{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,21]],"date-time":"2026-01-21T12:16:22Z","timestamp":1768997782839,"version":"3.49.0"},"reference-count":54,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,1,28]],"date-time":"2020-01-28T00:00:00Z","timestamp":1580169600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,1,28]],"date-time":"2020-01-28T00:00:00Z","timestamp":1580169600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100001201","name":"Kavli Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100001201","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005416","name":"Norges Forskningsr\u00e5d","doi-asserted-by":"publisher","award":["22326"],"award-info":[{"award-number":["22326"]}],"id":[{"id":"10.13039\/501100005416","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010665","name":"H2020 Marie Sk&lstrok;odowska-Curie Actions","doi-asserted-by":"publisher","award":["754411"],"award-info":[{"award-number":["754411"]}],"id":[{"id":"10.13039\/100010665","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Comput Neurosci"],"published-print":{"date-parts":[[2020,2]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Neuronal responses to complex stimuli and tasks can encompass a wide range of time scales. Understanding these responses requires measures that characterize how the information on these response patterns are represented across multiple temporal resolutions. In this paper we propose a metric \u2013 which we call multiscale relevance (MSR) \u2013 to capture the dynamical variability of the activity of single neurons across different time scales. The MSR is a non-parametric, fully featureless indicator in that it uses only the time stamps of the firing activity without resorting to any <jats:italic>a priori<\/jats:italic> covariate or invoking any specific structure in the tuning curve for neural activity. When applied to neural data from the mEC and from the ADn and PoS regions of freely-behaving rodents, we found that neurons having low MSR tend to have low mutual information and low firing sparsity across the correlates that are believed to be encoded by the region of the brain where the recordings were made. In addition, neurons with high MSR contain significant information on spatial navigation and allow to decode spatial position or head direction as efficiently as those neurons whose firing activity has high mutual information with the covariate to be decoded and significantly better than the set of neurons with high local variations in their interspike intervals. Given these results, we propose that the MSR can be used as a measure to rank and select neurons for their information content without the need to appeal to any <jats:italic>a priori<\/jats:italic> covariate.<\/jats:p>","DOI":"10.1007\/s10827-020-00740-x","type":"journal-article","created":{"date-parts":[[2020,1,28]],"date-time":"2020-01-28T06:04:10Z","timestamp":1580191450000},"page":"85-102","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Multiscale relevance and informative encoding in neuronal spike trains"],"prefix":"10.1007","volume":"48","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0002-1867","authenticated-orcid":false,"given":"Ryan John","family":"Cubero","sequence":"first","affiliation":[]},{"given":"Matteo","family":"Marsili","sequence":"additional","affiliation":[]},{"given":"Yasser","family":"Roudi","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2020,1,28]]},"reference":[{"key":"740_CR1","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1016\/j.coisb.2016.12.010","volume":"1","author":"C Battistin","year":"2017","unstructured":"Battistin, C., Dunn, B., Roudi, Y. (2017). Learning with unknowns: analyzing biological data in the presence of hidden variables. Current Opinion in Systems Biology, 1, 122\u2013128.","journal-title":"Current Opinion in Systems Biology"},{"issue":"5","key":"740_CR2","doi-asserted-by":"publisher","first-page":"710","DOI":"10.1038\/nn.3696","volume":"17","author":"C Buetfering","year":"2014","unstructured":"Buetfering, C., Allen, K., Monyer, H. (2014). Parvalbumin interneurons provide grid cell\u2013driven recurrent inhibition in the medial entorhinal cortex. Nature Neuroscience, 17(5), 710\u2013718.","journal-title":"Nature Neuroscience"},{"issue":"42","key":"740_CR3","doi-asserted-by":"publisher","first-page":"16344","DOI":"10.1073\/pnas.0807744105","volume":"105","author":"MI Chelaru","year":"2008","unstructured":"Chelaru, M.I., & Dragoi, V. (2008). Efficient coding in heterogeneous neuronal populations. Proceedings of the National Academy of Sciences, 105(42), 16344\u201316349.","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"3","key":"740_CR4","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1038\/nn.3310","volume":"16","author":"JJ Couey","year":"2013","unstructured":"Couey, J.J., Witoelar, A., Zhang, S.-J., Zheng, K., Ye, J., Dunn, B., Czajkowski, R., Moser, M.-B., Moser, E.I., Roudi, Y., et al. (2013). Recurrent inhibitory circuitry as a mechanism for grid formation. Nature Neuroscience, 16(3), 318\u2013324.","journal-title":"Nature Neuroscience"},{"key":"740_CR5","unstructured":"Cover, T.M., & Thomas, J.A. (2012). Elements of Information Theory. Wiley."},{"key":"740_CR6","doi-asserted-by":"publisher","first-page":"10","DOI":"10.3390\/e20100755","volume":"20","author":"RJ Cubero","year":"2018","unstructured":"Cubero, R.J., Marsili, M., Roudi, Y. (2018). Minimum description length codes are critical. Entropy, 20, 10.","journal-title":"Entropy"},{"issue":"6","key":"740_CR7","doi-asserted-by":"publisher","first-page":"P063402","DOI":"10.1088\/1742-5468\/ab16c8","volume":"2019","author":"RJ Cubero","year":"2019","unstructured":"Cubero, R.J., Jo, J., Marsili, M., Roudi, Y., Song, J. (2019). Statistical criticality arises in most informative representations. Journal of Statistical Mechanics: Theory and Experiment, 2019(6), P063402.","journal-title":"Journal of Statistical Mechanics: Theory and Experiment"},{"issue":"2","key":"740_CR8","doi-asserted-by":"publisher","first-page":"e1004052","DOI":"10.1371\/journal.pcbi.1004052","volume":"11","author":"B Dunn","year":"2015","unstructured":"Dunn, B., M\u00f8rreaunet, M., Roudi, Y. (2015). Correlations and functional connections in a population of grid cells. PLoS Computational Biology, 11(2), e1004052.","journal-title":"PLoS Computational Biology"},{"key":"740_CR9","doi-asserted-by":"crossref","unstructured":"Dunn, B., Wennberg, D., Huang, Z., Roudi, Y. (2017). Grid cells show field-to-field variability and this explains the aperiodic response of inhibitory interneurons. arXiv:1701.04893.","DOI":"10.1101\/101899"},{"issue":"4","key":"740_CR10","doi-asserted-by":"publisher","first-page":"1005","DOI":"10.1016\/j.celrep.2016.06.057","volume":"16","author":"CL Ebbesen","year":"2016","unstructured":"Ebbesen, C.L., Reifenstein, E.T., Tang, Q., Burgalossi, A., Ray, S., Schreiber, S., Kempter, R., Brecht, M. (2016). Cell type-specific differences in spike timing and spike shape in the rat parasubiculum and superficial medial entorhinal cortex. Cell reports, 16(4), 1005\u20131015.","journal-title":"Cell reports"},{"issue":"4","key":"740_CR11","doi-asserted-by":"publisher","first-page":"48002","DOI":"10.1209\/0295-5075\/81\/48002","volume":"81","author":"K-I Goh","year":"2008","unstructured":"Goh, K.-I., & Barab\u00e1si, A.-L. (2008). Burstiness and memory in complex systems. EPL (Europhysics Letters), 81(4), 48002.","journal-title":"EPL (Europhysics Letters)"},{"issue":"7","key":"740_CR12","doi-asserted-by":"publisher","first-page":"2147","DOI":"10.1039\/C6MB00047A","volume":"12","author":"S Grigolon","year":"2016","unstructured":"Grigolon, S., Franz, S., Marsili, M. (2016). Identifying relevant positions in proteins by critical variable selection. Molecular BioSystems, 12(7), 2147\u20132158.","journal-title":"Molecular BioSystems"},{"issue":"7052","key":"740_CR13","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1038\/nature03721","volume":"436","author":"T Hafting","year":"2005","unstructured":"Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., Moser, E.I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436(7052), 801.","journal-title":"Nature"},{"issue":"10","key":"740_CR14","doi-asserted-by":"publisher","first-page":"P10013","DOI":"10.1088\/1742-5468\/2015\/10\/P10013","volume":"2015","author":"A Haimovici","year":"2015","unstructured":"Haimovici, A., & Marsili, M. (2015). Criticality of mostly informative samples: a Bayesian model selection approach. Journal of Statistical Mechanics: Theory and Experiment, 2015(10), P10013.","journal-title":"Journal of Statistical Mechanics: Theory and Experiment"},{"issue":"2","key":"740_CR15","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1016\/j.neuron.2017.03.025","volume":"94","author":"K Hardcastle","year":"2017","unstructured":"Hardcastle, K., Maheswaranathan, N., Ganguli, S., Giocomo, L.M. (2017). A multiplexed, heterogeneous, and adaptive code for navigation in medial entorhinal cortex. Neuron, 94(2), 375\u2013387.","journal-title":"Neuron"},{"issue":"3","key":"740_CR16","doi-asserted-by":"publisher","first-page":"574","DOI":"10.1113\/jphysiol.1959.sp006308","volume":"148","author":"DH Hubel","year":"1959","unstructured":"Hubel, D.H., & Wiesel, T.N. (1959). Receptive fields of single neurones in the cat\u2019s striate cortex. The Journal of Physiology, 148(3), 574\u2013591.","journal-title":"The Journal of Physiology"},{"key":"740_CR17","doi-asserted-by":"publisher","first-page":"e42409","DOI":"10.7554\/eLife.42409","volume":"8","author":"MN Insanally","year":"2019","unstructured":"Insanally, M.N., Carcea, I., Field, R.E., Rodgers, C.C., DePasquale, B., Rajan, K., DeWeese, M.R., Albanna, B.F., Froemke, R.C. (2019). Spike-timing-dependent ensemble encoding by non-classically responsive cortical neurons. eLife, 8, e42409.","journal-title":"eLife"},{"issue":"7561","key":"740_CR18","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1038\/nature14622","volume":"523","author":"E Kropff","year":"2015","unstructured":"Kropff, E., Carmichael, J.E., Moser, M.-B., Moser, E.I. (2015). Speed cells in the medial entorhinal cortex. Nature, 523(7561), 419\u2013424.","journal-title":"Nature"},{"key":"740_CR19","doi-asserted-by":"publisher","first-page":"7538","DOI":"10.1038\/nature14153","volume":"518","author":"J Krupic","year":"2015","unstructured":"Krupic, J., Bauza, M., Burton, S., Barry, C., O\u2019Keefe, J. (2015). Grid cell symmetry is shaped by environmental geometry. Nature, 518, 7538.","journal-title":"Nature"},{"issue":"5985","key":"740_CR20","doi-asserted-by":"publisher","first-page":"1576","DOI":"10.1126\/science.1188210","volume":"328","author":"RF Langston","year":"2010","unstructured":"Langston, R.F., Ainge, J.A., Couey, J.J., Canto, C.B., Bjerknes, T.L., Witter, M.P., Moser, E.I., Moser, M. -B. (2010). Development of the spatial representation system in the rat. Science, 328(5985), 1576\u20131580.","journal-title":"Science"},{"issue":"31","key":"740_CR21","doi-asserted-by":"publisher","first-page":"10963","DOI":"10.1523\/JNEUROSCI.0276-15.2015","volume":"35","author":"P Latuske","year":"2015","unstructured":"Latuske, P., Toader, O., Allen, K. (2015). Interspike intervals reveal functionally distinct cell populations in the medial entorhinal cortex. Journal of Neuroscience, 35(31), 10963\u201310976.","journal-title":"Journal of Neuroscience"},{"key":"740_CR22","unstructured":"Lederberger, D., Battistin, C., Gardner, R.J., Roudi, Y., Witter, M., Moser, M.B., Moser, E.I. (2018). Multiplexed spatial representations in subiculum. FENS abstract."},{"issue":"09","key":"740_CR23","doi-asserted-by":"publisher","first-page":"P09003","DOI":"10.1088\/1742-5468\/2013\/09\/P09003","volume":"2013","author":"M Marsili","year":"2013","unstructured":"Marsili, M., Mastromatteo, I., Roudi, Y. (2013). On sampling and modeling complex systems. Journal of Statistical Mechanics: Theory and Experiment, 2013(09), P09003.","journal-title":"Journal of Statistical Mechanics: Theory and Experiment"},{"issue":"8","key":"740_CR24","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1038\/nrn1932","volume":"7","author":"BL McNaughton","year":"2006","unstructured":"McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I., Moser, M.-B. (2006). Path integration and the neural basis of the \u2019cognitive map\u2019. Nature Reviews Neuroscience, 7(8), 663\u2013678.","journal-title":"Nature Reviews Neuroscience"},{"issue":"6","key":"740_CR25","doi-asserted-by":"publisher","first-page":"1130","DOI":"10.1016\/j.celrep.2017.04.050","volume":"19","author":"RA Mease","year":"2017","unstructured":"Mease, R.A., Kuner, T., Fairhall, A.L., Groh, A. (2017). Multiplexed spike coding and adaptation in the thalamus. Cell Reports, 19(6), 1130\u20131140.","journal-title":"Cell Reports"},{"issue":"2","key":"740_CR26","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1152\/jn.1975.38.2.231","volume":"38","author":"MM Merzenich","year":"1975","unstructured":"Merzenich, M.M., Knight, P.L., Roth, G.L. (1975). Representation of cochlea within primary auditory cortex in the cat. Journal of Neurophysiology, 38(2), 231\u2013249.","journal-title":"Journal of Neurophysiology"},{"issue":"5","key":"740_CR27","doi-asserted-by":"publisher","first-page":"1178","DOI":"10.1016\/j.neuron.2017.10.027","volume":"96","author":"L Meshulam","year":"2017","unstructured":"Meshulam, L., Gauthier, J.L., Brody, C.D., Tank, D.W., Bialek, W. (2017). Collective behavior of place and non-place neurons in the hippocampal network. Neuron, 96(5), 1178\u20131191.","journal-title":"Neuron"},{"key":"740_CR28","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1016\/0006-8993(71)90358-1","volume":"34","author":"J O\u2019Keefe","year":"1971","unstructured":"O\u2019Keefe, J., & Dostrovsky, J. (1971). The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Research, 34, 171\u2013175.","journal-title":"Brain Research"},{"issue":"3","key":"740_CR29","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.tins.2009.12.001","volume":"33","author":"S Panzeri","year":"2010","unstructured":"Panzeri, S., Brunel, N., Logothetis, N.K., Kayser, C. (2010). Sensory neural codes using multiplexed temporal scales. Trends in Neurosciences, 33(3), 111\u2013120.","journal-title":"Trends in Neurosciences"},{"issue":"1","key":"740_CR30","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/j.neuron.2012.11.032","volume":"77","author":"H Pastoll","year":"2013","unstructured":"Pastoll, H., Solanka, L., van Rossum, M.C., Nolan, M.F. (2013). Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Neuron, 77(1), 141\u2013154.","journal-title":"Neuron"},{"key":"740_CR31","doi-asserted-by":"publisher","unstructured":"Peyrache, A., & Buzs\u00e1ki, G. (2015). Extracellular recordings from multi-site silicon probes in the anterior thalamus and subicular formation of freely moving mice. https:\/\/doi.org\/10.6080\/k0g15xs1.","DOI":"10.6080\/k0g15xs1"},{"issue":"4","key":"740_CR32","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1038\/nn.3968","volume":"18","author":"A Peyrache","year":"2015","unstructured":"Peyrache, A., Lacroix, M.M., Petersen, P.C., Buzs\u00e1ki, G. (2015). Internally organized mechanisms of the head direction sense. Nature Neuroscience, 18(4), 569\u2013575.","journal-title":"Nature Neuroscience"},{"issue":"1","key":"740_CR33","doi-asserted-by":"publisher","first-page":"1752","DOI":"10.1038\/s41467-017-01908-3","volume":"8","author":"A Peyrache","year":"2017","unstructured":"Peyrache, A., Schieferstein, N., Buzs\u00e1ki, G. (2017). Transformation of the head-direction signal into a spatial code. Nature Communications, 8(1), 1752.","journal-title":"Nature Communications"},{"issue":"2","key":"740_CR34","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1209\/0295-5075\/22\/2\/013","volume":"22","author":"F Rieke","year":"1993","unstructured":"Rieke, F., Warland, D., Bialek, W. (1993). Coding efficiency and information rates in sensory neurons. EPL (Europhysics Letters), 22(2), 151.","journal-title":"EPL (Europhysics Letters)"},{"issue":"5","key":"740_CR35","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1038\/nn.3704","volume":"17","author":"Y Roudi","year":"2014","unstructured":"Roudi, Y., & Moser, E.I. (2014). Grid cells in an inhibitory network. Nature Neuroscience, 17(5), 639\u2013641.","journal-title":"Nature Neuroscience"},{"key":"740_CR36","doi-asserted-by":"publisher","first-page":"e19428","DOI":"10.7554\/eLife.19428","volume":"6","author":"E Russo","year":"2017","unstructured":"Russo, E., & Durstewitz, D. (2017). Cell assemblies at multiple time scales with arbitrary lag constellations. Elife, 6, e19428.","journal-title":"Elife"},{"issue":"5774","key":"740_CR37","doi-asserted-by":"publisher","first-page":"758","DOI":"10.1126\/science.1125572","volume":"312","author":"F Sargolini","year":"2006","unstructured":"Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B.L., Witter, M.P., Moser, M.-B., Moser, E.I. (2006). Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science, 312(5774), 758\u2013762.","journal-title":"Science"},{"issue":"4","key":"740_CR38","doi-asserted-by":"publisher","first-page":"2339","DOI":"10.1523\/JNEUROSCI.14-04-02339.1994","volume":"14","author":"PE Sharp","year":"1994","unstructured":"Sharp, P.E., & Green, C. (1994). Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. Journal of Neuroscience, 14(4), 2339\u20132356.","journal-title":"Journal of Neuroscience"},{"issue":"12","key":"740_CR39","doi-asserted-by":"publisher","first-page":"2823","DOI":"10.1162\/089976603322518759","volume":"15","author":"S Shinomoto","year":"2003","unstructured":"Shinomoto, S., Shima, K., Tanji, J. (2003). Differences in spiking patterns among cortical neurons. Neural Computation, 15(12), 2823\u20132842.","journal-title":"Neural Computation"},{"issue":"1\u20133","key":"740_CR40","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.biosystems.2004.09.023","volume":"79","author":"S Shinomoto","year":"2005","unstructured":"Shinomoto, S., Miura, K., Koyama, S. (2005). A measure of local variation of inter-spike intervals. Bio Systems, 79(1\u20133), 67\u201372.","journal-title":"Bio Systems"},{"issue":"7","key":"740_CR41","doi-asserted-by":"publisher","first-page":"e1000433","DOI":"10.1371\/journal.pcbi.1000433","volume":"5","author":"S Shinomoto","year":"2009","unstructured":"Shinomoto, S., Kim, H., Shimokawa, T., Matsuno, N., Funahashi, S., Shima, K., Fujita, I., Tamura, H., Doi, T., Kawano, K., et al. (2009). Relating neuronal firing patterns to functional differentiation of cerebral cortex. PLoS Computational Biology, 5(7), e1000433.","journal-title":"PLoS Computational Biology"},{"key":"740_CR42","unstructured":"Skaggs, W.E., McNaughton, B.L., Gothard, K.M. (1993). An information-theoretic approach to deciphering the hippocampal code. In Advances in Neural Information Processing Systems (pp. 1030\u20131037)."},{"issue":"2","key":"740_CR43","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1002\/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K","volume":"6","author":"WE Skaggs","year":"1996","unstructured":"Skaggs, W.E., McNaughton, B.L., Wilson, M.A., Barnes, C.A. (1996). Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus, 6(2), 149\u2013172.","journal-title":"Hippocampus"},{"issue":"5909","key":"740_CR44","doi-asserted-by":"publisher","first-page":"1865","DOI":"10.1126\/science.1166466","volume":"322","author":"T Solstad","year":"2008","unstructured":"Solstad, T., Boccara, C.N., Kropff, E., Moser, M.-B., Moser, E.I. (2008). Representation of geometric borders in the entorhinal cortex. Science, 322(5909), 1865\u20131868.","journal-title":"Science"},{"issue":"12","key":"740_CR45","doi-asserted-by":"publisher","first-page":"123406","DOI":"10.1088\/1742-5468\/aaf10f","volume":"2018","author":"J Song","year":"2018","unstructured":"Song, J., Marsili, M., Jo, J. (2018). Resolution and relevance trade-offs in deep learning. Journal of Statistical Mechanics: Theory and Experiment, 2018(12), 123406.","journal-title":"Journal of Statistical Mechanics: Theory and Experiment"},{"issue":"6","key":"740_CR46","doi-asserted-by":"publisher","first-page":"797","DOI":"10.1016\/S0006-3495(67)86623-2","volume":"7","author":"RB Stein","year":"1967","unstructured":"Stein, R.B. (1967). The information capacity of nerve cells using a frequency code. Biophysical Journal, 7(6), 797\u2013826.","journal-title":"Biophysical Journal"},{"issue":"5","key":"740_CR47","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1038\/nrn1668","volume":"6","author":"RB Stein","year":"2005","unstructured":"Stein, R.B., Gossen, E.R., Jones, K.E. (2005). Neuronal variability: noise or part of the signal? Nature Reviews Neuroscience, 6(5), 389.","journal-title":"Nature Reviews Neuroscience"},{"issue":"7427","key":"740_CR48","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1038\/nature11649","volume":"492","author":"H Stensola","year":"2012","unstructured":"Stensola, H., Stensola, T., Solstad, T., Fr\u00f8land, K, Moser, M.-B., Moser, E.I. (2012). The entorhinal grid map is discretized. Nature, 492(7427), 72\u201378.","journal-title":"Nature"},{"issue":"7538","key":"740_CR49","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1038\/nature14151","volume":"518","author":"T Stensola","year":"2015","unstructured":"Stensola, T., Stensola, H., Moser, M.-B., Moser, E.I. (2015). Shearing-induced asymmetry in entorhinal grid cells. Nature, 518(7538), 207\u2013212.","journal-title":"Nature"},{"issue":"1","key":"740_CR50","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1103\/PhysRevLett.80.197","volume":"80","author":"SP Strong","year":"1998","unstructured":"Strong, S.P., Koberle, R., van Steveninck, R.R.d.R., Bialek, W. (1998). Entropy and information in neural spike trains. Physical Review Letters, 80(1), 197.","journal-title":"Physical Review Letters"},{"issue":"1","key":"740_CR51","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1523\/JNEUROSCI.15-01-00070.1995","volume":"15","author":"JS Taube","year":"1995","unstructured":"Taube, J.S. (1995). Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. Journal of Neuroscience, 15(1), 70\u201386.","journal-title":"Journal of Neuroscience"},{"issue":"2","key":"740_CR52","doi-asserted-by":"publisher","first-page":"420","DOI":"10.1523\/JNEUROSCI.10-02-00420.1990","volume":"10","author":"JS Taube","year":"1990","unstructured":"Taube, J.S., Muller, R.U., Ranck, J.B. (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. i. Description and quantitative analysis. Journal of Neuroscience, 10(2), 420\u2013435.","journal-title":"Journal of Neuroscience"},{"issue":"2","key":"740_CR53","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1162\/neco.1995.7.2.399","volume":"7","author":"A Treves","year":"1995","unstructured":"Treves, A., & Panzeri, S. (1995). The upward bias in measures of information derived from limited data samples. Neural Computation, 7(2), 399\u2013407.","journal-title":"Neural Computation"},{"issue":"2","key":"740_CR54","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.1152\/jn.1998.79.2.1017","volume":"79","author":"K Zhang","year":"1998","unstructured":"Zhang, K., Ginzburg, I., McNaughton, B.L., Sejnowski, T.J. (1998). Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. Journal of Neurophysiology, 79(2), 1017\u20131044.","journal-title":"Journal of Neurophysiology"}],"container-title":["Journal of Computational Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10827-020-00740-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s10827-020-00740-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10827-020-00740-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,15]],"date-time":"2024-08-15T08:03:31Z","timestamp":1723709011000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s10827-020-00740-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,28]]},"references-count":54,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2020,2]]}},"alternative-id":["740"],"URL":"https:\/\/doi.org\/10.1007\/s10827-020-00740-x","relation":{},"ISSN":["0929-5313","1573-6873"],"issn-type":[{"value":"0929-5313","type":"print"},{"value":"1573-6873","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,28]]},"assertion":[{"value":"19 July 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 December 2019","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 January 2020","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 January 2020","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with Ethical Standards"}},{"value":"The authors declare no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"<!--Emphasis Type='Bold' removed-->Conflict of interests"}}]}}