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Cooperative Activity of Neurons in the Nucleus Accumbens and Frontal Cortex in Cats Trained to Select Reinforcements of Different Value

Neuroscience and Behavioral Physiology volume 39, pages 741–747 (2009)Cite this article

Results obtained at the level of the organization of interneuronal interactions of cells in the nucleus accumbens and frontal cortex revealed the features of the involvement of this component in “impulsive” and “self-controlled” behavior, consisting of an increase in bidirectional interactions between the structures of interest, accompanied by simultaneous reductions in the regularity of interactions with increases in “impulsivity” and decreases in “self-control.” Long-latency reactions appearing only in “impulsive” animals were associated with decreases in the control of frontal cortex cells by the nucleus accumbens during the signal period, which correlated with the low activity of the network activity of the nucleus accumbens in these animals. Comparison of the patterns of frontal-accumbens interactions as the animals performed a single type of activity demonstrated that the connections in neuron pairs during the presignal and signal periods were similar, while significant differences in patterns were seen during the performance of different types of activity.

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References

  1. V. N. Dumenko, Baseline Electrical Activity in the Dog Neocortex in Several Integral Types of Behavior [in Russian], Naukova Dumka, Kiev (1977).

    Google Scholar 

  2. E. P. Kuleshova, É. E. Dolbakyan, G. A. Grigoryan, and G. Kh. Merzhanova, “Organization of interneuronal connections in the nucleus accumbens in ‘impulsive’ and ‘self-controlled’ behavior in cats,” Zh. Vyssh. Nerv. Deyat., 58, No. 2, 172–182 (2008).

    CAS  Google Scholar 

  3. G. Kh. Merzhanova, “Local and distributed neural networks and individuality,” Ros. Fiziol. Zh., 87, No. 6, 873–884 (2001).

    Google Scholar 

  4. G. Kh. Merzhanova, “Activity of three-neuron cortical microsystems in cats in conditioned reflex switching,” Zh. Vyssh. Nerv. Deyat., 35, No. 3, 435–441 (1985).

    Google Scholar 

  5. K. B. Shapovalova, A. I. Gorbachevskaya, and N. B. Saul’skaya, “Structural organization and neurochemical mechanisms of involvement of the nucleus accumbens in interactions with the limbic and motor systems in the regulation of motor behavior,” Zh. Vyssh. Nerv. Deyat., 42, No. 2, 226–276 (1992).

    CAS  Google Scholar 

  6. S. Ahn and A. G. Phillips, “Independent modulation of basal and feeding-evoked dopamine efflux in the nucleus accumbens and medial prefrontal cortex by the central and basolateral amygdalar nuclei in the rat,” Neurosci., 116, No. 1, 295–305 (2003).

    Article  CAS  Google Scholar 

  7. S. Bandyopadhyay and J. J. Hablitz, “Dopaminergic modulation of local network activity in rat prefrontal cortex,” J. Neurophysiol., 97, No. 6, 4120–4128 (2007).

    PubMed  Article  CAS  Google Scholar 

  8. R. N. Cardinal, C. A. Winstanley, T. W. Robbins, and B. J. Everitt, “Limbic corticostriatal systems and delayed reinforcement,” Ann. N.Y. Acad. Sci., 1021, 33–50 (2004).

    PubMed  Article  Google Scholar 

  9. H. T. Chang and S. T. Kitai, “Projection neurons of the nucleus accumbens: an intracellular labeling study,” Brain Res., 347, No. 1, 112–116 (1985).

    PubMed  Article  CAS  Google Scholar 

  10. N. Chuhma, H. Zhang, J. Masson, X. Zhuang, D. Sulzer, R. Hen, and S. J. Rayport, “Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses,” Neurosci., 24, No. 4, 972–981 (2004).

    Article  CAS  Google Scholar 

  11. R. A. Depue and P. F. Collins, “Neurobiology of the structure of personality: dopamine, facilitation of incentive motivation, and extraversion,” Behav. Brain Sci., 22, No. 3, 491–517 (1999).

    PubMed  CAS  Google Scholar 

  12. S. B. Floresco, M. T. Tse, and S. Ghods-Sharifi, “Dopaminergic and glutamatergic regulation of effort- and delay-based decision making,” Neuropsychopharmacology Advance Online Publication, September 5, 2007.

  13. D. Geldwert, J. M. Norris, I. G. Feldman, J. J. Schulman, M. P. Joyce, and S. Rayport, “Dopamine presynaptically and heterogeneously modulates nucleus accumbens medium-spiny neuron GABA synapses in vitro,” BMC Neurosci., 7, 53 (2006).

    PubMed  Article  CAS  Google Scholar 

  14. N. Gorelova, J. K. Seamans, and C. R. Yang, “Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex,” J. Neurophysiol., 88, No. 6, 3150–3166 (2002).

    PubMed  Article  CAS  Google Scholar 

  15. A. J. Gruber, S. A. Solla, D. J. Surmeier, and J. C. Houk, “Modulation of striatal single units by expected reward: a spiny neuron model displaying dopamine-induced bistability,” J. Neurophysiol., 90, No. 2, 1095–1114 (2003).

    PubMed  Article  Google Scholar 

  16. G. O. Hjelmstad, “Dopamine excites nucleus accumbens neurons through the differential modulation of glutamate and GABA release,” Neurosci., 24, No. 39, 8621–8628 (2004).

    Article  CAS  Google Scholar 

  17. H. Homayoun and B. Moghaddam, “Bursting of prefrontal cortex neurons in awake rats is regulated by metabotropic glutamate 5 (mGlu5) receptors: rate-dependent influence and interaction with NMDA receptors,” Cereb. Cortex, 16, No. 1, 93–105 (2006).

    PubMed  Article  Google Scholar 

  18. R. A. Koene and M. E. Hasselmo, “An integrate-and-fire model of prefrontal cortex neuronal activity during performance of goal-directed decision making,” Cereb. Cortex, 15, No. 12, 1964–1981 (2005).

    PubMed  Article  Google Scholar 

  19. S. Kroner, L. S. Krimer, D. A. Lewis, an G. Barrionuevo, “Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modulation of interneurons,” Cereb. Cortex, 17, No. 5, 1020–1032 (2007).

    PubMed  Article  Google Scholar 

  20. K. Miyazaki, K. W. Miyazaki, and G. Matsumoto, “Different representation of forthcoming reward in nucleus accumbens and medial prefrontal cortex,” Neuroreport, 15, No. 4, 721–726 (2004).

    PubMed  Article  Google Scholar 

  21. G. J. Morgenson and C. R. Yang, “The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action,” Adv. Exptl. Med. Biol., 295, 267–290 (1991).

    Google Scholar 

  22. K. Nakamura, M. R. Roesch, and C. R. Olson, “Neuronal activity in macaque SEF and ACC during performance of tasks involving conflict,” J. Neurophysiol., 93, No. 2, 884–908 (2005).

    PubMed  Article  Google Scholar 

  23. S. Otani, “Prefrontal cortex function, quasi-physiological stimuli, and synaptic plasticity,” J. Physiol. (France), 97, No. 4–6, 423–430 (2003).

    Google Scholar 

  24. C. M. Pennartz ad F. H. Lopes da Silva, “Muscarinic modulation of synaptic transmission in slices of the rat ventral striatum is dependent on the frequency of afferent stimulation,” Brain Res., 645. No. 1–2, 231–239 (1994).

    PubMed  Article  CAS  Google Scholar 

  25. F. Reinoso-Suarez, Topographischer Hirnatlas der Katze (Für Experimental-Physiologische Untersuchungen), Herausgegeben von E. Merck, Darmstadt (1961).

    Google Scholar 

  26. I. D. Salmona, M. Correa, A. Farrar, and S. M. I. Mingote, “Effortrelated functions of nucleus accumbens dopamine and associated forebrain circuits,” Psychopharmacology (Berlin), 191, No. 3, 461–482 (2007).

    Article  CAS  Google Scholar 

  27. W. Schultz, L. Tremblay, and J. R. Hollerman, “Changes in behavior-related neuronal activity in the striatum during learning,” Trends Neurosci., 26, No. 6, 321–328 (2003).

    PubMed  Article  CAS  Google Scholar 

  28. S. Taverna, Y. C. van Dongen, H. J. Groenewegen, and C. M. Pennartz, “Direct physiological evidence for synaptic connectivity between medium-sized spiny neurons in rat nucleus accumbens in situ,” J. Neurophysiol., 91, No. 3, 1111–1121 (2004).

    PubMed  Article  Google Scholar 

  29. S. Tsujimoto and T. Sawaguchi, “Neuronal activity representing temporal prediction of reward in the primate prefrontal cortex,” Neurophysiology, 93, No. 6, 3687–3692 (2005).

    PubMed  Article  Google Scholar 

  30. K. Watanabe, S. Igaki, and S. Funahashi, “Contributions of prefrontal cue-, delay-, and response-period activity to the decision process of saccade direction in a free-choice ODR task,” Neural Netw., 19, No. 8, 1203–1220 (2006).

    PubMed  Article  Google Scholar 

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Affiliations

  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

    E. P. Kuleshova, É. E. Dolbakyan, G. A. Grigor’yan & G. Kh. Merzhanova

  2. Moscow Physical-Technical Institute, Moscow, Russia

    A. V. Zaleshin

Authors
  1. E. P. Kuleshova
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  2. A. V. Zaleshin
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  3. É. E. Dolbakyan
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  4. G. A. Grigor’yan
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  5. G. Kh. Merzhanova
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Correspondence to G. Kh. Merzhanova.

Additional information

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 58, No. 4, pp. 449–457, July–August, 2008.

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Kuleshova, E.P., Zaleshin, A.V., Dolbakyan, É.E. et al. Cooperative Activity of Neurons in the Nucleus Accumbens and Frontal Cortex in Cats Trained to Select Reinforcements of Different Value. Neurosci Behav Physi 39, 741–747 (2009). https://doi.org/10.1007/s11055-009-9196-5

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  • DOI: https://doi.org/10.1007/s11055-009-9196-5

Key words

  • selection behavior
  • impulsivity
  • self-control
  • nucleus accumbens
  • frontal cortex
  • neuron
  • frontalaccumbens interactions