Experiments on cats employing two different strategies of operant behavior (impulsive and self-controlled) revealed narrow and wide peaks on cross-correlation histograms of spike trains recorded from multiple neurons and the numbers of these were used to evaluate the functional connectivity of nerve cells within and between the frontal cortex and hippocampus. Functional connectivity of neurons in these brain formations were more marked in cats with self-controlled behavior than in animals with impulsive/mixed reactions. Conversely, the effects of external sources, assessed in terms of the number of wide cross-correlation histogram peaks, were greater in cats with impulsive/mixed reactions. Blockade of M-cholinoreceptors degraded the functional connectivity between neurons in and between the frontal cortex and hippocampus but increased the effects on them of external sources, i.e., other brain structures. At the level of the hippocampus, choline blockade decreased the functional connectivity of neurons in all animals, increased the effects of external sources in self-controlled animals, and had no effect on cats with impulsive/mixed reactions. These data provide evidence that functional connectivity and the associative characteristics of neuronal networks in the frontal cortex and hippocampus are decreased during the solution of complex tasks in conditions of deficiency of cholinergic transmission.
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P. V. Bukh-Viner, I. V. Volkov, and G. Kh. Merzhanova, “Spike ‘Collector’,” Zh. Vyssh. Nerv. Deyat., 40, No. 6, 1194–1199 (1990).
G. A. Grigoryan and G. Kh. Merzhanova, “Reflection of individual typological differences in different phases of the learning process and concomitant changes in dopamine transmission in the mesolimbic dopaminergic system of the brain,” Zh. Vyssh. Nerv. Deyat., 36, No. 1, 22–27 (2006).
E. P. Kuleshova, A. V. Zaleshin, E. E. Dolbakyan, G. A. Grigoryan, and G. Kh. Merzhanova, “Cooperative activity of neurons in the nucleus accumbens and frontal cortex in cats trained to choose between reinforcements of different value,” Zh. Vyssh. Nerv. Deyat., 58, No. 3, 449–457 (2008).
G. Kh. Merzhanova, “Local and disseminated neural networks and individuality,” Ros. Fiziol. Zh., 87, No. 6, 873–884 (2001).
G. Kh. Merzhanova, E. E. Merzhanova, and V. N. Khokhlova, “Interneuronal frontohippocampal interactions in cats trained to choose reinforcement quality,” Zh. Vyssh. Nerv. Deyat., 53, No. 3, 290–298 (2003).
V. N. Khokhlova, G. Kh. Merzhanova, and E. E. Dolbakyan, “Network activity of neurons in the motor and frontal cortex of the brain in trained cats on the background of systemic administration of M-cholinoreceptor blockers,” Zh. Vyssh. Nerv. Deyat., 51, No. 5, 604–616 (2001).
E. Ahissar, E. Vaadia, M. Ahissar, H. Bergman, A. Arieli, and M. Abeles, “Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context,” 257, 1412–1415 (1992).
E. H. Blaeg,Y. B. Kim, J. Kim, J.-W. Ghim, J. J. Kim, and M. W. Jung, “Learning-induced enduring changes in functional connectivity among prefrontal cortical neurons,” Neurosci., 27, No. 4, 909–918 (2007).
T. V. Bliss and T. Lomo, “Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path,” J. Physiol. (London), 232, 331–356 (1973).
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).
Ch. Constantinidis, M. N. Franowicz, and P. S. Goldman-Rakic, “Coding specificity in cortical microcircuits: A multiple-electrode analysis of primate pre-frontal cortex,” J. Neurosci., 21, No. 10, 3646–3655 (2001).
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).
P. E. Gold, “Acetylcholine modulation of neural systems involved in learning and memory,” Neurobiol. Learn. Mem., 80, 194–210 (2003).
D. Eytan, A. Minerbi, N. Ziv, and S. Marom, “Dopamine-induced dispersion of correlations between action potentials in networks of cortical neurons,” J. Neurophysiol., 92, No. 3, 1817–1824 (2004).
S. Funahashi and M. Inoue, “Neuronal interactions related to working memory processes in the primate pre-frontal cortex revealed by crosscorrelation analysis,” Cereb. Cortex., 10, No. 6, 535–551 (2000).
D. O. Hebb, The Organization of Behavior,Wiley, New York (1949).
K. L. Hoffman and B. L. McNaughton, “Coordinated reactivation of distributed memory traces in primate neocortex,” Science, 297, 2070–2073 (2002).
S. Ichihara-Takeda and S. Funahashi, “Activity of primate orbitofrontal and dorsolateral prefrontal neurons: Effect of reward schedule on taskrelated activity,” J. Cogn. Neurosci., 20, No. 4, 563–579 (2008).
G. Kh. Merzhanova, “Interneuronal cortical connections and intertrial responses in appetitive instrumental learning,” Acta Neurobiol. Exp., 57, 247–253 (1997).
C. M. Pennartz, E. Lee, J. Verheul, P. Lipa, C. A. Barnes, and B. L. McNaughton, “The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples,” J. Neurosci., 24, No. 29, 6446–6456 (2004).
D. H. Perkel, G. L. Gerstein, and G. P. Moore, “Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains,” Biophys. J., 7, 419–440 (1967).
Y. L. Qin, B. J. McNaughton,W. E. Skaggs, and C. A. Barnes, “Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles,” Phil. Trans. Roy. Soc. Lond. Biol. Sci., 352, 1525–1533 (1997).
G. J. Quirk, C. Repa, and J. E. LeDoux, “Fear conditioning enhances shortlatency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat,” Neuron, 15, 1029–1039 (1995).
F. Reinoso-Suarez, Topographischer Hirnatlas der Katze (für experimental-physiologische Untersuchungen), Darmstadt (1961).
E. V. L. Rolof, D. Harbaran, J. Micheau, B. Platt, and G. Riedel, “Dissociation of cholinergic function in spatial and procedural learning in rats,” Neurosci., 146, 875–889 (2007).
Y. Sakurai and S. Takahashi, “Dynamic synchrony of firing in the monkey prefrontal cortex during working-memory tasks,” J. Neurosci., 26, No. 40, 10141–10153 (2006).
G. Schoenbaum, A. A. Chiba, and M. Gallagher, “Changes in functional connectivity in orbitofrontal cortex and basolateral amygdala during learning and reversal training,” J. Neurosci., 20, 5179–5189 (2000).
E. Seidemann, I. Meilijson, M. Abeles, H. Bergman, and E. Vaadia, “Simultaneously recorded single units in the frontal cortex go through sequences of discrete and stable states in monkeys performing a delayed localization task,” J. Neurosci., 16, No. 2, 752–768 (1996).
W. Schultz and A. Dickinson, “Neuronal coding of prediction errors,” Ann. Rev. Neurosci., 23, 473–500 (2000).
T. Tateno,Y. Jimbo, and H. P. Robinson, “Spatio-temporal cholinergic modulation in cultured networks of rat cortical neurons: spontaneous activity,” Neurosci., 134, No. 2, 425–448 (2005).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 59, No. 6, pp. 696–706, November–December, 2009.
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Merzhanova, G.K., Dolbakyan, E.E. & Grigoryan, G.A. Functional Connectivity of Neurons in the Frontal Cortex and Hippocampus in Conditions of Cholinergic Deficit with Different Behavioral Strategies. Neurosci Behav Physi 41, 288–296 (2011). https://doi.org/10.1007/s11055-011-9415-8
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DOI: https://doi.org/10.1007/s11055-011-9415-8