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Activation of the cholinergic system of the striatum improves attention to conditioned reflex stimuli

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Abstract

Chronic experiments were performed on 16 dogs using a model of an operant defensive reflex associated with maintenance of a flexion pose to study the effects of uni-and bilateral microinjections of the acetylcholine agonist carbacholine (0.05–0.4 μg) and the choline receptor blocker scopolamine (0.5 μg) into the dorsolateral part of the head of the caudate nucleus andCM-Pf intralaminar thalamic nuclei. These experiments produced data showing that the cholinergic system of the striatum has an important role in realizing the sensory and motor components of the learned movement. Activation of the cholinergic system of the dorsal striatum led to general calming of behavior and inhibition of intersignal limb elevation and the phasic components of the movement, along with ordering and stabilizing of the pose and an increase in the tonic component of the operant response. This suggests that the cholinergic system of the striatum receives an indirect efferent output via motor structures and takes part in preparing the motor apparatus needed for transferring attention to significant stimuli. Microinjections of scopolamine had the opposite effects. Use of differential signals in the same behavioral model, along with special tests for attention, showed that the cholinergic system of the striatum plays an important role in the sensory control of attemtion. Activation of the strital cholinergic system led to a significant improvement in responses to differential signals and defensive signals of intensity 2–3 times slower than normal signals, and these changes were accompanied by clearer responses in special tests for attention. Scopolamine microinjections had the opposite effects. Carbacholine microinjections into the intralaminar thalamic nuclei potentiated the effects of cholinergic activation of the striatum. These data indicate that the dorsal striatum can be regarded not only as a parallel level of information processing, but also as a control system for passing this information to various levels of both sensory and motor structures. One important result of this type of control may be that of improving attention to significant stimuli.

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References

  1. S. V. Al'bertin, “Involvement of the dopaminergic system of the caudate nucleus in conditions of operant reflexes depending on their degree of complexity,”Fiziol. Zh. SSSR,84, No. 1, 87–94 (1985).

    Google Scholar 

  2. É. B. Arushanyan and V. A. Otellin,The Caudate Nucleus [in Russian], Nauka, Leningrad (1976).

    Google Scholar 

  3. H. Dzhed, E. Gruen, and Ch. D. Vudi, “The cholinergic dependence of the cortical neuronal mechanism underlying the Pavlovian conditioned blink reflex,”Ros. Fiziol. Zh. im. I. M. Sechenova,81, No. 11, 10–17 (1995).

    Google Scholar 

  4. V. P. Petropavlovskii, “A method for conditioned motor reflexes,”Fiziol. Zh. SSSR,17, No. 2, 217–225 (1934).

    Google Scholar 

  5. N. F. Suvorov, K. B. Shapovalova, and V. N. Shustov, “The role of the head of the caudate nucleus in the sensorimotor control various types of behavior,”Zh. Vyssh. Nerv. Deyat.,27, No. 4, 747–758 (1977).

    CAS  Google Scholar 

  6. K. B. Shapovalova, “Afferent and efferent mechanisms fo increasing the cholinergic activity of the striatum,”Ros. Fiziol. Zh. im. I. M. Sechenova,80, No. 1, 47–59 (1994).

    CAS  Google Scholar 

  7. K. B. Shapovalova, “The cholinergic system of the striatum: its role in the motor and sensory components of motor behavior. A Review,”Zh. Vyssh. Nerv. Deyat.,47, No. 2, 393–411 (1997).

    CAS  Google Scholar 

  8. K. B. Shapovalova and E. V. Pominova, “Features of the involvement of cholinergic mechanisms of the accumbens and caudate nuclei in regulating an operant defensive reflex in dogs,”Ros. Fiziol. Zh. im. I. M. Sechenova,79, No. 7, 29–40 (1993).

    CAS  Google Scholar 

  9. A. F. Yakimovskii,The Role of the Dopamin-and Enkephalinergic Systems of the Caudate Nucleus in Controlling the Activity of Conditioned Reflexes [in Russian], Author's abstract of Doctoral Dissertation, Leningrad (1984).

  10. G. E. Alexander and M. D. Crutcher, “Functional architecture of basal ganglia circuits. Neuronal substrates of parallel processing,”Trends Neurosci.,13, No. 7, 366–375 (1990).

    Google Scholar 

  11. H. Berendse and H. Groenewegen, “Organization of thalamo-striatal projections in the rat with the special emphasis on the ventral striatum,”J. Comp. Neurol.,299, No. 2, 187–228 (1990).

    Article  PubMed  CAS  Google Scholar 

  12. J. P. Bolam, B. N. Wainer, and A. Smith, “Characterization of cholinergic neurons in the rat neostriatum: a combination of choline acetyltransferase immunocytochemistry, Golgi impregnation and electron microscopy,”Neurosci.,12, No. 4, 711–712 (1984).

    Article  CAS  Google Scholar 

  13. G. Chevalier, S. Vacher, J. Deniau, and D. Albe-Fossard, “Tonic nigral control of tecto-sinal/tecto-diencephalic branched neurons: a possible implication of basal ganglia in orienting behavior,” in:Basal Ganglia. Structure and Functions, Plenum Press, New York (1984), pp. 247–259.

    Google Scholar 

  14. C. Contant, D. umbriaco, S. Garcia, K. C. Watkins, and L. Descarries, “Ultrastructural characterization of the acetylcholine innervation in adult rat neostriatum,”Neurosci.,71, No. 4, 937–947 (1996).

    Article  CAS  Google Scholar 

  15. S. B. Dunnet, B. J. Everitt, and T. W. Robbins, “The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions,”Trends Neurosci.,14, No. 11, 989–992 (1991).

    Article  Google Scholar 

  16. S. A. Eagger, R. Levy, and B. J. Sahakian, “Tacrine in Alzheimer's disease,”Lancet,337, No. 7, 989–992 (1991).

    Article  PubMed  CAS  Google Scholar 

  17. Ch. Gerfen, “The neostriatal mosaic: multiple levels of compartmental organization of the basal ganglia,”Ann. Rev. Neurosci.,15, 285–320 (1992).

    Article  PubMed  CAS  Google Scholar 

  18. J. M. Fuster, “Interotemporal units in selective visual attention and short-term memory,”J. Neurophysiol.,64, No. 4, 681–697 (1990).

    PubMed  CAS  Google Scholar 

  19. K. M. Heilman, R. T. Watson, E. Valenstein, and M. E. Goldberg, “Attention: behavioural and neural mechanisms,” in:Handbook of Physiology, Section 1:The Nervous System, Vol. 5:Higher Functions of the Brain, Part 1. V. B. Mountcastle, et al. (Eds.), Amer. Physiol. Soc., Bethesda, MA (1987), pp. 461–481.

    Google Scholar 

  20. Y. Lay and J. M. Siegel, “Pontomedullary glutamate receptors mediated locomotion and muscle tone suppression,”J. Neurosci.,11, No. 1, 29–31 (1991).

    Google Scholar 

  21. I. R. Lapper and J. P. Bolam, “Input from the frontal cortex and parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat,”Neurosci.,51, No. 3, 533–545 (1992).

    Article  CAS  Google Scholar 

  22. M. Mesulam, J. Elliot, E. Mufson, et al., “Cholinergic innervation of cortex by basal forebrain cytochemistry and cortical connections to the septal area diagonal band nucleus, nucleus basalis (substantia innominata) and hypothalamus in the rhesus monkey,”J. Comp. Neurol.,214, No. 2, 170–178 (1983).

    Article  PubMed  CAS  Google Scholar 

  23. J. L. Muir, S. B. Dunnett, T. W. Robbins, and B. J. Everitt, “Attentional functions of the forebrain cholinergic systems: effects of intraventricular hemicholinium, physostigmine, basal forebrain lesions and intracortical grafts on a multiplechoice serial reaction time task,”Exp. Brain Res.,89, No. 4, 611–622 (1992).

    PubMed  CAS  Google Scholar 

  24. D. S. Olton and K. Pang, “Interaction of neurotransmitters and neuroanatomy: it's not what you do, it's the place that you do it,” in:Neurotransmitters and Cognitive Function, E. D. Levin, et al. (eds.), Birkhauser, Boston (1992), pp. 277–286.

    Google Scholar 

  25. D. S. Olton, G. L. Wenk, R. M. Church, and W. H. Meck, “Attention and the frontal cortex as examined by simultaneous temporal processing,”Neuropsychologia,26, No. 2, 307–318 (1988).

    Article  PubMed  CAS  Google Scholar 

  26. A. Parent, “Extrinsic connections of the basal ganglia,”Trends Neurosci.,8, No. 7, 415–420 (1990).

    Google Scholar 

  27. A. Parent and L.-N. Hazrati, “Anatomical aspects of information processing in primate basal ganglia,”Trends Neurosci.,16, No. 3, 111–116 (1993).

    Article  PubMed  CAS  Google Scholar 

  28. R. Richardson and M. DeLong, “A reappraisal of the functions of the nucleus basalis of Meynert,”Trends Neurosci.,11, No. 6, 264–267 (1988).

    Article  PubMed  CAS  Google Scholar 

  29. R. Richardson and M. R. DeLong, “Functional implications of tonic and phasic activity changes in nucleus basalis neurons. Activation to acquisition,” in:Functional Aspects of the Basal Forebrain Cholinergic System, R. T. Richardson (ed.), Birkhauser, Boston (1991), pp. 135–166.

    Google Scholar 

  30. D. L. Robinson, E. M. Bowman, and C. Kertzman, “Covert orienting of attention in macaque. II. A signal in parietal cortex to disengage attention,”Soc. Neurosci. Abstr.,17, 442 (1991).

    Google Scholar 

  31. A. Sadikot, A. Parent, and C. Francois, “Efferent connections of the centromedian and parafascicular nuclei in squirrel monkey. A PHA-L study of subcortical projection,”J. Comp. Neurol.,315, No. 2, 137–159 (1992).

    Article  PubMed  CAS  Google Scholar 

  32. K. B. Shapovalova, “Possible mechanisms of participation of the neostriatum in regulation of voluntary movement,” in:Soviet Scientific Reviews, T. Turpaev (Ed.), Harwood Academic Publ. (1993).

  33. M. Sidibe and Y. Smith, “Differential synaptic innervation of striatofugal neurones projecting to the internal or external segments of the globus pallidus by thalamic efferents in the squirrel monkey,”J. Comp. Neurol.,365, No. 4, 445–465 (1996).

    Article  PubMed  CAS  Google Scholar 

  34. M. L. Voytko, D. S. Olton, R. T. Richardson, et al., “Basal forebrain lesions in monkeys disrupt attention, but not learning and memory,”J. Neurosci. 14, No. 1, 167–186 (1994).

    PubMed  CAS  Google Scholar 

  35. J. Q. Wang and J. F. McGinty, “Muscarinic receptors regulate striatal neuropeptide gene expression in normal and amphetamine-treated rats,”Neurosci.,75, No. 1, 43–50 (1996).

    Article  CAS  Google Scholar 

  36. K. T. Watson, E. Valenstrein, and K. M. Heilman, “Thalamic neglect: the possible role of the medial thalamus and nucleus reticularis thalami in behaviour,”Arch. Neurol. 38, No. 3, 501–507 (1981).

    PubMed  CAS  Google Scholar 

  37. K. Wesnes and D. M. Warburton, “Effects of scopolamine on stimulus sensitivity and response bias in a visual vigilance task,”Neuropsychobiology,9, No. 1, 154–157 (1983).

    Article  PubMed  CAS  Google Scholar 

  38. C. J. Wilson, H. T. Chang, and S. T. Kitai, “Firing patterns and synaptic potential of identified giant aspiny interneurons in the rat neostriatum,”J. Neurosci.,10, No. 2, 508–519 (1990).

    PubMed  CAS  Google Scholar 

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  1. Laboratory for the Physiology of Higher Nervous Activity, I. P. Pavlov Institute of Physiology, Russian Academy of Sciences, 6 Makarov Bank, 199034 St., Petersburg, Russia

    K. B. Shapovalova

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Shapovalova, K.B. Activation of the cholinergic system of the striatum improves attention to conditioned reflex stimuli. Neurosci Behav Physiol 29, 493–503 (1999). https://doi.org/10.1007/BF02461141

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  • DOI: https://doi.org/10.1007/BF02461141

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