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Inhibitory synapses between striatal projection neurons support efficient enhancement of cortical signals: A computational model

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Abstract

The function of lateral inhibitory synapses between striatal projection neurons is currently poorly understood. This paper puts forward a model suggesting that inhibitory collaterals can be used to enhance the incoming cortical signals. In particular, we propose that lateral inhibition between projection neurons performs a signal-enhancing process that resembles the image processing technique of “unsharp masking”, where a blurred copy is used to enhance and sharpen an input image. The paper also presents the results of computer simulations deomsntrating that the proposed mechanisms is compatible with known properties of striatal projection neurons, and outperforms alternative models of lateral inhibition. Finally, this paper illustrates the advantages of the proposed model and discusses the relevance of these conclusions for existing computational models of the basal ganglia and their role in cognition.

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References

  • Albin, R.L., Young, A.B., Penney, J.B. (1989). The functional anatomy of basal ganglia disorders. Trends in Neurosciences, 12, 366–375.

    Article  CAS  PubMed  Google Scholar 

  • Alexander, G.E., DeLong, M.R., Strick, P.L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357–381.

    Article  CAS  PubMed  Google Scholar 

  • Bar-Gad, I., Havazelet-Heimer, G., Goldberg, J.A., Ruppin, E., Bergman, H. (2000). Reinforcement-driven dimensionality reduction–a model for information processing in the basal ganglia. Journal of Basic and Clinical Physiology and Pharmacology, 11, 305–320.

    Article  CAS  PubMed  Google Scholar 

  • Bogacz, R., & Gurney, K. (2007). The basal ganglia and cortex implement optimal decision making between alternative actions. Neural computation, 19(2), 442–477.

    Article  PubMed  Google Scholar 

  • Fox, M.D., Snyder, A., Vincent, J., Corbetta, M., Essen, D.V., Raichle, M. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences, 102, 9673–9678.

    Article  CAS  Google Scholar 

  • Frank, M.J., & Claus, E.D. (2006). Anatomy of a decision: striatoorbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychological Review, 113(2), 300.

    Article  PubMed  Google Scholar 

  • Frank, M.J., Loughry, B., O’Reilly, R.C. (2001). Interactions between frontal cortex and basal ganglia in working memory: a computational model. Cognitive, Affective & Behavioral Neuroscience, 1, 137–160.

    Article  CAS  Google Scholar 

  • Frank, M.J., Seeberger, L.C., O’Reilly, R.C. (2004). By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science, 306(5703), 1940–1943.

    Article  CAS  PubMed  Google Scholar 

  • Gurney, K., Prescott, T.J., Redgrave, P. (2001a). A computational model of action selection in the basal ganglia. i. a new functional anatomy. Biological Cybernetics, 84, 401–410.

    Article  CAS  PubMed  Google Scholar 

  • Gurney, K., Prescott, T.J., Redgrave, P. (2001b). A computational model of action selection in the basal ganglia. ii. analysis and simulation of behaviour. Biological Cybernetics, 84, 411–423.

    Article  CAS  PubMed  Google Scholar 

  • Haber, S.N. (2003). The primate basal ganglia: parallel and integrative networks. Journal of Chemical Neuroanatomy, 26(4), 317–330.

    Article  PubMed  Google Scholar 

  • Humphries, M.D., Wood, R., Gurney, K. (2009). Dopamine-modulated dynamic cell assemblies generated by the gabaergic striatal micro-circuit. Neural Networks, 22(8), 1174–1188.

    Article  PubMed  Google Scholar 

  • Humphries, M.D., Wood, R., Gurney, K. (2010). Reconstructing the three-dimensional gabaergic microcircuit of the striatum. PLoS Computational Biology, 6(11), e1001,011.

    Article  Google Scholar 

  • Izhikevich, E.M., & Edelman, G. (2008). Large-scale model of mammalian thalamocortical systems. Proceedings of the National Academy of Sciences, 105, 3593–3598.

    Article  CAS  Google Scholar 

  • Jaeger, D., Kita, H., Wilson, C.J. (1994). Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. Journal of Neurophysiology, 72, 2555–2558.

    CAS  PubMed  Google Scholar 

  • Kemp, J.M., & Powell, T.P. (1970). The corticostriate projection in the monkey. Brain, 93, 525–546.

    Article  CAS  PubMed  Google Scholar 

  • Levi, L. (1974). Unsharp masking and related image enhancement techniques. Computer Graphics and Image Processing, 3, 163–177.

    Article  Google Scholar 

  • Lippman, R.P. (1987). An introduction to computing with neural nets. IEEE Transaction on Acoustics, Speech, and Signal Processing, 35, 2–44.

    Article  Google Scholar 

  • McNab, F., & Klingberg, T. (2008). Prefrontal cortex and basal ganglia control access to working memory. Nature Neuroscience, 11, 103–107.

    Article  CAS  PubMed  Google Scholar 

  • Moyer, J.T., Wolf, J.A., Finkel, L.H. (2007). Effects of dopaminergic modulation on the integrative properties of the ventral striatal medium spiny neuron. Journal of Neurophysiology, 98(6), 3731–3748.

    Article  CAS  PubMed  Google Scholar 

  • Nisenbaum, E., & Berger, T. (1992). Functionally distinct subpopulations of striatal neurons are differentially regulated by gabaergic and dopaminergic inputs—I. In vivo analysis. Neuroscience, 48(3), 561–578.

    Article  CAS  PubMed  Google Scholar 

  • O’Reilly, R.C., & Frank, M.J. (2006). Making working memory work: A computational model of learning in the prefrontal cortex and basal ganglia. Neural Computation, 18, 283–328.

    Article  PubMed  Google Scholar 

  • O’Reilly, R.C., & Munakata, Y. (2000). Computational explorations in cognitive neuroscience. Cambridge: MIT Press.

    Google Scholar 

  • Packard, M.G., & Knowlton, B.J. (2002). Learning and memory functions of the basal ganglia. Annual Review of Neuroscience, 25(1), 563–593.

    Article  CAS  PubMed  Google Scholar 

  • Parent, A., & Hazrati, L.N. (1995a). Functional anatomy of the basal ganglia. i. the cortico-basal ganglia-thalamo-cortical loop. Brain Research Reviews, 20(1), 91–127.

    Article  CAS  PubMed  Google Scholar 

  • Parent, A., & Hazrati, L.N. (1995b). Functional anatomy of the basal ganglia. ii. the place of subthalamic nucleus and external pallidium in basal ganglia circuitry. Brain Research Reviews, 20(1), 128–154.

    Article  CAS  PubMed  Google Scholar 

  • Plenz, D. (2003). When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function. Trends in Neurosciences, 26(8), 436–443.

    Article  CAS  PubMed  Google Scholar 

  • Pouget, A., Dayan, P., Zemel, R. (2000). Information processing with population codes. Nature Reviews Neuroscience, 1, 125–132.

    Article  CAS  PubMed  Google Scholar 

  • Redgrave, P., Prescott, T.J., Gurney, K. (1999). The basal ganglia: A vertebrate solution to the selection problem. Neuroscience, 89, 1009–1023.

    Article  CAS  PubMed  Google Scholar 

  • Schultz, W., Dayan, P., Montague, P.R. (1997). A neural substrate of prediction and reward. Science, 275(5306), 1593–1599

    Article  CAS  PubMed  Google Scholar 

  • Stern, E.A., Jaeger, D., Wilson, C.J. (1998). Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo. Nature, 394(6692), 475–478.

    Article  CAS  PubMed  Google Scholar 

  • Stocco, A. (2012). Acetylcholine-based entropy in response selection: a model of how striatal interneurons modulate exploration, exploitation, and response variability in decision-making. Frontiers in Neuroscience, 6.

  • Stocco, A., & Anderson, J.R. (2008). Endogenous control and task representation: an fmri study in algebraic problem-solving. Journal of Cognitive Neuroscience, 20(7), 1300–1314.

    Article  PubMed  Google Scholar 

  • Stocco, A., Lebiere, C., Anderson, J.R. (2010). Conditional routing of information to the cortex: A model of the basal ganglia’s role in cognitive coordination. Psychological Review, 117, 541–574.

    Article  PubMed Central  PubMed  Google Scholar 

  • Stocco, A., Lebiere, C., O’Reilly, R.C., Anderson, J.R. (2012). Distinct contributions of the caudate nucleus, rostral prefrontal cortex, and parietal cortex to the execution of instructed tasks. Cognitive, Affective, & Behavioral Neuroscience, 12(4), 611–628.

    Article  Google Scholar 

  • Tecuapetla, F., Carrillo-Reid, L., Guzmán, J.N., Galarraga, E., Bargas, J. (2005). Different inhibitory inputs onto neostriatal projection neurons as revealed by field stimulation. Journal of Neurophysiology, 93(2), 1119–1126.

    Article  PubMed  Google Scholar 

  • Tepper, J.M., Koós, T., Wilson, C.J. (2004). Gabaergic microcircuits in the neostriatum. Trends in Neurosciences, 27(11), 662–669.

    Article  CAS  PubMed  Google Scholar 

  • Tepper, J.M.,Wilson, C.J., Koós, T. (2008). Feedforward and feedback inhibition in neostriatal gabaergic spiny neurons. Brain Research Reviews, 58(2), 272–281.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tunstall, M.J., Oorschot, D.E., Kean, A., Wickens, J.R. (2002). Inhibitory interactions between spiny projection neurons in the rat striatum. Journal of Neurophysiology, 88, 1263–1269.

    PubMed  Google Scholar 

  • Wickens, J., Kotter, R., Alexander, M. (1995). Effects of local connectivity on striatal function: Simulation and analysis of a model. Synapse, 20(4), 281–298.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, C.J. (2007). Gabaergic inhibition in the neostriatum. Progress in Brain Research, 160, 91–110.

    Article  CAS  PubMed  Google Scholar 

  • Yelnik, J., Francois, C., Percheron, G., Tande, D. (1991). Morphological taxonomy of the neurons of the primate striatum. Journal of Comparative Neurology, 313, 273–294.

    Article  CAS  PubMed  Google Scholar 

  • Yin, H.H., & Knowlton, B.J. (2006). The role of the basal ganglia in habit formation. Nature Reviews Neuroscience, 7(6), 464–476.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, T., & Wilson, C.J. (2002). Corticostriatal combinatorics: The implications of corticostriatal axonal arborizations. Journal of Neurophysiology, 87(2), 1007–1017.

    CAS  PubMed  Google Scholar 

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Correspondence to Andrea Stocco.

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Action Editor: Alessandro Treves

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Stocco, A., Lebiere, C. Inhibitory synapses between striatal projection neurons support efficient enhancement of cortical signals: A computational model. J Comput Neurosci 37, 65–80 (2014). https://doi.org/10.1007/s10827-013-0490-4

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  • DOI: https://doi.org/10.1007/s10827-013-0490-4

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