Functional territories in primate substantia nigra pars reticulata separately signaling stable and flexible values

Journal of Neurophysiology

Volumn 113, Issue 6, 2015, Pages 1681-1696

  Yasuda, Masaharu ^a   Hikosaka, Okihide ^a  

^a NATIONAL EYE INSTITUTE   (United States)

Author keywords

Caudate nucleus; Monkey; Reward; Saccade; Superior colliculus

Indexed keywords

ARTICLE; BASAL GANGLION; CAUDATE NUCLEUS; CONTROLLED STUDY; ELECTROSTIMULATION; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA PARS RETICULATA; SUPERIOR COLLICULUS; ANIMAL; CONNECTOME; CYTOLOGY; NERVE CELL INHIBITION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE;

ANIMALS; CONNECTOME; MACACA MULATTA; MALE; NEURAL INHIBITION; NEURONS; PARS RETICULATA; PSYCHOMOTOR PERFORMANCE;

EID: 84930855719     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00674.2014     Document Type: Article

References (72)

1. Anderson BA, Yantis S. Value-driven attentional and oculomotor capture during goal-directed, unconstrained viewing. Atten Percept Psychophys 74: 1644–1653, 2012.
2. Apicella P, Scarnati E, Ljungberg T, Schultz W. Neuronal activity in monkey striatum related to the expectation of predictable environmental events. J Neurophysiol 68: 945–960, 1992.
3. Basso MA, Wurtz RH. Neuronal activity in substantia nigra pars reticulata during target selection. J Neurosci 22: 1883–1894, 2002.
4. Beckstead RM, Frankfurter A. The distribution and some morphological features of substantia nigra neurons that project to the thalamus, superior colliculus and pedunculopontine nucleus in the monkey. Neuroscience 7: 2377–2388, 1982.
5. Bichot NP, Schall JD. Effects of similarity and history on neural mechanisms of visual selection. Nat Neurosci 2: 549–554, 1999.
6. Bromberg-Martin ES, Hikosaka O, Nakamura K. Coding of task reward value in the dorsal raphe nucleus. J Neurosci 30: 6262–6272, 2010.
7. Caan W, Perrett DI, Rolls ET. Responses of striatal neurons in the behaving monkey. 2. Visual processing in the caudal neostriatum. Brain Res 290: 53–65, 1984.
8. Cowan N. The magical number 4 in short-term memory: a reconsideration of mental storage capacity. Behav Brain Sci 24: 87–114; discussion 114–185, 2001.
9. Cowan WM, Powell TP. Strio-pallidal projection in the monkey. J Neurol Neurosurg Psychiatry 29: 426–439, 1966.
10. Della Libera C, Chelazzi L. Learning to attend and to ignore is a matter of gains and losses. Psychol Sci 20: 778–784, 2009.
11. DeLong MR. Activity of pallidal neurons during movement. J Neurophysiol 34: 414–427, 1971.
12. Fernandez-Ruiz J, Wang J, Aigner TG, Mishkin M. Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum. Proc Natl Acad Sci U S A 98: 4196–4201, 2001.
13. Francois C, Percheron G, Yelnik J. Localization of nigrostriatal, nigrothalamic and nigrotectal neurons in ventricular coordinates in macaques. Neuroscience 13: 61–76, 1984.
14. Francois C, Percheron G, Yelnik J, Heyner S. A histological atlas of the macaque (Macaca mulatta) substantia nigra in ventricular coordinates. Brain Res Bull 14: 349–367, 1985.
15. Francois C, Yelnik J, Percheron G, Fenelon G. Topographic distribution of the axonal endings from the sensorimotor and associative striatum in the macaque pallidum and substantia nigra. Exp Brain Res 102: 305–318, 1994.
16. Graybiel AM. Habits, rituals, and the evaluative brain. Annu Rev Neurosci 31: 359–387, 2008.
17. Graybiel AM. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 13: 244–254, 1990.
18. Grillner S, Hellgren J, Menard A, Saitoh K, Wikstrom MA. Mechanisms for selection of basic motor programs–roles for the striatum and pallidum. Trends Neurosci 28: 364–370, 2005.
19. Handel A, Glimcher PW. Quantitative analysis of substantia nigra pars reticulata activity during a visually guided saccade task. J Neurophysiol 82: 3458–3475, 1999.
20. Hayhoe M, Ballard D. Eye movements in natural behavior. Trends Cogn Sci 9: 188–194, 2005.
21. Henderson JM. Human gaze control during real-world scene perception. Trends Cogn Sci 7: 498–504, 2003.
22. Hikosaka O, Nakamura K, Nakahara H. Basal ganglia orient eyes to reward. J Neurophysiol 95: 567–584, 2006.
23. Hikosaka O, Sakamoto M, Miyashita N. Effects of caudate nucleus stimulation on substantia nigra cell activity in monkey. Exp Brain Res 95: 457–472, 1993.
24. Hikosaka O, Sakamoto M, Usui S. Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J Neurophysiol 61: 814–832, 1989.
25. Hikosaka O, Takikawa Y, Kawagoe R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80: 953–978, 2000.
26. Hikosaka O, Wurtz RH. Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J Neurophysiol 49: 1230–1253, 1983a.
27. Hikosaka O, Wurtz RH. Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J Neurophysiol 49: 1285–1301, 1983b.
28. Hikosaka O, Yamamoto S, Yasuda M, Kim HF. Why skill matters. Trends Cogn Sci 17: 434–441, 2013.
29. Hong S, Hikosaka O. Dopamine-mediated learning and switching in corticostriatal circuit explain behavioral changes in reinforcement learning. Front Behav Neurosci 5: 15, 2011.
30. Johansson RS, Westling G, Bäckström A, Flanagan JR. Eye-hand coordination in object manipulation. J Neurosci 21: 6917–6932, 2001.
31. Just MA, Carpenter PA. Eye fixations and cognitive processes. Cogn Psychol 8: 441–480, 1976.
32. Karabelas AB, Moschovakis AK. Nigral inhibitory termination on efferent neurons of the superior colliculus: an intracellular horseradish peroxidase study in the cat. J Comp Neurol 239: 309–329, 1985.
33. Kawagoe R, Takikawa Y, Hikosaka O. Expectation of reward modulates cognitive signals in the basal ganglia. Nat Neurosci 1: 411–416, 1998.
34. Kermadi I, Joseph JP. Activity in the caudate nucleus of monkey during spatial sequencing. J Neurophysiol 74: 911–933, 1995.
35. Kim B, Basso MA. A probabilistic strategy for understanding action selection. J Neurosci 30: 2340–2355, 2010.
36. Kim HF, Hikosaka O. Distinct basal ganglia circuits controlling behaviors guided by flexible and stable values. Neuron 79: 1001–1010, 2013.
37. Kimura M. Behaviorally contingent property of movement-related activity of the primate putamen. J Neurophysiol 63: 1277–1296, 1990.
38. Kording KP, Wolpert DM. Bayesian decision theory in sensorimotor control. Trends Cogn Sci 10: 319–326, 2006.
39. Land MF. Eye movements and the control of actions in everyday life. Prog Retin Eye Res 25: 296–324, 2006.
40. Land MF, Hayhoe M. In what ways do eye movements contribute to everyday activities? Vision Res 41: 3559–3565, 2001.
41. Matsumura M, Kojima J, Gardiner TW, Hikosaka O. Visual and oculomotor functions of monkey subthalamic nucleus. J Neurophysiol 67: 1615h–1632, 1992.
42. McNamara JM, Green RF, Olsson O. Bayes’ theorem and its applications in animal behaviour. Oikos 112: 243–251, 2006.
43. Mink JW. The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50: 381–425, 1996.
44. Miyashita K, Rand MK, Miyachi S, Hikosaka O. Anticipatory saccades in sequential procedural learning in monkeys. J Neurophysiol 76: 1361–1366, 1996.
45. Parent A, Bouchard C, Smith Y. The striatopallidal and striatonigral projections: two distinct fiber systems in primate. Brain Res 303: 385–390, 1984.
46. Parent A, Mackey A, Smith Y, Boucher R. The output organization of the substantia nigra in primate as revealed by a retrograde double labeling method. Brain Res Bull 10: 529–537, 1983.
47. Peck CJ, Jangraw DC, Suzuki M, Efem R, Gottlieb J. Reward modulates attention independently of action value in posterior parietal cortex. J Neurosci 29: 11182–11191, 2009.
48. Precht W, Yoshida M. Blockage of caudate-evoked inhibition of neurons in the substantia nigra by picrotoxin. Brain Res 32: 229–233, 1971.
49. Rolls ET, Thorpe SJ, Maddison SP. Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus. Behav Brain Res 7: 179–210, 1983.
50. Saint-Cyr JA, Ungerleider LG, Desimone R. Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey. J Comp Neurol 298: 129–156, 1990.
51. Saleem KS, Logothetis NK. A Combined MRI and Histology Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates. London: Academic, 2007.
52. Samejima K, Ueda Y, Doya K, Kimura M. Representation of action-specific reward values in the striatum. Science 310: 1337–1340, 2005.
53. Sato M, Hikosaka O. Role of primate substantia nigra pars reticulata in reward-oriented saccadic eye movement. J Neurosci 22: 2363–2373, 2002.
54. Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1–27, 1998.
55. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science 275: 1593–1599, 1997.
56. Seitz AR, Kim D, Watanabe T. Rewards evoke learning of unconsciously processed visual stimuli in adult humans. Neuron 61: 700–707, 2009.
57. Shiffrin RM, Schneider W. Controlled and automatic human information processing. II. Perceptual learning, automatic attending, and a general theory. Psychol Rev 84: 127–190, 1977.
58. Smith Y, Parent A. Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus). Neuroscience 18: 347–371, 1986.
59. Sparks DL. The brainstem control of saccadic eye movements. Nat Rev Neurosci 3: 952–964, 2002.
60. Szabo J. The course and distribution of efferents from the tail of the caudate nucleus in the monkey. Exp Neurol 37: 562–572, 1972.
61. Szabo J. Projections from the body of the caudate nucleus in the rhesus monkey. Exp Neurol 27: 1–15, 1970.
62. Tanibuchi I, Kitano H, Jinnai K. Substantia nigra output to prefrontal cortex via thalamus in monkeys. I. Electrophysiological identification of thalamic relay neurons. J Neurophysiol 102: 2933–2945, 2009.
63. Theeuwes J, Belopolsky AV. Reward grabs the eye: oculomotor capture by rewarding stimuli. Vision Res 74: 80–85, 2012.
64. Treisman AM, Gelade G. A feature-integration theory of attention. Cogn Psychol 12: 97–136, 1980.
65. Turner RS, Anderson ME. Context-dependent modulation of movementrelated discharge in the primate globus pallidus. J Neurosci 25: 2965–2976, 2005.
66. Yamamoto S, Kim HF, Hikosaka O. Reward value-contingent changes of visual responses in the primate caudate tail associated with a visuomotor skill. J Neurosci 33: 11227–11238, 2013.
67. Yamamoto S, Monosov IE, Yasuda M, Hikosaka O. What and where information in the caudate tail guides saccades to visual objects. J Neurosci 32: 11005–11016, 2012.
68. Yarbus AL. Eye Movements and Vision. New York: Plenum, 1967.
69. Yasuda M, Yamamoto S, Hikosaka O. Robust representation of stable object values in the oculomotor basal ganglia. J Neurosci 32: 16917–16932, 2012.
70. Yelnik J, Francois C, Percheron G, Heyner S. Golgi study of the primate substantia nigra. I. Quantitative morphology and typology of nigral neurons. J Comp Neurol 265: 455–472, 1987.
71. Yin HH, Knowlton BJ. The role of the basal ganglia in habit formation. Nat Rev Neurosci 7: 464–476, 2006.
72. Yoshida M, Precht W. Monosynaptic inhibition of neurons of the substantia nigra by caudato-nigral fibers. Brain Res 32: 225–228, 1971.