Abstract
Prefrontal damage disrupts planning, as measured by disorders of the activities of daily living (Humphreys & Forde, 1998; Shallice & Burgess, 1991). In a monkey model of this form of planning, a variant of the delayed alternation task was performed by freely moving monkeys. In a 16×16-ft. testing room, four feeders were located in the middle of each wall. In the north task, monkeys alternated between feeders: west-north-east-north-west, and so forth. In the south task, the alternation sequence was east-south-west-south-east, and so forth. Neuronal activity was recorded during walking along the eight paths, constituting the north and south tasks. To succeed, monkeys had to memorize the alternation rule and monitor both their place in the sequence and the previously made spatially directed action before deciding to walk to a new location to the left or right of the current location. Responsive dorsolateral prefrontal neurons are strikingly selective. Sustained neuronal activity reflects the spatial direction of an ongoing or upcoming response. It is important that such selective responses occur in one but not both tasks, even though the movements are exactly the same in both tasks and at each location. We suggest that selective neuronal activity is tuned through learning and reflects the fundamental units of a planning mechanism: Individual neurons encode specific components of a sequence of behavioral actions and their temporal order. Populations of such neurons represent all the steps necessary to perform the north and south tasks. The sustained activity of these neurons suggests that planning and working memory mechanisms are integrated.
Article PDF
Avoid common mistakes on your manuscript.
References
Baddeley, A. D. (1996). Exploring the central executive. Quarterly Journal of Experimental Psychology, 49A, 5–28.
Barone, P., & Joseph, J.-P. (1989). Prefrontal cortex and spatial sequencing in macaque monkey. Experimental Brain Research, 78, 447–464.
Butters, N., & Pandya, D. (1969). Retention of delayed-alternation: Effect of selective lesions of sulcus principalis. Science, 165, 1271–1273.
Carlson, S., Rama, P., Tanila, H., Linnankoski, I., & Mansikka, H. (1997). Dissociation of mnemonic coding and other functional neuronal processing in the monkey prefrontal cortex. Journal of Neurophysiology, 77, 761–774.
Cavada, C., & Goldman-Rakic, P. S. (1989). Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. Journal of Comparative Neurology, 287, 393–421.
Courtney, S. M., Ungerleider, L. G., Keil, K., & Haxby, J. V. (1997). Transient and sustained activity in a distributed neural system for human working memory. Nature, 386, 608–611.
Della Malva, C. L., Stuss, D. T., D’Alton, J., & Willmer, J. (1993). Capture errors and sequencing after frontal brain lesions. Neuropsychologia, 31, 363–372.
D’Esposito, M., & Postle, B. R. (1999). The dependence of span and delayed-response performance on prefrontal cortex. Neuropsychologia, 37, 1303–1315.
Dombrowski, S. M., Hilgetag, C. C., & Barbas, H. (2001). Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cerebral Cortex, 11, 975–988.
Friedman, H. R., & Goldman-Rakic, P. S. (1994). Coactivation of prefrontal cortex and inferior parietal cortex in working memory tasks revealed by 2DG functional mapping in the rhesus monkey. Journal of Neuroscience, 14, 2775–2788.
Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1989). Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. Journal of Neurophysiology, 61, 331–349.
Funahashi, S., Inoue, M., & Kubota, K. (1997). Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation. Behavioural Brain Research, 84, 203–223.
Fuster, J. M. (1997). The prefrontal cortex: Anatomy, physiology, and neuropsychology of the frontal lobe. New York: Raven.
Fuster, J. M., Bauer, R. H., & Jervey, J. P. (1982). Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks. Experimental Neurology, 77, 679–694.
Goldman, P. S., & Rosvold, H. E. (1970). Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. Experimental Neurology, 27, 291–304.
Goldman-Rakic, P. S. (1987). Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In J. M. Brookhart &. V. B. Mountcastle(Series Eds.) & F. Plum (Vol. Ed.), Handbook of physiology: Section 1. The nervous system: Vol. 5. Higher functions of the brain (pp. 373–417). Washington, DC: American Physiological Society.
Greenberg, P. A., & Wilson, F. A. W. (2004). Functional stability of dorsolateral prefrontal neurons. Journal of Neurophysiology, 92, 1042–1055.
Gross, C. G., & Weiskrantz, L. (1962). Evidence for dissociation of impairment on auditory discrimination and delayed response following lateral frontal lesions in monkeys.Experimental Neurology, 5, 453–476.
Humphreys, G.W., & Forde, E. M. E. (1998). Disordered action schema and action disorganization syndrome. Cognitive Neuropsychology, 15, 771–811.
Inoue, M., & Mikami, A. (2002). Delay period activity of the primate prefrontal cortex during the serial probe reproduction task. Society for Neuroscience Abstracts, 28, 676.13.
Jacobsen, C. F. (1935). Functions of the frontal association areas in primates. Archives of Neurology & Psychiatry, 33, 558–569.
Kim, B.-H., Lim, S.-L., Ryou, J.-W., & Wilson, F. A.W. (2004). Taskrelated remapping of hippocampal place fields in freely moving monkeys. Society for Neuroscience Abstracts, 30, 1007.2
Lei, Y., Sun, N., Wilson, F. A. W., Wang, X., Chen, N., Yang, J., Peng, Y., Wang, J., Tian, S., Wang, M., Miao, Y., Xhu, W., Qi, H., & Ma, Y. Y. (2004). Telemetric recordings of single neuron activity and visual scenes in monkeys walking in an open field. Journal of Neuroscience Methods, 135, 35–41.
Lepage, M., & Richer, F. (1996). Inter-response interference contributes to the sequencing deficit in frontal lobe lesions. Brain, 119, 1289–1295.
Levy, R., & Goldman-Rakic, P. S. (2000). Segregation of working memory functions within the dorsolateral prefrontal cortex. Experimental Brain Research, 133, 23–32.
Ma, Y.-Y., Ryou, J.-W., Kim, B.-H., & Wilson, F. A. W. (2003). Spatially directed movement and neuronal activity in freely moving monkeys. In S. Mori, D. G. Stuart, & M. Wiesendanger (Eds.), Brain mechanisms for the integration of posture and movement (Progress in Brain Research, Vol. 143, pp. 505–512). Amsterdam: Elsevier.
Malmo, R. B. (1942). Interference factors in delayed response in monkeys after removal of frontal lobes. Journal of Neurophysiology, 5, 295–308.
Mikami, A., Nakamura, K., & Kubota, K. (1994). Neuronal responses to photographs in the superior temporal sulcus of the rhesus monkey. Behavioural Brain Research, 60, 1–13.
Mishkin, M. (1957). Effects of small frontal lesion on delayed alternation in monkeys. Journal of Neurophysiology, 20, 615–622.
Niki, H. (1974). Prefrontal unit activity during delayed alternation in the monkey: 1. Relation to direction of response. Brain Research, 68, 185–196.
Ninokura, Y., Mushiake, H., & Tanji, J. (2003). Representation of the temporal order of visual objects in the primate lateral prefrontal cortex. Journal of Neurophysiology, 89, 2868–2873.
O’Keefe, J. (1999). Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus, 9, 352–364.
Ó Scalaidhe, S. P., Wilson, F. A.W., & Goldman-Rakic, P. S. (1999). Face selective neurons during passive viewing and working memory performance of rhesus monkeys: Evidence for intrinsic specialization of neuronal coding. Cerebral Cortex, 9, 459–475.
Petrides, M., & Milner, B. (1982). Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia, 20, 249–262.
Rajkowska, G., & Goldman-Rakic, P. S. (1995). Cytoarchitectonic definition of prefrontal areas in the normal human cortex: I. Remapping of areas 9 and 46 using quantitative criteria. Cerebral Cortex, 5, 307–322.
Schwartz, M. F., Reed, E. S., Montgomery, M. W., Palmer, C., & Mayer, M. H. (1991). The quantitative description of action disorganization after brain damage: A case study. Cognitive Neuropsychology, 8, 381–414.
Sereno, A. B., & Holzman, P. S. (1995). Antisaccades and smooth pursuit eye movements in schizophrenia. Biological Psychiatry, 37, 394–401.
Shallice, T., & Burgess, P.W. (1991). Deficits in strategy application following frontal lobe damage in man. Brain, 114, 727–741.
Sirigu, A., Cohen, L., Zalla, T., Pradat-Diehl, P., Van Eeckhout, P., Grafman, J., & Agid, Y. (1998). Distinct frontal regions for processing sentence syntax and story grammar. Cortex, 34, 771–778.
Smith, E. E., & Jonides, J. (1999). Storage and executive processes in the frontal lobes. Science, 283, 1657–1661.
Stamm, J. S. (1987). The riddle of the monkey’s delayed-response deficit has been solved. In E. Perecman(Ed.), The frontal lobes revisited (pp. 73–89). New York: IRBN Press.
Stuss, D. T., & Benson, D. F. (1986). The frontal lobes. New York: Raven.
Taube, J. S. (1998). Head direction cells and the neurophysiological basis for a sense of direction. Progress in Neurobiology, 55, 225–256.
Thompson-Schill, S. L., Jonides, J., Marschuetz, C., Smith, E. E., D’Esposito, M., Kan, I. P., Knight, R. T., & Swick, D. (2002). Effects of frontal lobe damage on interference effects in working memory. Cognitive, Affective, & Behavioral Neuroscience, 2, 109–120.
Wilson, F. A. W., Ma, Y.-Y., Greenberg, P. A., Ryou, J.-W., & Kim, B.-H. (2003). A microelectrode drive for long-term recording of neurons in freely moving and chaired monkeys. Journal of Neuroscience Methods, 27, 49–61.
Wilson, F. A. W., Greenberg, P. A., Seok, B., & Ma, Y.-Y. (2004). Learning-related responses in go/no-go neurons in dorsolateral prefrontal cortex. Society for Neuroscience Abstracts, 32, 324.5.
Wilson, F. A.W., Kim, B.-H., Ryou, J.-W., & Ma, Y.-Y. (in press). An automated food-delivery system for behavioral and neurophysiological studies of learning and memory in freely moving monkeys. Behavior Research Methods, Instruments, & Computers.
Zanini, S., Rumiati, R. I., & Shallice, T. (2002). Action sequencing deficit following frontal lobe lesion. Neurocase, 8, 88–99.
Author information
Authors and Affiliations
Corresponding author
Additional information
This research was supported by Whitehall Foundation Grant A89-04 and NIH Grant MH58415.
Rights and permissions
About this article
Cite this article
Ryou, JW., Wilson, F.A.W. Making your next move: Dorsolateral prefrontal cortex and planning a sequence of actions in freely moving monkeys. Cognitive, Affective, & Behavioral Neuroscience 4, 430–443 (2004). https://doi.org/10.3758/CABN.4.4.430
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.3758/CABN.4.4.430