Combined lesions of direct and indirect basal ganglia pathways but not changes in dopamine levels explain learning deficits in patients with Huntington's disease

European Journal of Neuroscience

Volumn 41, Issue 9, 2015, Pages 1227-1244

  Schroll, Henning ^a,b,c   Beste, Christian ^d   Hamker, Fred H ^a,c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c CHEMNITZ UNIVERSITY OF TECHNOLOGY   (Germany)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Computational modeling; Dopamine; Neurodegeneration; Stimulus response learning; Striatum

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR;

ARTICLE; BRAIN DAMAGE; COGNITIVE DEFECT; COMPUTER SIMULATION; CONTROLLED STUDY; CORPUS STRIATUM; DIRECT BASAL GANGLIA PATHWAY DAMAGE; DISEASE ASSOCIATION; DOPAMINERGIC TRANSMISSION; EFFECT SIZE; GLOBUS PALLIDUS; GLOBUS PALLIDUS EXTERNUS; GLOBUS PALLIDUS INTERNUS; HUMAN; HUNTINGTON CHOREA; INDIRECT BASAL GANGLIA PATHWAY DAMAGE; LEARNING; LEARNING DISORDER; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MATHEMATICAL MODEL; MEDIUM SPINY NEURON; MOTOR DYSFUNCTION; NEGATIVE FEEDBACK; NERVE CELL; NERVE DEGENERATION; NEUROCOMPUTATIONAL MODEL; POSITIVE FEEDBACK; PREDICTIVE VALUE; PRIORITY JOURNAL; RECEPTOR BINDING; REINFORCEMENT BASED CATEGORY LEARNING; REINFORCEMENT BASED REVERSAL LEARNING; REINFORCEMENT BASED SEQUENCE LEARNING; REPRODUCIBILITY; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; SUBSTANTIA NIGRA PARS COMPACTA; SUBTHALAMIC NUCLEUS; UNIFIED HUNTINGTON DISEASE RATING SCALE; WORKING MEMORY; BASAL GANGLION; BIOLOGICAL MODEL; METABOLISM; PATHOPHYSIOLOGY;

BASAL GANGLIA; DOPAMINE; HUMANS; HUNTINGTON DISEASE; LEARNING; MODELS, NEUROLOGICAL;

EID: 84928774882     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12868     Document Type: Article

References (56)

1. Albin, R.L., Young, A.B. & Penney, J.B. (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci., 12, 166-175.
2. Albin, R.L., Reiner, A., Anderson, K.D., Dure, L.S., Handelin, B., Balfour, R., Whetsell, B.O., Penney, J.B. & Young, A.B. (1992) Preferential loss of striato-external pallidal projection neurons in presymptomatic Huntington's disease. Ann. Neurol., 31, 425-430.
3. Alexander, G.E., Crutcher, M.D. & DeLong, M.R. (1989) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, 'prefrontal' and 'limbic' functions. Prog. Brain Res., 85, 119-146.
4. André, V.M., Cepeda, C. & Levine, M.S. (2010) Dopamine and glutamate in Huntington's disease: a balancing act. CNS Neurosci. Ther., 16, 163-178.
5. André, V.M., Fisher, Y.E. & Levine, M.S. (2011) Altered balance of activity in the striatal direct and indirect pathways in mouse models of Huntington's disease. Front. Syst. Neurosci., 5, 46.
6. Antonini, A., Leenders, K.L., Spiegel, R., Meier, D., Vontobel, P., Weigell-Weber, M., Snachez-Pernaute, R., de Yébenez, J.G., Boesiger, P., Weindl, A. & Maguire, R.P. (1996) Striatal glucose metabolism and dopamine D2 receptor binding in asymptomatic gene carriers and patients with Huntington's disease. Brain, 119, 2085-2095.
7. Antzoulatos, E.G. & Miller, E.K. (2011) Differences between neural activity in prefrontal cortex and striatum during learning of novel abstract categories. Neuron, 71, 243-249.
8. Bäckman, L., Robins-Wahlin, T.B., Lundin, A., Ginovart, N. & Farde, L. (1997) Cognitive deficits in Huntington's disease are predicted by dopaminergic PET markers and brain volumes. Brain, 120, 2207-2217.
9. Beste, C., Saft, C., Andrich, J., Müller, T., Gold, R. & Falkenstein, M. (2007) Time processing in Huntington's disease: a group-control study. PLoS One, 2, e1263.
10. Beste, C., Saft, C., Andrich, J., Gold, R. & Falkenstein, M. (2008a) Response inhibition in Huntington's disease - a study using ERPs and sLORETA. Neuropsychologia, 46, 1290-1297.
11. Beste, C., Saft, C., Andrich, J., Gold, R. & Falkenstein, M. (2008b) Stimulus-response compatibility in Huntington's disease: a cognitive-neurophysiological analysis. J. Neurophysiol., 99, 1213-1223.
12. Beste, C., Saft, C., Güntürkün, O. & Falkenstein, M. (2008c) 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.
13. Beste, C., Willemssen, R., Saft, C. & Falkenstein, M. (2010) Response inhibition subprocesses and dopaminergic pathways: basal ganglia disease effects. Neuropsychologia, 48, 366-373.
14. Beste, C., Ness, V., Falkenstein, M. & Saft, C. (2011) On the role of fronto-striatal neural synchronization processes for response inhibition - evidence from ERP phase-synchronization analyses in pre-manifest Huntington's disease gene mutation carriers. Neuropsychologia, 49, 3484-3493.
15. Beste, C., Ness, V., Lukas, C., Hoffmann, R., Stüwe, S., Falkenstein, M. & Saft, C. (2012) Mechanisms mediating parallel action monitoring in fronto-striatal circuits. NeuroImage, 62, 137-146.
16. Beste, C., Stock, A.K., Ness, V., Hoffmann, R., Lukas, C. & Saft, C. (2013) A novel cognitive-neurophysiological state biomarker in premanifest Huntington's disease validated on longitudinal data. Sci. Rep., 3, 1797.
17. Beste, C., Humphries, M. & Saft, C. (2014) Striatal disorders dissociate mechanisms of enhanced and impaired response selection - evidence from cognitive neurophysiology and computational modelling. Neuroimage Clin., 4, 623-634.
18. Braak, H. & Del Tredici, K. (2008) Cortico-basal ganglia-cortical circuitry in Parkinson's disease reconsidered. Exp. Neurol., 212, 226-229.
19. Brown, R.G., Redondo-Verge, L., Chacon, J.R., Lucas, M.L. & Channon, S. (2001) Dissociation between intentional and incidental sequence learning in Huntington's disease. Brain, 124, 2188-2202.
20. Canteras, N.S., Shammah-Lagnado, S.J., Silva, B.A. & Ricardo, J.A. (1990) Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res., 513, 43-59.
21. Delmaire, C., Dumas, E.M., Sharman, M.A., den Bogaard, S.J., Valabregue, R., Jauffret, C., Justo, D., Reilmann, R., Stout, J.C., Craufurd, D., Trabrizi, S.J., Roos, R.A.C., Durr, A. & Lehéricy, S. (2013) The structural correlates of functional deficits in early Huntington's disease. Hum. Brain Mapp., 34, 2141-2153.
22. DeLong, M.R. (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci., 13, 281-285.
23. Denny-Brown, D. (1960) Diseases of the basal ganglia: their relation to disorders of movement. Lancet, 276, 1099-1105.
24. Ehrlich, M.E. (2012) Huntington's disease and the striatal medium spiny neuron: cell-autonomous and non-cell-autonomous mechanisms of disease. Neurotherapeutics, 9, 270-284.
25. Filoteo, J.V., Maddox, W.T. & Davis, J.D. (2001) A possible role of the striatum in linear and nonlinear category learning: evidence from patients with Hungtington's disease. Behav. Neurosci., 115, 786-798.
26. Frank, M.J., Moustafa, A.A., Haughey, H.M., Curran, T. & Hutchison, K.E. (2007) Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning. Proc. Natl. Acad. Sci. USA, 104, 16311-16316.
27. Freedman, D.J., Riesenhuber, M., Poggio, T. & Miller, E.K. (2001) Categorical representation of visual stimuli in the primate prefrontal cortex. Science, 291, 312-316.
28. A receptor alterations in the human basal ganglia in Huntington's disease. Neuroscience, 97, 505-519.
29. Glimcher, P.W. (2011) Understanding dopamine and reinforcement learning: the dopamine reward prediction error hypothesis. Proc. Natl. Acad. Sci. USA, 108, 15647-15654.
30. Haber, S.N. (2003) The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat., 26, 317-330.
31. Hartmann-von Monakow, K., Akert, K. & Künzle, H. (1978) Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp. Brain Res., 33, 395-403.
32. Hazrati, L.N. & Parent, A. (1992a) Convergence of subthalamic and striatal efferents at pallidal level in primates: an anterograde double-labeling study with biocytin and PHA-L. Brain Res., 569, 336-340.
33. Hazrati, L.N. & Parent, A. (1992b) The striatopallidal projection displays a high degree of anatomical specificity in the primate. Brain Res., 592, 213-227.
34. Ho, A.K., Sahakian, B.J., Robbins, T.W., Barker, R.A., Rosser, A.E. & Hodges, J.R. (2002) Verbal fluency in Huntington's disease: a longitudinal analysis of phonemic and semantic clustering and switching. Neuropsychologia, 40, 1277-1284.
35. Lawrence, A.D., Sahakian, B.J., Rogers, R.D., Hodges, J.R. & Robbins, T.W. (1999) Discrimination, reversal, and shift learning in Huntington's disease: mechanisms of impaired response selection. Neuropsychologia, 37, 1359-1374.
36. Maia, T.V. & Frank, M.J. (2011) From reinforcement learning models to psychiatric and neurological disorders. Nat. Neurosci., 14, 154-162.
37. Montoya, A., Pelletier, M., Menear, M., Duplessis, E., Richer, F. & Lepage, M. (2006a) Episodic memory impairment in Huntington's disease: a meta-analysis. Neuropsychologia, 44, 1984-1994.
38. Montoya, A., Price, B.H., Menear, M. & Lepage, M. (2006b) Brain imaging and cognitive dysfunctions in Huntington's disease. J. Psychiatr. Neurosci., 31, 21-29.
39. O'Kusky, J.R., Nasir, J., Cicchetti, F., Parent, A. & Hayden, M.R. (1999) Neuronal degeneration in the basal ganglia and loss of pallido-subthalamic synapses in mice with targeted disruption of the Huntington's disease gene. Brain Res., 818, 468-479.
40. Peinemann, A., Schuller, S., Pohl, C., Jahn, T., Weindl, A. & Kassubek, J. (2005) Executive dysfunction in early stages of Huntington's disease is associated with striatal and insular atrophy: a neuropsychological and voxel-based morphometric study. J. Neurol. Sci., 239, 11-19.
41. Raymond, L.A., André, V.M., Cepeda, C., Gladding, C.M., Milnerwood, A.J. & Levine, M.S. (2011) Pathophysiology of Huntington's disease: time-dependent alterations in synaptic and receptor function. Neuroscience, 198, 252-273.
42. Reiner, A., Albin, R.L., Anderson, K.D., D'Amato, C.J., Penney, J.B. & Young, A.B. (1988) Differential loss of striatal projection neurons in Huntington disease. Proc. Natl. Acad. Sci. USA, 85, 5733-5737.
43. Schroll, H. & Hamker, F.H. (2013) Computational models of basal-ganglia pathway functions: focus on functional neuroanatomy. Front. Syst. Neurosci., 7, 122.
44. Schroll, H., Vitay, J. & Hamker, F.H. (2014) Dysfunctional and compensatory synaptic plasticity in Parkinson's disease. Eur. J. Neurosci., 39, 688-702.
45. Shen, W., Flajolet, M., Greengard, P. & Surmeier, D.J. (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science, 321, 848-851.
46. Smith, Y., Bevan, M.D., Shink, E. & Bolam, J.P. (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience, 86, 353.
47. Sprengelmeyer, R., Lange, H. & Hömberg, V. (1995) The pattern of attentional deficits in Huntington's disease. Brain, 118, 145-152.
48. Storey, E. & Beal, M.F. (1993) Neurochemical substrates of rigidity and chorea in Huntington's disease. Brain, 116, 1201-1222.
49. Tabrizi, S.J., Reilmann, R., Roos, R.A., Durr, A., Leavitt, B., Owen, G., Jones, R., Johnson, H., Craufurd, D., Hicks, S.L., Kennard, C., Landwehrmeyer, B., Stout, J.C., Borowsky, B., Scahill, R.I., Frost, C. & Langbehn, D.R. (2012) Potential endpoints for clinical trials in premanifest and early Huntington's disease in the TRACK-HD study: analysis of 24 month observational data. Lancet Neurol., 11, 42-53.
50. Tabrizi, S.J., Scahill, R.I., Owen, G., Durr, A., Leavitt, B.R., Roos, R.A., Borowsky, B., Landwehrmeyer, B., Frost, C., Johnson, H., Craufurd, D., Reilmann, R., Stout, J.C. & Langbehn, D.R. (2013) Predictors of phenotypic progression and disease onset in premanifest and early-stage Huntington's disease in the TRACK-HD study: analysis of 36-month observational data. Lancet Neurol., 12, 637-649.
51. Thompson, P.D., Berardelli, A., Rothwell, J.C., Day, B.L., Dick, J.P.R., Benecke, R. & Marsden, C.D. (1988) The coexistence of bradykinesia and chorea in Huntington's disease and its implications for theories of basal ganglia control of movement. Brain, 111, 223-244.
52. Tomkins, A., Vasilaki, E., Beste, C., Gurney, K. & Humphries, M.D. (2013) Transient and steady-state selection in the striatal microcircuit. Front. Comput. Neurosci., 7, 192.
53. Van Oostrom, J.C.H., Maguire, R.P., Verschuuren-Bemelmans, C.C., Veenma-Van Der Duin, L., Pruim, J., Roos, R.A.C. & Leenders, K.L. (2005) Striatal dopamine D2 receptors, metabolism, and volume in preclinical Huntington disease. Neurology, 65, 941-943.
54. Verleger, R., Schroll, H. & Hamker, F.H. (2013) The unstable bridge from stimulus processing to correct responding in Parkinson's disease. Neuropsychologia, 51, 2512-2525.
55. Waelti, P., Dickinson, A. & Schultz, W. (2001) Dopamine responses comply with basic assumptions of formal learning theory. Nature, 412, 43-48.
56. Weeks, R.A., Piccini, P., Harding, A.E. & Brooks, D.J. (1996) Striatal D1 and D2 dopamine receptor loss in asymptomatic mutation carriers of Huntington's disease. Ann. Neurol., 40, 49-54.