., 7, 3105–3116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner, M. J., Kim, T. H., Kadmon, J., Nguyen, N. D., Ganguli, S., Schnitzer, M. J., & Luo, L. (2019). Shared cortex-cerebellum dynamics in the execution and learning of a motor task. Cell., 177, 669–682. e24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welsh, J. P., Lang, E. J., Suglhara, I., & Llinas, R. (1995). Dynamic organization of motor control within the olivocerebellar system. Nature, 374, 453–457.

    Article  CAS  PubMed  Google Scholar 

  • Yellin, D., Berkovich-Ohana, A., & Malach, R. (2015). Coupling between pupil fluctuations and resting-state fMRI uncovers a slow build-up of antagonistic responses in the human cortex. Neuroimage, 106, 414–427.

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported in part by NIH grant R01NS067201 to D.Jaeger. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Cerebellar data were recorded in the Heck lab at UTHS.

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Correspondence to Dieter Jaeger.

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Abbasi, S., Maran, S. & Jaeger, D. A general method to generate artificial spike train populations matching recorded neurons. J Comput Neurosci 48, 47–63 (2020). https://doi.org/10.1007/s10827-020-00741-w

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