Skip to main content
Log in

Causal networks in simulated neural systems

  • Research Article
  • Published:
Cognitive Neurodynamics Aims and scope Submit manuscript

Abstract

Neurons engage in causal interactions with one another and with the surrounding body and environment. Neural systems can therefore be analyzed in terms of causal networks, without assumptions about information processing, neural coding, and the like. Here, we review a series of studies analyzing causal networks in simulated neural systems using a combination of Granger causality analysis and graph theory. Analysis of a simple target-fixation model shows that causal networks provide intuitive representations of neural dynamics during behavior which can be validated by lesion experiments. Extension of the approach to a neurorobotic model of the hippocampus and surrounding areas identifies shifting causal pathways during learning of a spatial navigation task. Analysis of causal interactions at the population level in the model shows that behavioral learning is accompanied by selection of specific causal pathways—“causal cores”—from among large and variable repertoires of neuronal interactions. Finally, we argue that a causal network perspective may be useful for characterizing the complex neural dynamics underlying consciousness.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Notes

  1. Many applications in neurophysiology make use of a frequency-domain version of Granger causality (Geweke 1982; Kaminski et al. 2001). However, because in this paper we analyze simulation models without oscillatory dynamics, we remain in the (simpler) time domain.

  2. The fitness function was F = t fix  + 0.25(35 − d̄), where t fix denotes the proportion of time for which the target was fixated and d̄ the mean offset between H and G (the environment was a toroidal square plane with side length 100).

  3. The analyzed time series varied in length from 450 to 4,994 time-steps. Robustness to different lengths was assessed by reanalyzing causal interactions after dividing each time series into two parts; results were qualitatively identical (see (Seth and Edelman 2007) for details).

  4. Recursive complexity refers to the balance between differentiation and integration across different levels of description. The phenomenal structure of consciousness appears to be recursive inasmuch as individual features of conscious scenes are themselves Gestalts which share organizational properties with the conscious scene as a whole.

  5. Because Granger causality is based on linear regression it assumes a continuous signal, but neural systems at the level of spikes are discontinuous. A straightforward adaptation of the technique is to convolve spikes with a continuous function (e.g., a half-Gaussian) in order to generate a continuous signal. A more principled but more complex alternative is to substitute linear regression modelling with a point-process prediction algorithm (Okatan et al. 2005; Nykamp 2007).

  6. J. Feng, personal communication.

References

  • Ancona N, Marinazzo D, Stramaglia S (2004) Radial basis function approaches to nonlinear granger causality of time series. Phys Rev E 70:056221

    Article  Google Scholar 

  • Bernasconi C, Konig P (1999) On the directionality of cortical interactions studied by structural analysis of electrophysiological recordings. Biol Cybern 81:199–210

    Article  PubMed  CAS  Google Scholar 

  • Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificit and binocular interaction in the visual cortex. J Neurosci 2(1):32–48

    PubMed  CAS  Google Scholar 

  • Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R, Bressler S (2004) Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc Natl Acad Sci USA 101(26):9849–9854

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Rangarajan G, Feng J, Ding M (2004) Analyzing multiple nonlinear time series with extended Granger causality. Phys Lett A 324:26–35

    Article  CAS  Google Scholar 

  • Churchland P, Sejnowski T (1994) The computational brain. MIT Press, Cambridge, MA

    Google Scholar 

  • Clark A (1997) Being there: putting brain, body, and world together again. MIT Press, Cambridge, MA

    Google Scholar 

  • deCharms RC, Zador A (2000) Neural representation and the cortical code. Annu Rev Neurosci 23:613–647

    Article  PubMed  CAS  Google Scholar 

  • Ding M, Bressler S, Yang W, Liang H (2000) Short-window spectral analysis of cortical event-related potentials by adaptive multivariate autoregressive modeling: data prepocessing, model validation, and variability assessment. Biol Cybern 83:35–45

    Article  PubMed  CAS  Google Scholar 

  • Ding M, Chen Y, Bressler S (2006) Granger causality: basic theory and application to neuroscience. In: Schelter S, Winterhalder M, Timmer J (eds) Handbook of time series analysis. Wiley, Wienheim, pp 438–460

    Google Scholar 

  • Dityatev AE, Bolshakov VY (2005) Amygdala, long-term potentiation, and fear conditioning. Neuroscientist 11:75–88

    Article  PubMed  CAS  Google Scholar 

  • Drew PJ, Abbott LF (2006) Extending the effects of spike-timing-dependent plasticity to behavioral timescales. Proc Natl Acad Sci USA 103(23):8876–8881

    Article  PubMed  CAS  Google Scholar 

  • Edelman GM (1987) Neural Darwinism. Basic Books, New York

    Google Scholar 

  • Edelman GM (1993) Selection and reentrant signaling in higher brain function. Neuron 10:115–125

    Article  PubMed  CAS  Google Scholar 

  • Edelman GM (2003) Naturalizing consciousness: a theoretical framework. Proc Natl Acad Sci USA 100(9):5520–5524

    Article  PubMed  CAS  Google Scholar 

  • Edelman GM, Tononi G (2000) A universe of consciousness: how matter becomes imagination. Basic Books, New York

    Google Scholar 

  • Eichler M (2005) A graphical approach for evaluating effective connectivity in neural systems. Philos Trans R Soc B 360:953–967

    Article  Google Scholar 

  • Friewald WA, Valdes P, Bosch J, Biscay R, Jimenez JC, Rodriguez LM, Rodriguez V, Kreiter AK, Singer W (1999) The use of time-variant EEG Granger causality for inspecting directed interdependencies of neural assemblies. J Neurosci Methods 94:105–119

    Article  Google Scholar 

  • Friston K (1994) Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp 2:56–78

    Article  Google Scholar 

  • Friston K (2005) A theory of cortical responses. Philos Trans R Soc Lond B Biol Sci 360:815–836

    Article  PubMed  Google Scholar 

  • Friston K, Harrison L, Penny W (2003) Dynamic causal modeling. Neuroimage 19(4):1273–1302

    Article  PubMed  CAS  Google Scholar 

  • Geweke J (1982) Measurement of linear dependence and feedback between multiple time series. J Am Stat Assoc 77:304–313

    Article  Google Scholar 

  • Granger CWJ (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37:424–438

    Article  Google Scholar 

  • Grossberg S (1999) The link between brain learning, attention, and consciousness. Conscious Cogn 8:1–44

    Article  PubMed  CAS  Google Scholar 

  • Hamilton JD (1994) Time series analysis. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Hesse W, Möller E, Arnold M, Schack B (2003) The use of time-variant EEG Granger causality for inspecting directed interdependencies of neural assemblies. J Neurosc Methods 124:27–44

    Article  Google Scholar 

  • Horwitz B, Warner B, Fitzer J, Tagamets M, Husain F, Long T (2005) Investigating the neural basis for functional and effective connectivity. Application to fmri. Philos Trans R Soc Lond B Biol Sci 360:1093–1108

    Article  PubMed  Google Scholar 

  • James W (1904) Does consciousness exist? J Philos Pyschol Sci Methods 1:477–491

    Article  Google Scholar 

  • Kaminski M, Ding M, Truccolo WA, Bressler SL (2001) Evaluating causal relations in neural systems: Granger causality, directed transfer function and statistical assessment of significance. Biol Cybern 85:145–157

    Article  PubMed  CAS  Google Scholar 

  • Keinan A, Sandbank B, Hilgetag CC, Meilijson I, Ruppin E (2004) Fair attribution of functional contribution in artificial and biological networks. Neural Comput 16:1887–1915

    Article  PubMed  Google Scholar 

  • Kelly RM, Strick PL (2004) Macro-architecture of basal ganglia loops with the cerebral cortex: use of rabies virus to reveal multisynaptic circuits. Prog Brain Res 143:449–459

    PubMed  Google Scholar 

  • Knoblauch A, Palm G (2005) What is signal and what is noise in the brain? Biosystems 79(1–3):83–90

    Article  PubMed  Google Scholar 

  • Konkle AT, Bielajew C (2004) Tracing the neuroanatomical profiles of reward pathways with markers of neuronal activation. Rev Neurosci 15(6):383–414

    PubMed  Google Scholar 

  • Krichmar JL, Edelman GM (2002) Machine psychology: autonomous behavior, perceptual categorization and conditioning in a brain-based device. Cereb Cortex 12(8):818–830

    Article  PubMed  Google Scholar 

  • Krichmar JL, Nitz DA, Gally JA, Edelman GM (2005a) Characterizing functional hippocampal pathways in a brain-based device as it solves a spatial memory task. Proc Natl Acad Sci USA 102(6):2111–2116

    Article  PubMed  CAS  Google Scholar 

  • Krichmar JL, Seth AK, Nitz DA, Fleischer JG, Edelman GM (2005b) Spatial navigation and causal analysis in a brain-based device modeling cortical-hippocampal interactions. Neuroinformatics 3(3):197–222

    Article  PubMed  Google Scholar 

  • Lavenex P, Amaral D (2000) Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10:420–430

    Article  PubMed  CAS  Google Scholar 

  • Liang H, Ding M, Nakamura R, Bressler SL (2000) Causal influences in primate cerebral cortex during visual pattern discrimination. Neuroreport 11(13):2875–2880

    Article  PubMed  CAS  Google Scholar 

  • Lin L, Osan R, Tsien J (2006) Organizing principles of real-time memory encoding: neural clique assemblies and universal neural codes. Trends Neurosci 29(1):48–57

    Article  PubMed  CAS  Google Scholar 

  • Lungarella M, Ishiguro K, Kuniyoshi Y, Otsu N (2007) Methods for quantifying the causal structure of bivariate time series. Int J Bifurcat Chaos 17(3):903–921

    Article  Google Scholar 

  • Makarov V, Panetsos F, de Feo O (2005) A method for determining neural connectivity and inferring the underlying neural dynamics using extracellular spike recordings. J Neurosci Methods 144:265–279

    PubMed  Google Scholar 

  • Malenka RC, Bear M (2004) LTP and LTD: an embarrasment of riches. Neuron 44:5–21

    Article  PubMed  CAS  Google Scholar 

  • McIntosh AR, Gonzalez-Lima F (1994) Structural equation modeling and its application to network analysis in functional brain imaging. Hum Brain Mapp 2:2–22

    Article  Google Scholar 

  • Morris RGM (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47–60

    Article  PubMed  CAS  Google Scholar 

  • Nykamp D (2007) A mathematical framework for inferring connectivity in probabilistic neuronal networks. Math Biosci 205(2):204–251

    Article  PubMed  Google Scholar 

  • Okatan M, Wilson MA, Brown EN (2005) Analyzing functional connectivity using a network likelihood model of ensemble neural spiking activity. Neural Comput 17(9):1927–1961

    Article  PubMed  Google Scholar 

  • Pearl J (1999) Causality: models, reasoning, and inference. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Raffi M, Siegel RM (2005) Functional architecture of spatial attention in the parietal cortex of the behaving monkey. J Neurosci 25:5171–5186

    Article  PubMed  CAS  Google Scholar 

  • Rees G, Kreiman G, Koch C (2002) Neural correlates of consciousness in humans. Nat Rev Neurosci 3(4):261–270

    Article  PubMed  CAS  Google Scholar 

  • Roebroeck A, Formisano E, Goebel R (2005) Mapping directed influence over the brain using granger causality and fmri. Neuroimage 25(1):230–242

    Article  PubMed  Google Scholar 

  • Schreiber T (2000) Measuring information transfer. Phys Rev Lett 85(2):461–464

    Article  PubMed  CAS  Google Scholar 

  • Schwartz G (1978) Estimating the dimension of a model. Ann Stat 5(2):461–464

    Article  Google Scholar 

  • Seth AK (2005) Causal connectivity of evolved neural networks during behavior. Network Comput Neural Syst 16:35–54

    Article  Google Scholar 

  • Seth AK (2007) Granger causality. Scholarpedia, page 15501

  • Seth AK (2007) Granger causality analysis of MEG signals during a working memory task. Abst Soc Neurosci

  • Seth AK, Baars BJ (2005) Neural Darwinism and consciousness. Conscious Cogn 14:140–168

    Article  PubMed  Google Scholar 

  • Seth AK, Baars BJ, Edelman DB (2005) Criteria for consciousness in humans and other mammals. Conscious Cogn 14(1):119–139

    Article  PubMed  Google Scholar 

  • Seth AK, Edelman GM (2004) Environment and behavior influence the complexity of evolved neural networks. Adapt Behav 12:5–21

    Article  Google Scholar 

  • Seth AK, Edelman GM (2007) Distinguishing causal interactions in neural populations. Neural Comput 19:910–933

    Article  PubMed  Google Scholar 

  • Seth AK, Izhikevich E, Reeke GN, Edelman GM (2006) Theories and measures of consciousness: an extended framework. Proc Natl Acad Sci USA 103(28):10799–10804

    Article  PubMed  CAS  Google Scholar 

  • Sherman M, Guillery R (2002) The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc B Biol Sci 357:1695–1708

    Article  Google Scholar 

  • Smith V, Yu J, Smulders T, Hartemink A, Jarvis E (2006) Computational inference of neural information flow networks. PLoS Comput Biol 2(11):e161

    Article  PubMed  Google Scholar 

  • Sporns O, Lungarella M (2006) Information flow in sensorimotor networks. PLoS Comput Biol 2(10):e144

    Article  PubMed  Google Scholar 

  • Sporns O, Tononi G, Kotter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1(4):e42

    Article  PubMed  Google Scholar 

  • Stein RB, Gossen ER, Jones KE (2005) Neuronal variability: noise or part of the signal? Nat Rev Neurosci 6(5):389–397

    Article  PubMed  CAS  Google Scholar 

  • Sutton R, Barto A (1998) Reinforcement learning. MIT Press, Cambridge, MA

    Google Scholar 

  • Timme M (2007) Revealing network connectivity from response dynamics. Phys Rev Lett 98:224101

    Article  PubMed  Google Scholar 

  • Tononi G (2004) An information integration theory of consciousness. BMC Neurosci 5(1):42

    Article  PubMed  Google Scholar 

  • Tononi G, Edelman GM (1998) Consciousness and complexity. Science 282:1846–1851

    Article  PubMed  CAS  Google Scholar 

  • Tononi G, Sporns O (2003) Measuring information integration. BMC Neurosci 4(1):31

    Article  PubMed  Google Scholar 

  • Tononi G, Sporns O, Edelman GM (1994) A measure for brain complexity: relating functional segregation and integration in the nervous system. Proc Natl Acad Sci USA 91:5033–5037

    Google Scholar 

  • Valdes-Sosa P, Sanchez-Bornot J, Lage-Castellanos A, Vega-Hernandez M, Bosch-Bayard J, Melie-Garcia L, Canales-Rodriguez E (2005) Estimating brain functional connectivity with sparse multivariate autoregression. Philos Trans R Soc Lond B Biol Sci 360:969–981

    Article  Google Scholar 

  • Zellner A (1971) An introduction to Bayesian inference in econometrics. Wiley, New York

    Google Scholar 

Download references

Acknowledgment

The research described in this paper was largely carried out while the author was at The Neurosciences Institute, La Jolla, California, with support from the Neurosciences Research Foundation. Many thanks to my colleagues there and in particular to Jeffrey L. Krichmar and Gerald M. Edelman who were instrumental in enabling this work. I am also grateful for the comments of two anonymous reviewers.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anil K. Seth.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seth, A.K. Causal networks in simulated neural systems. Cogn Neurodyn 2, 49–64 (2008). https://doi.org/10.1007/s11571-007-9031-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-007-9031-z

Keywords

Navigation