In behavioral experiments, cats placed in a situation of choosing between a high-value time-delayed and a low-value rapid food reinforcement elected to wait for the preferred reward (they demonstrated “selfcontrol”) or to obtain the worse reward quickly (they demonstrated impulsive behavior). On the basis of the selected behavioral strategy, the cats were divided into three groups – “impulsive,” “ambivalent,” and “self-controlled.” Cross-correlation analysis was used to assess the linked activity of cells in the nucleus accumbens, which reflects the nature of interactions between close-lying neurons. In cats with self-control, interneuronal interactions appeared in a significantly larger proportion of cases than in impulsive cats. In combinations resulting in long-latency reactions, cats with self-controlled and impulsive behavior showed no significant difference in the occurrence frequency of interneuronal interactions. The numbers of interneuronal interactions were greater during erroneous responses as compared with correctly performed reactions in animals of the different groups. These data indicate a key role for the interrelated activity of nucleus accumbens neurons in organizing the pattern of long-latency responses typical of selfcontrolled behavior.
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P. B. Bukh-Viner, I. V. Volkov, and G. Kh. Merzhanova, “Spike ‘Collector’,” Zh. Vyssh. Nerv. Deyat., 40, No. 6, 1194–1199 (1990).
G. A. Grigor’yan and G. Kh. Merzhanova, “Reflection of individual typological differences in various phases of the learning process and accompanying changes in dopamine transmission in the mesolimbic system of the brain,” Zh. Vyssh. Nerv. Deyat., 56, No. 1, 22–37 (2006).
G. Kh. Merzhanova, “Local and distributed neural networks and individuality,” Ros. Fiziol. Zh., 87, No. 6, 873–884 (2001).
G. Kh. Merzhanova, É. E. Dolbakyan, and V. I. Khokhlova, “Organization of frontohippocampal neural networks in cats during different types of voluntary behavior,” Zh. Vyssh. Nerv. Deyat., 54, No. 4, 508–518 (2004).
I. A. Smirnitskaya, A. A. Frolov, and G. Kh. Merzhanova, “A model for reward selection based on reinforcement learning theory,” Zh. Vyssh. Nerv. Deyat., 57, No. 2, 133–143 (2007).
M. Abeles and Y. Prut, “Spatio-temporal firing patterns in the frontal cortex of behaving monkeys,” J. Physiol. (France), 90. No. 3–4, 249–250 (1996).
H. Bergman, A. Feingold, A. Nini, A. Raz, H. Slovin, M. Abeles, and E. Vaadia, “Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates,” Trends Neurosci., 21, 32–38 (1998).
R. N. Cardinal, “Neural systems implicated in delayed and probabilistic reinforcement,” Neural Netw., 19, No. 8, 1277–1301 (2006).
K. P. Datla, R. G. Ahier, A. M. Young, J. A. Gray, and M. H. Joseph, “Conditioned appetitive stimulus increases extracellular dopamine in the nucleus accumbens of the rat,” Eur. J. Neurosci., 16, No. 10, 1987–1993 (2002).
J. J. Day, R. A. Wheeler, M. F. Roitman, and R. M. Carelli, “Nucleus accumbens neurons encode Pavlovian approach behaviors: evidence from an autoshaping paradigm,” Eur. J. Neurosci., 23, No. 5, 1341–1351 (2006).
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, 491–569 (1999).
I. E. Espinosa and G. L. Gerstein, “Cortical auditory neuron interactions during presentation of 3-tone sequences: effective connectivity,” Brain Res., 450, No. 1–2, 39–50 (1988).
J. L. Evenden, “Varieties of impulsivity,” Psychopharmacology, 146, 348–361 (1999).
U. G. Gassanov, G. Kh. Merzhanova, and A. G. Galashina, “Interneuronal relations within and between cortical areas during conditioning in cats,” Behav. Brain Res., 15, 137–146 (1985).
J. E. Mazur, “Choice, delay, probability and conditioned reinforcement,” Anim. Learn. Behav., 25, 131–147 (1997).
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).
J. P. Moore, J. P. Segundo, G. H. Perkel, and H. Levitan, “Statistical signs of synaptic interaction in neurons,” Biophys. J., 10, No. 9, 876–900 (1970).
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).
F. Reinoso-Suarez, Topographischer Hirnatlas der Katze (Für experimental-physiologische Untersuchungen), Herausgegeben von A. Merck, Darmstadt (1961).
J. B. Richards, S. H. Mitchell, H. de Wit, and L. S. Seiden, “Determination of discount functions in rats with an adjustingamount procedure,” J. Exptl. Anal. Behav., 67, No. 3, 353–366 (1997).
Y. Sakurai, “How do cell assemblies encode information in the brain?” Neurosci. Biobehav. Rev., 23, No. 6, 785–796 (1999).
I. D. Salamone, M. Correa, A. Farrar, and S. M. Mingote, “Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits,” Psychopharmacology (Berlin), 191, No. 3, 461–482 (2007).
W. Schultz and A. Dickinson, “Neuronal coding of prediction errors,” Ann. Rev. Neurosci., 23, 473–500 (2000).
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).
K. Toyama, “The structure-functional problem in visual-cortical circuitry studied by cross-correlation techniques and multi-channel recording,” in: Neuronal Cooperativity, J. Kruger (ed.), Springer-Verlag, Berlin (1991).
S. Tsujimoto and T. Sawaguchi, “Neuronal activity representing temporal prediction of reward in the primate prefrontal cortex,” Neurophysiology, 93, No. 6, 3687–3692 (2005).
E. Vaadia, E. Ahissar, H. Bergman, and Y. Lavner, “Correlated activity of neurons: a neural code for higher brain functions,” in: Neuronal Cooperativity, J. Kruger (ed.), Springer-Verlag, Berlin (1991), pp. 249–276.
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, 1203–1222 (2006).
D. I. Wilson and E. M. Bowman, “Rat nucleus accumbens neurons predominantly respond to the outcome-related properties of conditioned stimuli rather than their behavioral-switching properties,” J. Neurophysiol., 94, No. 1, 49–61 (2005).
A. M. Young, “Increased extracellular dopamine in nucleus accumbens in response to unconditioned and conditioned aversive stimuli: studies using 1 min microdialysis in rats,” J. Neurosci. Meth., 138, No. 1–2, 57–63 (2004).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 58, No. 2, pp. 172–182, March–April, 2008.
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Kuleshova, E.P., Dolbakyan, É.E., Grigor’yan, G.A. et al. Organization of Interneuronal Connections in the Nucleus Accumbens in “Impulsive” and “Self-Controlled” Behavior in Cats. Neurosci Behav Physi 39, 387–394 (2009). https://doi.org/10.1007/s11055-009-9138-2
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DOI: https://doi.org/10.1007/s11055-009-9138-2