Transient and steady-state selection in the striatal microcircuit

Frontiers in Computational Neuroscience

Volumn , Issue JAN, 2014, Pages

  Tomkins, Adam ^a   Vasilaki, Eleni ^a   Beste, Christian ^b   Gurney, Kevin ^a   Humphries, Mark D ^c  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Action selection; Basal ganglia; Excitotoxicity; Huntington's disease; Response selection; Striatum

Indexed keywords

ACTION SELECTION; BASAL GANGLIA; EXCITOTOXICITY; HUNTINGTON'S DISEASE; RESPONSE SELECTION; STRIATUM;

SIGNAL PROCESSING;

NEURODEGENERATIVE DISEASES;

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; BASAL GANGLION; COGNITION; COGNITIVE DEFECT; DECISION MAKING; EXPERIMENTAL TEST; GABAERGIC SYSTEM; HUNTINGTON CHOREA; SIGNAL PROCESSING; STEADY STATE; SUBTHALAMIC NUCLEUS; TASK PERFORMANCE; THALAMOCORTICAL TRACT; WORKING MEMORY; ADAPTATION; ARTIFICIAL NEURAL NETWORK; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; FUNCTIONAL ASSESSMENT; HUMAN; INTERMETHOD COMPARISON; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; SELECTION BIAS; SPIKE WAVE; STEADY STATE SELECTION; STIMULUS RESPONSE; STRIATE CORTEX; TRANSIENT SELECTION;

EID: 84892970146     PISSN: 16625188     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncom.2013.00192     Document Type: Article

References (65)

1. Alexander, M. E., and Wickens, J. R. (1993). Analysis of striatal dynamics: the existence of two modes of behaviour. J. Theor. Biol. 163, 413-438. doi: 10.1006/jtbi.1993.1128
2. Asaad, W. F., Rainer, G., and Miller, E. K. (2000). Task-specific neural activity in the primate prefrontal cortex. J. Neurophysiol. 84, 451-459.
3. Bamford, K. A., Caine, E. D., Kido, D. K., Cox, C., and Shoulson, I. (1995). A prospective evaluation of cognitive decline in early Huntington's disease: functional and radiographic correlates. Neurology 45, 1867-1873. doi: 10.1212/WNL.45.10.1867
4. Berns, G. S., and Sejnowski, T. J. (1998). A computational model of how the basal ganglia produce sequences. J. Cogn. Neurosci. 10, 108-121. doi: 10.1162/089892998563815
5. Beste, C., Saft, C., Güntürkün, O., and Falkenstein, M. (2008). Increased cognitive functioning in symptomatic Huntington's disease as revealed by behavioral and event-related potential indices of auditory sensory memory and attention. J. Neurosci. 28, 11695-11702. doi: 10.1523/JNEUROSCI.2659-08.2008
6. Bracci, E., Centonze, D., Bernardi, G., and Calabresi, P. (2002). Dopamine excites fast-spiking interneurons in the striatum. J. Neurophysiol. 87, 2190-2194. doi: 10.1152/jn.00754.2001
7. Centonze, D., Grande, C., Usiello, A., Gubellini, P., Erbs, E., Martin, A. B., et al. (2003). Receptor subtypes involved in the presynaptic and postsynaptic actions of dopamine on striatal interneurons. J. Neurosci. 23, 6245-6254.
8. Chambers, J. M., Gurney, K., Humphries, M., and Prescott, A. (2011). "Mechanisms of choice in the primate brain: a quick look at positive feedback, " in Modelling Natural Action Selection, eds J. J. Bryson, T. J. Prescott, and A. K. Seth (Cambridge, UK: CUP), 390-420.
9. Chevalier, G., and Deniau, J. M. (1990). Disinhibition as a basic process in the expression of striatal function. Trends Neurosci. 13, 277-280. doi: 10.1016/0166-2236(90)90109-N
10. Chuhma, N., Tanaka, K. F., Hen, R., and Rayport, S. (2011). Functional connectome of the striatal medium spiny neuron. J. Neurosci. 31, 1183-1192. doi: 10.1523/JNEUROSCI.3833-10.2011
11. Czubayko, U., and Plenz, D. (2002). Fast synaptic transmission between striatal spiny projection neurons. Proc. Natl. Acad. Sci. U.S.A. 99, 15764-15769. doi: 10.1073/pnas.242428599
12. Ding, L., and Gold, J. I. (2013). The basal ganglia's contributions to perceptual decision making. Neuron 79, 640-649. doi: 10.1016/j.neuron.2013.07.042
13. Fan, M. M. Y., and Raymond, L. A. (2007). N-methyl-D-aspartate (NMDA) receptor function and excitotoxicity in Huntington's disease. Prog. Neurobiol. 81, 272-293. doi: 10.1016/j.pneurobio.2006.11.003
14. Fukai, T., and Tanaka, S. (1997). A simple neural network exhibiting selective activation of neuronal ensembles: from winner-take-all to winners-share-all. Neural Comput. 9, 77-97. doi: 10.1162/neco.1997.9.1.77
15. Fukuda, T. (2009). Network architecture of gap junction-coupled neuronal linkage in the striatum. J. Neurosci. 29, 1235-1243. doi: 10.1523/JNEUROSCI.4418-08.2009
16. Galarreta, M., and Hestrin, S. (1999). A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402, 72-75. doi: 10.1038/47029
17. Gerfen, C., Engber, T., Mahan, L., Susel, Z., Chase, T., Monsma, F., et al. (1990). D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429-1432. doi: 10.1126/science.2147780
18. Ghiglieri, V., Bagetta, V., Calabresi, P., and Picconi, B. (2012). Functional interactions within striatal microcircuit in animal models of Huntington's disease. Neuroscience 211, 165-184. doi: 10.1016/j.neuroscience.2011.06.075
19. Gittis, A. H., Nelson, A. B., Thwin, M. T., Palop, J. J., and Kreitzer, A. C. (2010). Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J. Neurosci. 30, 2223-2234. doi: 10.1523/JNEUROSCI.4870-09.2010
20. Gorelova, N., Seamans, J. K., and Yang, C. R. (2002). Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J. Neurophysiol. 88, 3150-3166. doi: 10.1152/jn.00335.2002
21. Grillner, S., Hellgren, J., Menard, A., Saitoh, K., and Wikstrom, M. A. (2005). Mechanisms for selection of basic motor programs-roles for the striatum and pallidum. Trends Neurosci. 28, 364-370. doi: 10.1016/j.tins.2005.05.004
22. Gruber, A. J., Dayan, P., Gutkin, B. S., and Solla, S. A. (2006). Dopamine modulation in the basal ganglia locks the gate to working memory. J. Comput. Neurosci. 20, 153-166. doi: 10.1007/s10827-005-5705-x
23. Gurney, K., Prescott, T. J., and Redgrave, P. (2001a). A computational model of action selection in the basal ganglia {I}: {A} new functional anatomy. Biol. Cybernet. 85, 401-410. doi: 10.1007/PL00007984
24. Gurney, K., Prescott, T. J., and Redgrave, P. (2001b). A computational model of action selection in the basal ganglia {II}: {A}nalysis and simulation of behaviour. Biol. Cybernet. 85, 411-423. doi: 10.1007/PL00007985
25. Guzman, J. N., Hernandez, A., Galarraga, E., Tapia, D., Laville, A., Vergara, R., et al. (2003). Dopaminergic modulation of axon collaterals interconnecting spiny neurons of the rat striatum. J. Neurosci. 23, 8931-8940.
26. Hartline, H. K., and Ratliff, F. (1958). Spatial summation of inhibitory influences in the eye of Limulus, and the mutual interaction of receptor units. J. Gen. Physiol. 41, 1049-1066. doi: 10.1085/jgp.41.5.1049
27. Ho, A., Sahakian, B., Brown, R., Barker, R., Hodges, J., Ané, M.-N., et al. (2003). Profile of cognitive progression in early Huntington's disease. Neurology 61, 1702-1706. doi: 10.1212/01.WNL.0000098878.47789.BD
28. Houk, J. C., and Wise, S. P. (1995). Distributed modular architectures linking basal ganglia, cerebellum, and cerebral cortex: their role in planning and controlling action. Cereb. Cortex 5, 95-110. doi: 10.1093/cercor/5.2.95
29. Humphries, M. D., and Gurney, K. (2002). The role of intra-thalamic and thalamocortical circuits in action selection. Network 13, 131-156. doi: 10.1088/0954-898X/13/1/305
30. Humphries, M. D., Lepora, N., Wood, R., and Gurney, K. (2009a). Capturing dopaminergic modulation and bimodal membrane behaviour of striatal medium spiny neurons in accurate, reduced models. Front. Comput. Neurosci. 3:26. doi: 10.3389/neuro.10.026.2009
31. Humphries, M. D., Wood, R., and Gurney, K. (2009b). Dopamine-modulated dynamic cell assemblies generated by the {GABA}ergic striatal microcircuit. Neural Netw. 22, 1174-1188. doi: 10.1016/j.neunet.2009.07.018
32. Humphries, M. D., Stewart, R. D., and Gurney, K. N. (2006). A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J. Neurosci. 26, 12921-12942. doi: 10.1523/JNEUROSCI.3486-06.2006
33. Humphries, M. D., Wood, R., and Gurney, K. (2010). Reconstructing the three-dimensional {GABA}ergic microcircuit of the striatum. PLoS Comput. Biol. 6:e1001011. doi: 10.1371/journal.pcbi.1001011
34. Izhikevich, E. M. (2003). Simple model of spiking neurons. IEEE Trans. Neural Netw. 14, 1569-1572. doi: 10.1109/TNN.2003.820440
35. Izhikevich, E. M. (2007a). Dynamical Systems in Neuroscience. Cambridge, MA: MIT Press.
36. Izhikevich, E. M. (2007b). Solving the distal reward problem through linkage of STDP and dopamine signaling. Cereb. Cortex 17, 2443-2452. doi: 10.1093/cercor/bhl152
37. Jaeger, D., Hitoshi, K., and Wilson, C. J. (1994). Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. J. Neurophysiol. 72, 2555-2558.
38. Jahr, C. E., and Stevens, C. F. (1990). A quantitative description of {NMDA} receptor-channel kinetic behavior. J. Neurosci. 10, 1830-1837.
39. Jin, X., and Costa, R. M. (2010). Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466, 457-462. doi: 10.1038/nature09263
40. Knopman, D., and Nissen, M. J. (1991). Procedural learning is impaired in Huntington's disease: evidence from the serial reaction time task. Neuropsychologia 29, 245-254. doi: 10.1016/0028-3932(91)90085-M
41. Koos, T., Tepper, J. M., and Wilson, C. J. (2004). Comparison of {IPSCs} evoked by spiny and fast-spiking neurons in the neostriatum. J. Neurosci. 24, 7916-7922. doi: 10.1523/JNEUROSCI.2163-04.2004
42. Kubota, Y., and Kawaguchi, Y. (1993). Spatial distributions of chemically identified intrinsic neurons in relation to patch and matrix compartments of rat neostriatum. J. Comp. Neurol. 332, 499-513. doi: 10.1002/cne.903320409
43. Lawrence, A. D., Sahakian, B. J., and Robbins, T. W. (1998). Cognitive functions and corticostriatal circuits: insights from Huntington's disease. Trends Cogn. Sci. 2, 379-388. doi: 10.1016/S1364-6613(98)01231-5
44. Leblois, A., Boraud, T., Meissner, W., Bergman, H., and Hansel, D. (2006). Competition between feedback loops underlies normal and pathological dynamics in the basal ganglia. J. Neurosci. 26, 3567-3583. doi: 10.1523/JNEUROSCI.5050-05.2006
45. Lester, R. A., Clements, J. D., Westbrook, G. L., and Jahr, C. E. (1990). Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346, 565-567. doi: 10.1038/346565a0
46. Mahon, S. (2000). Role of a striatal slowly inactivating potassium current in short-term facilitation of corticostriatal inputs: a computer simulation study. Learn. Mem. 7, 357-362. doi: 10.1101/lm.34800
47. Mallet, N., Ballion, B., Le Moine, C., and Gonon, F. (2006). Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J. Neurosci. 26, 3875-3884. doi: 10.1523/JNEUROSCI.4439-05.2006
48. Mao, Z.-H., and Massaquoi, S. G. (2007). Dynamics of winner-take-all competition in recurrent neural networks with lateral inhibition. IEEE Trans. Neural Netw. 18, 55-69. doi: 10.1109/TNN.2006.883724
49. Matamales, M., Bertran-Gonzalez, J., Salomon, L., Degos, B., Deniau, J.-M., Valjent, E., et al. (2009). Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS ONE 4:e4770. doi: 10.1371/journal.pone.0004770
50. Mink, J. W. (1996). The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50, 381-425. doi: 10.1016/S0301-0082(96)00042-1
51. Moyer, J. T., Wolf, J. A., and Finkel, L. H. (2007). Effects of dopaminergic modulation on the integrative properties of the ventral striatal medium spiny neuron. J. Neurophysiol. 98, 3731-3748. doi: 10.1152/jn.00335.2007
52. Nicola, S. M., Surmeier, J., and Malenka, R. C. (2000). Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu. Rev. Neurosci. 23, 185-215. doi: 10.1146/annurev.neuro.23.1.185
53. Oorschot, D. E. (1996). Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the cavalieri and optical disector methods. J. Comp. Neurol. 366, 580-599. doi: 10.1002/(SICI)1096-9861(19960318)366:4<580::AID-CNE3>3.0.CO;2-0
54. Oorschot, D. E., Lin, N., Cooper, B. H., Reynolds, J. N., Sun, H., and Wickens, J. R. (2013). Synaptic connectivity between rat striatal spiny projection neurons in vivo: unexpected multiple somatic innervation in the context of overall sparse proximal connectivity. Basal Ganglia 3, 93-108. doi: 10.1016/j.baga.2013.04.001
55. Planert, H., Szydlowski, S. N., Hjorth, J. J. J., Grillner, S., and Silberberg, G. (2010). Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways. J. Neurosci. 30, 3499-3507. doi: 10.1523/JNEUROSCI.5139-09.2010
56. Plenz, D. (2003). When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function. Trends Neurosci. 26, 436-443. doi: 10.1016/S0166-2236(03)00196-6
57. Prescott, T. J., Redgrave, P., and Gurney, K. (1999). Layered control architectures in robots and vertebrates. Adapt. Behav. 7, 99-127. doi: 10.1177/105971239900700105
58. Redgrave, P., Prescott, T. J., and Gurney, K. (1999). The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89, 1009-1023. doi: 10.1016/S0306-4522(98)00319-4
59. Surmeier, D. J., Ding, J., Day, M., Wang, Z., and Shen, W. (2007). D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci. 30, 228-235. doi: 10.1016/j.tins.2007.03.008
60. Tateno, T., Harsch, A., and Robinson, H. P. (2004). Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. J. Neurophysiol. 92, 2283-2294. doi: 10.1152/jn.00109.2004
61. Tomkins, A., Humphries, M., Beste, C., Vasilaki, E., and Gurney, K. N. (2012). How degrading networks can increase cognitive functions. ICANN 7552, 185-192. doi: 10.1007/978-3-642-33269-2_24
62. Tunstall, M. J., Oorschot, D. E., Kean, A., and Wickens, J. R. (2002). Inhibitory interactions between spiny projection neurons in the rat striatum. J. Neurophysiol. 88, 1263-1269.
63. Wickens, J. (1997). Basal ganglia: structure and computations. Network Comput. Neural Syst. 8, R77-R109. doi: 10.1088/0954-898X/8/4/001
64. Wilson, C. J., and Groves, P. M. (1980). Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular inject of horseradish peroxidase. J. Comp. Neurol. 194, 599-615. doi: 10.1002/cne.901940308
65. Yim, M. Y., Aertsen, A., and Kumar, A. (2011). Significance of input correlations in striatal function. PLoS Comput. Biol. 7:e1002254. doi: 10.1371/journal.pcbi.1002254