Experimental Brain Research

, Volume 85, Issue 3, pp 491–500 | Cite as

Responses to reward in monkey dorsal and ventral striatum

  • P. Apicella
  • T. Ljungberg
  • E. Scarnati
  • W. Schultz


The sources of input and the behavioral effects of lesions and drug administration suggest that the striatum participates in motivational processes. We investigated the activity of single striatal neurons of monkeys in response to reward delivered for performing in a go-nogo task. A drop of liquid was given each time the animal correctly executed or withheld an arm movement in reaction to a visual stimulus. Of 1593 neurons, 115 showed increased activity in response to delivery of liquid reward in both go and nogo trials. Responding neurons were predominantly located in dorsal and ventromedial parts of anterior putamen, in dorsal and ventral caudate, and in nucleus accumbens. They were twice as frequent in ventral as compared to dorsal striatal areas. Responses occurred at a median latency of 337 ms and lasted for 525 ms, with insignificant differences between dorsal and ventral striatum. Reward responses differed from activity recorded in the face area of posterior putamen which varied synchronously with individual mouth movements. Responses were directly related to delivery of primary liquid reward and not to auditory stimuli associated with it. Most of them also occurred when reward was delivered outside of the task. These results demonstrate that neurons of dorsal and particularly ventral striatum are involved in processing information concerning the attribution of primary reward.

Key words

Basal ganglia Caudate Putamen Accumbens Behavior Drinking Motivation Stimulusreward association Monkey 


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  1. Apicella, P, Scarnati E, Schultz W (1991) Tonically discharging neurons of monkey striatum respond to preparatory and rewarding stimuli. Exp Brain Res 84: 672–675Google Scholar
  2. Baleydier C, Mauguiere F (1980) The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypotheses. Brain 103: 525–554Google Scholar
  3. Blackburn JR, Phillips AG, Jakubovic A, Fibiger HC (1989) Dopamine and preparatory behavior. II. A neurochemical analysis. Behav Neurosci 103: 15–23Google Scholar
  4. Cador M, Robbins TW, Everitt BJ (1989) Involvement of the amygdala in stimulus-reward associatons: interaction with the ventral striatum. Neuroscience 30: 77–86CrossRefPubMedGoogle Scholar
  5. Crutcher MD, DeLong MR (1984a) Single cell studies of the primate putamen. I. Functional organization. Exp Brain Res 53: 233–243Google Scholar
  6. Crutcher MD, DeLong MR (1984b) Single cell studies of the primate putamen. II. Relations to direction of movement and pattern of muscular activity. Exp Brain Res 53: 244–258Google Scholar
  7. Fibiger HC, Phillips AG (1986) Reward, motivation, cognition: psychobiology of mesotelencephalic dopamine systems. In: Handbook of physiology: the nervous system IV. American Physiological Society, Bethesda, pp 647–675Google Scholar
  8. Fibiger HC, LePiane FG, Jakubovic A, Phillips AG (1987) The role of dopamine in intracranial self-stimulation of the ventral tegmental area. J Neurosci 7: 3888–3896Google Scholar
  9. Gaffan D, Harrison S (1987) Amygdalectomy and disconnection in visual learning for auditory secondary reinforcement by monkeys. J Neurosci 7: 2285–2292PubMedGoogle Scholar
  10. Gaffan EA, Gaffan D, Harrison S (1988) Disconnection of the amygdala from visual association cortex impairs visual reward association learning in monkeys. J Neurosci 8: 3144–3150Google Scholar
  11. Hikosaka O, Sakamoto M, Usui S (1989) Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J Neurophysiol 61: 814–832Google Scholar
  12. Ito, N, Ishida H, Miyakawa F, Naito H (1974) Microelectrode study of projections from the amygdaloid complex to the nucleus accumbens in the cat. Brain Res 67: 338–341Google Scholar
  13. Kimura M (1990) Behaviorally contingent property of movement-related activity of the primate putamen. J Neurophysiol 63: 1277–1296Google Scholar
  14. Künzle H (1975) Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia: an autoradiographic study in Macaca fascicularis. Brain Res 88: 195–209Google Scholar
  15. Künzle H (1977) Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp Brain Res 30: 481–492Google Scholar
  16. Liles SL (1985) Activity of neurons in putamen during active and passive movements of the wrist. J Neurophysiol 53: 217–236Google Scholar
  17. Louilot A, Taghzouti K, Simon H, LeMoal M (1989) Limbic system, basal ganglia and dopaminergic neurons. Brain Behav Evol 33: 157–161Google Scholar
  18. Markowitsch HJ, Pritzel M (1976) Reward related neurons in cat association cortex. Brain Res 111: 185–188Google Scholar
  19. Niki H, Watanabe M (1979) Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Res 171: 213–224Google Scholar
  20. Nishijo H, Ono T, Nishino H (1988) Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance. J Neurosci 8: 3570–3583Google Scholar
  21. Parent A, Mackey A, De Bellefeuille L (1983) The subcortical afferents to caudate nucleus and putamen in primate: a fluorescence retrograde double labeling study. Neuroscience 10: 1137–1150Google Scholar
  22. Rolls ET, Thorpe SJ, Maddison SP (1983) Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus. Behav Brain Res 7: 179–210Google Scholar
  23. Romo R, Schultz W (1990) Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements. J Neurophysiol 63: 592–606Google Scholar
  24. Russchen FT, Bakst I, Amaral DG, Price JL (1985) The amygdalostriatal projections in the monkey: an anterograde tracing study. Brain Res 329: 241–257Google Scholar
  25. Schneider JS (1987) Ingestion-related activity of caudate and entopeduncular neurons in the cat. Exp Neurol 95: 216–233Google Scholar
  26. Schultz W, Romo R (1988) Neuronal activity in the monkey striatum during the initiation of movements. Exp Brain Res 71: 431–436Google Scholar
  27. Selemon LD, Goldman-Rakic PS (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci 5: 776–794Google Scholar
  28. Soltysik S, Hull CD, Buchwald NA, Fekete T (1975) Single unit activity in basal ganglia of monkeys during performance of a delayed response task. Electroencephalogr Clin Neurophysiol 39: 65–78Google Scholar
  29. Spyraki C, Fibiger HC, Phillips AG (1982) Dopaminergic substrates of amphetamine-induced place preference conditioning. Brain Res 253: 185–193Google Scholar
  30. Taylor JR, Robbins TW (1984) Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacology 84: 405–412Google Scholar
  31. Thorpe SJ, Rolls ET, Maddison S (1983) The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp Brain Res 49: 93–115Google Scholar
  32. Watanabe M (1990) Prefrontal unit activity during associative learning in the monkey. Exp Brain Res 80: 296–309Google Scholar
  33. Williams GV (1989) Neuronal activity in the primate caudate nucleus and ventral striatum reflects the association between stimuli determining behavior. In: Crossman AR Sambrook MA (eds) Neural mechanisms in disorders of movement John Libbey, London, pp 63–73Google Scholar
  34. Wilson FAW, Rolls ET (1990) Neuronal responses related to reinforcement in the primate basal forebrain. Brain Res 509: 213–231Google Scholar
  35. Wise RA (1982) Neuroleptics and operant behavior: the anhedonia hypothesis. Behav Brain Sci 5: 39–87Google Scholar
  36. Yim CY, Mogenson GJ (1982) Response of nucleus accumbens neurons to amygdala stimulation and its modification by dopamine. Brain Res 239: 401–415Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • P. Apicella
    • 1
  • T. Ljungberg
    • 1
  • E. Scarnati
    • 1
  • W. Schultz
    • 1
  1. 1.Institut de Physiologie, Université de FribourgFribourgSwitzerland

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