Properties of Neurons in External Globus Pallidus Can Support Optimal Action Selection

PLoS Computational Biology

Volumn 12, Issue 7, 2016, Pages

  Bogacz, Rafal ^a   Martin Moraud, Eduardo ^a   Abdi, Azzedine ^b,c   Magill, Peter J ^a   Baufreton, Jérôme ^b,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN;

ACTION SELECTION; BASAL GANGLIA; BASAL GANGLIA CIRCUITS; CELL TYPES; COMPUTATIONAL MODELLING; GLOBUS PALLIDUS; OPTIMAL ACTIONS; PROPERTY; RESPONSE PROPERTIES; SUBTHALAMIC NUCLEUS;

NEURONS;

GLOBUS PALLIDUS; NERVE CELL; POPULATION MODEL; PREDICTION; PROBABILITY; SUBTHALAMIC NUCLEUS; BIOLOGICAL MODEL; BIOLOGY; CYTOLOGY; PHYSIOLOGICAL FEEDBACK; PHYSIOLOGY;

COMPUTATIONAL BIOLOGY; FEEDBACK, PHYSIOLOGICAL; GLOBUS PALLIDUS; MODELS, NEUROLOGICAL; NEURONS;

EID: 84980047553     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1005004     Document Type: Article

References (56)

1. Redgrave P, Prescott TJ, Gurney K, The basal ganglia: a vertebrate solution to the selection problem?Neuroscience1999; 89: 1009–1023. 10362291
2. Kita H, Globus pallidus external segment. Prog Brain Res2007; 160: 111–133. 17499111
3. Smith Y, Bevan MD, Shink E, Bolam JP, Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience1998; 86: 353–387. 9881853
4. Frank MJ, Seeberger LC, O'Reilly R C, By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science2004; 306: 1940–1943. 15528409
5. Gurney K, Prescott TJ, Redgrave P, A computational model of action selection in the basal ganglia. I. A new functional anatomy. Biol Cybern2001; 84: 401–410. 11417052
6. Humphries MD, Stewart RD, Gurney KN, A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J Neurosci2006; 26: 12921–12942. 17167083
7. Berns GS, Sejnowski TJ, Damasio A, Damasio H, Christen Y, How the basal ganglia make decisions. In: Neurobiology of decision making. Berlin: Springer-Verlag; 1996. pp. 101–114.
8. Berns GS, Sejnowski TJ, A computational model of how the basal ganglia produce sequences. J Cogn Neurosci1998; 10: 108–121. 9526086
9. Bogacz R, Gurney K, The basal ganglia and cortex implement optimal decision making between alternative actions. Neural Computation2007; 19: 442–477. 17206871
10. Bogacz R, Larsen T, Integration of reinforcement learning and optimal decision-making theories of the basal ganglia. Neural Comput2011; 23: 817–851. doi: 10.1162/NECO_a_0010321222528
11. Ditterich J, A Comparison between Mechanisms of Multi-Alternative Perceptual Decision Making: Ability to Explain Human Behavior, Predictions for Neurophysiology, and Relationship with Decision Theory. Front Neurosci2010; 4: 184. doi: 10.3389/fnins.2010.0018421152262
12. Lepora NF, Gurney KN, The basal ganglia optimize decision making over general perceptual hypotheses. Neural Comput2012; 24: 2924–2945. doi: 10.1162/NECO_a_0036022920846
13. Baum CW, Veeravalli VV, A sequential procedure for multihypothesis testing. IEEE Transactions on Information Theory1994; 40: 1996–2007.
14. Dragalin VP, Tertakovsky AG, Veeravalli VV, Multihypothesis sequential probability ratio tests–part I: asymptotic optimality. IEEE Transactions on Information Theory1999; 45: 2448–2461.
15. McMillen T, Holmes P, The dynamics of choice among multiple alternatives. Journal of Mathematical Psychology2006; 50: 30–57.
16. Ma WJ, Beck JM, Latham PE, Pouget A, Bayesian inference with probabilistic population codes. Nat Neurosci2006; 9: 1432–1438. 17057707
17. Wei W, Rubin JE, Wang XJ, Role of the indirect pathway of the basal ganglia in perceptual decision making. J Neurosci2015; 35: 4052–4064. doi: 10.1523/JNEUROSCI.3611-14.201525740532
18. Dodson PD, Larvin JT, Duffell JM, Garas FN, Doig NM, et al. Distinct developmental origins manifest in the specialized encoding of movement by adult neurons of the external globus pallidus. Neuron2015; 86: 501–513. doi: 10.1016/j.neuron.2015.03.00725843402
19. Abdi A, Mallet N, Mohamed FY, Sharott A, Dodson PD, et al. Prototypic and Arkypallidal Neurons in the Dopamine-Intact External Globus Pallidus. Journal of Neuroscience2015; 35: 6667–6688. doi: 10.1523/JNEUROSCI.4662-14.201525926446
20. Mallet N, Micklem BR, Henny P, Brown MT, Williams C, et al. Dichotomous organization of the external globus pallidus. Neuron2012; 74: 1075–1086. doi: 10.1016/j.neuron.2012.04.02722726837
21. Mallet N, Pogosyan A, Marton LF, Bolam JP, Brown P, et al. Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J Neurosci2008; 28: 14245–14258. doi: 10.1523/JNEUROSCI.4199-08.200819109506
22. O'Reilly RC, Munataka Y, Computational Explorations in Cognitive Neuroscience. Cambridge, MA: MIT Press; 2000.
23. Alexander GE, DeLong MR, Strick PL, Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci1986; 9: 357–381. 3085570
24. Gold JI, Shadlen MN, Neural computations that underlie decisions about sensory stimuli. Trends Cogn Sci2001; 5: 10–16. 11164731
25. Gold JI, Shadlen MN, Banburismus and the brain: decoding the relationship between sensory stimuli, decisions, and reward. Neuron2002; 36: 299–308. 12383783
26. Zhang J, Bogacz R, Optimal decision making on the basis of evidence represented in spike trains. Neural Computation2010; 22: 1113–1148. doi: 10.1162/neco.2009.05-09-102520028228
27. Parent A, Hazrati LN, Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev1995; 20: 128–154. 7711765
28. Hallworth NE, Wilson CJ, Bevan MD, Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. J Neurosci2003; 23: 7525–7542. 12930791
29. Wilson CJ, Weyrick A, Terman D, Hallworth NE, Bevan MD, A model of reverse spike frequency adaptation and repetitive firing of subthalamic nucleus neurons. J Neurophysiol2004; 91: 1963–1980. 14702332
30. Bevan MD, Wilson CJ, Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci1999; 19: 7617–7628. 10460267
31. Beurrier C, Bioulac B, Hammond C, Slowly inactivating sodium current (I(NaP)) underlies single-spike activity in rat subthalamic neurons. J Neurophysiol2000; 83: 1951–1957. 10758106
32. Carpenter RH, Williams ML, Neural computation of log likelihood in control of saccadic eye movements. Nature1995; 377: 59–62. 7659161
33. Bugaysen J, Bronfeld M, Tischler H, Bar-Gad I, Korngreen A, Electrophysiological characteristics of globus pallidus neurons. PLoS One2010; 5: e12001. doi: 10.1371/journal.pone.001200120700458
34. Deister CA, Chan CS, Surmeier DJ, Wilson CJ, Calcium-activated SK channels influence voltage-gated ion channels to determine the precision of firing in globus pallidus neurons. J Neurosci2009; 29: 8452–8461. doi: 10.1523/JNEUROSCI.0576-09.200919571136
35. Nambu A, Llinas R, Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol1994; 72: 1127–1139. 7807199
36. Nevado-Holgado AJ, Mallet N, Magill PJ, Bogacz R, Effective connectivity of the subthalamic nucleus-globus pallidus network during Parkinsonian oscillations. J Physiol2014; 592: 1429–1455. doi: 10.1113/jphysiol.2013.25972124344162
37. Kita H, Chang HT, Kitai ST, Pallidal inputs to subthalamus: intracellular analysis. Brain Res1983; 264: 255–265. 6303502
38. Nakanishi H, Kita H, Kitai ST, Electrical membrane properties of rat subthalamic neurons in an in vitro slice preparation. Brain Res1987; 437: 35–44. 3427481
39. Kita H, Kitai ST, Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res1991; 564: 296–305. 1810628
40. Nevado-Holgado AJ, Terry JR, Bogacz R, Conditions for the generation of beta oscillations in the subthalamic nucleus-globus pallidus network. J Neurosci2010; 30: 12340–12352. doi: 10.1523/JNEUROSCI.0817-10.201020844130
41. Pavlides A, Hogan SJ, Bogacz R, Improved conditions for the generation of beta oscillations in the subthalamic nucleus—globus pallidus network. Eur J Neurosci2012; 36: 2229–2239. doi: 10.1111/j.1460-9568.2012.08105.x22805067
42. Levesque M, Parent A, The striatofugal fiber system in primates: a reevaluation of its organization based on single-axon tracing studies. Proc Natl Acad Sci U S A2005; 102: 11888–11893. 16087877
43. Pasupathy A, Miller EK, Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature2005; 433: 873–876. 15729344
44. Doya K, Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr Opin Neurobiol2000; 10: 732–739. 11240282
45. Mink JW, The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol1996; 50: 381–425. 9004351
46. Frank MJ, Samanta J, Moustafa AA, Sherman SJ, Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science2007; 318: 1309–1312. 17962524
47. Engel AK, Fries P, Beta-band oscillations—signalling the status quo?Curr Opin Neurobiol2010; 20: 156–165. doi: 10.1016/j.conb.2010.02.01520359884
48. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, et al. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci2001; 21: 1033–1038. 11157088
49. Ramanathan S, Tkatch T, Atherton JF, Wilson CJ, Bevan MD, D2-like dopamine receptors modulate SKCa channel function in subthalamic nucleus neurons through inhibition of Cav2.2 channels. J Neurophysiol2008; 99: 442–459. 18094105
50. Cooper AJ, Stanford IM, Dopamine D2 receptor mediated presynaptic inhibition of striatopallidal GABA(A) IPSCs in vitro. Neuropharmacology2001; 41: 62–71. 11445186
51. Hernandez A, Ibanez-Sandoval O, Sierra A, Valdiosera R, Tapia D, et al. Control of the subthalamic innervation of the rat globus pallidus by D2/3 and D4 dopamine receptors. J Neurophysiol2006; 96: 2877–2888. 16899633
52. Baufreton J, Bevan MD, D2-like dopamine receptor-mediated modulation of activity-dependent plasticity at GABAergic synapses in the subthalamic nucleus. J Physiol2008; 586: 2121–2142. doi: 10.1113/jphysiol.2008.15111818292127
53. Fan KY, Baufreton J, Surmeier DJ, Chan CS, Bevan MD, Proliferation of external globus pallidus-subthalamic nucleus synapses following degeneration of midbrain dopamine neurons. J Neurosci2012; 32: 13718–13728. doi: 10.1523/JNEUROSCI.5750-11.201223035084
54. Chu HY, Atherton JF, Wokosin D, Surmeier DJ, Bevan MD, Heterosynaptic regulation of external globus pallidus inputs to the subthalamic nucleus by the motor cortex. Neuron2015; 85: 364–376. doi: 10.1016/j.neuron.2014.12.02225578364
55. Chan CS, Glajch KE, Gertler TS, Guzman JN, Mercer JN, et al. HCN channelopathy in external globus pallidus neurons in models of Parkinson's disease. Nat Neurosci2011; 14: 85–92. doi: 10.1038/nn.269221076425
56. Miguelez C, Morin S, Martinez A, Goillandeau M, Bezard E, et al. Altered pallido-pallidal synaptic transmission leads to aberrant firing of globus pallidus neurons in a rat model of Parkinson's disease. J Physiol2012; 590: 5861–5875. doi: 10.1113/jphysiol.2012.24133122890706