WJNS  Vol.4 No.4 , August 2014
Coherent Neuron Activity in Frontal Cortex, n. Accumbens and dorsomedial Striatum during Impulsive and Self-control Behavior in Cats
Cats placed in the situation of a choosing between a high-value time-delayed and a low-value immediate food rewards elected to wait for the preferred reward or to obtain the worse reward quickly. On the basis of the selected behavior strategy the cats were classified into three groups - self-control ones, choosing predominantly a delayed high-value food reward, impulsive, choosing predominantly an immediate low-value food reward, and ambivalent - with mixed types of reactions. The correlated firing between simultaneously recorded neurons in prefrontal cortex (PFC), n. accumbens (NAcb) and dorsomedial striatum (DMStr) during choice behavior task was studied. It was revealed that a total number of NAcb functional neuron interactions at cats showing self-control reactions exceeded that of observed at ambivalent and impulsive cats. The number of PFC and DMStr functional correlated firing at impulsive and ambivalent cats was more significant than at cats capable to self-control. Observed correlated firing between PFC and NAcb neurons (fronto-accumbal interactions) progressively increased with the shift of behavior to impulsiveness and decreased with self-control behavior. Our results demonstrate that performance of impulsive and self-control behavior alters the correlation structure of neural firing in PFC, NAcb, DMStr and suggest the key role of local PFC, NAcb, DMStr networks in realization of choice behavior.

Cite this paper
Merzhanova, G. , Kuleshova, E. , Sidorina, V. , Zaleshin, A. and Gerasimova, Y. (2014) Coherent Neuron Activity in Frontal Cortex, n. Accumbens and dorsomedial Striatum during Impulsive and Self-control Behavior in Cats. World Journal of Neuroscience, 4, 341-352. doi: 10.4236/wjns.2014.44039.
[1]   Day, J.J., Wheeler, R.A., Roitman, M.F. and Carelli, R.M. (2006) Nucleus Accumbens Neurons Encode Pavlovian Approach Behaviors: Evidence from an Autoshaping Paradigm. European Journal of Neuroscience, 23, 1341-1351.

[2]   Nakamura, K., Roesch, M.R. and Olson, C.R. (2005) Neuronal Activity in Macaque SEF and ACC during Performance of Tasks Involving Conflict. Journal of Neurophysiology, 93, 884-908.

[3]   Nicola, S.M. (2007) The Nucleus Accumbens as Part of a Basal Ganglia Action Selection Circuit. Psychopharmacology, 191, 521-550. http://dx.doi.org/10.1007/s00213-006-0510-4

[4]   Tsujimoto, S. and Sawaguchi, T. (2005) Neuronal Activity Representing Temporal Prediction of Reward in the Primate Prefrontal Cortex. Neurophysiology, 93, 3687-3692. http://dx.doi.org/10.1152/jn.01149.2004

[5]   Watanabe, K., Igaki, S. and Funahashi, S. (2006) Contributions of Prefrontal Cue-, Delay-, and Response-Period Activity to the Decision Process of Saccade Direction in a Free-Choice ODR Task. Neural Networks, 19, 1203-1222.

[6]   Espinosa, I.E. and Gerstein, G.L. (1988) Cortical Auditory Neuron Interactions during Presentation of 3-Tone Sequences: Effective Connectivity. Brain Research, 450, 39-50. http://dx.doi.org/10.1016/0006-8993(88)91542-9

[7]   Vaadia, E., Ahissar, E., Bergman, H. and Lavner, Y. (1991) Correlated Activity of Neurons: A Neural Code for Higher Brain Functions? Neuronal Сooperativity, 49, 249-276.

[8]   Qi, X.L. and Constantinidis, C. (2012) Correlated Discharges in the Primate Prefrontal Cortex before and after Working Memory Training. European Journal of Neuroscience, 36, 3538-3548.

[9]   Qi, X.L. and Constantinidis, C. (2013) Neural Changes after Training to Perform Cognitive Tasks. Behavioural Brain Research, 241, 235-243. http://dx.doi.org/10.1016/j.bbr.2012.12.017

[10]   Gassanov, U.G., Merzhanova, G.Kh. and Galashina, A.G. (1985) Interneuronal Relations within and between Cortical Areas during Conditioning in Cats. Behavioural Brain Research, 15, 137-146.

[11]   Merzhanova, G.Kh. (1985) Activity of Cortical Three-Neuronal Microsystems in Cats at Conditioned Switch-Over. I.P. Pavlov Journal of Higher Nervous Activity (Cited as Zh. Vyssh. Nerv. Deiat. I. P. Pavlova), 35, 435-441.

[12]   Merzhanova, G.Kh. (2003) Local and Distributed Neural Networks and Individuality. Neuroscience and Behavioral Physiology, 33, 163-170. http://dx.doi.org/10.1023/A:1021773914978

[13]   Sakurai, Y. (1999) How Do Cell Assemblies Encode Information in the Brain? Neuroscience & Biobehavioral Reviews, 23, 785-796. http://dx.doi.org/10.1016/S0149-7634(99)00017-2

[14]   Cardinal R.N. (2006) Neural Systems Implicated in Delayed and Probabilistic Reinforcement. Neural Networks, 19, 1277-1301. http://dx.doi.org/10.1016/j.neunet.2006.03.004

[15]   Depue, R.A. and Collins, P.F. (1999) Neurobiology of the Structure of Personality: Dopamine, Facilitation of Incentive Motivation, and Extraversion. Behavioral and Brain Sciences, 22, 491-569.

[16]   Evenden, J.L. (1999) Varieties of Impulsivity. Psychopharmacology, 146, 348-361.

[17]   Miyazaki, K., Miyazaki, K.W. and Matsumoto, G. (2004) Different Representation of Forthcoming Reward in Nucleus Accumbens and Medial Prefrontal Cortex. Neuroreport, 15, 721-726.

[18]   Mogenson, G.J. and Yang, C.R. (1991) The Contribution of Basal Forebrain to Limbic—Motor Integration and the Mediation of Motivation to Action. Advances in Experimental Medicine and Biology, 295, 267-290.

[19]   Salamone, I.D., Correa, M., Farrar, A. and Mingote, S.M. (2007) Effort-Related Functions of Nucleus Accumbens Dopamine and Associated Forebrain Circuits. Psychopharmacology, 191, 461-482.

[20]   Schultz, W. (2010) Subjective Neuronal Coding of Reward: Temporal Value Discounting and Risk. European Journal of Neuroscience, 31, 2124–2135. http://dx.doi.org/10.1111/j.1460-9568.2010.07282.x

[21]   Schultz, W. and Dickinson, A. (2000) Neuronal Coding of Prediction Errors. Annual Review of Neuroscience, 23, 473-500. http://dx.doi.org/10.1146/annurev.neuro.23.1.473

[22]   Cohen, M.R. and Maunsell, J.H. (2009) Attention Improves Performance Primarily by Reducing Interneuronal Correlations. Nature Neuroscience, 12, 1594-1600. http://dx.doi.org/10.1038/nn.2439

[23]   Cohen, M.R. and Maunsell, J.H. (2011) Using Neuronal Populations to Study the Mechanisms Underlying Spatial and Feature Attention. Neuron, 70, 1192-1204. http://dx.doi.org/10.1016/j.neuron.2011.04.029

[24]   Cohen, M.R. and Kohn, A. (2011) Measuring and Interpreting Neuronal Correlations. Nature Neuroscience, 14, 811-819. http://dx.doi.org/10.1038/nn.2842

[25]   Merzhanova, G.Kh., Kuleshova, E.P. and Grigiryan, G.G. (2006) Assessment of “Impulsive” Behavior by the Method with Calculation of Time. I.P. Pavlov Journal of Higher Nervous Activity (Cited as Zh. Vyssh. Nerv. Deiat. I. P. Pavlova), 56, 805-812.

[26]   Mazur, J.E. (1997) Choice, Delay, Probability and Conditioned Reinforcement. Animal Learning & Behavior, 25, 131-147. http://dx.doi.org/10.3758/BF03199051

[27]   Reinoso-Suarez, F. (1961) Topographischer Hirnatlas der Katze, fur Experimental-Physiologische Untersuchungen. Merck, Darmstadt.

[28]   Buch-Wiener, P.V., Volkov, I.V. and Merzhanova, G.K. (1990) “Collector” of Spikes. I.P. Pavlov Journal of Higher Nervous Activity (Cited as Zh. Vyssh. Nerv. Deiat. I. P. Pavlova), 40, 1194-1199.

[29]   Graham, K. and Duffin, J. (1981) Cross Correlation of Medullary Expiratory Neurons in the Cat. Experimental Neurology, 73, 451-464. http://dx.doi.org/10.1016/0014-4886(81)90279-X

[30]   Abeles, M. and Prut, Y. (1996) Spatiotemporal Firing Patterns in the Frontal Cortex of Behaving Monkeys. Journal of Physiology, 90, 249-250.

[31]   Moore, G.P., Segundo, J.P., Perkel, D.H. and Levitan, H. (1970) Statistical Signs of Synaptic Interaction in Neurons. Biophysical Journal, 10, 876-900. http://dx.doi.org/10.1016/S0006-3495(70)86341-X

[32]   Bolam, J.P., Hanley, J.J., Booth, P.A. and Bevan, M.D. (2000) Synaptic Organization of the Basal Ganglia. Journal of Anatomy, 196, 527-542. http://dx.doi.org/10.1046/j.1469-7580.2000.19640527.x

[33]   Kawaguchi, Y., Wilson, C.J., Augood, S.J. and Emson, P.C. (1995) Striatal Interneurones: Chemical, Physiological and Morphological Characterization. Trends in Neurosciences, 18, 527-535.

[34]   Bracci, E., Centonze, D., Bernardi, G. and Calabresi, P. (2003) Voltage-Dependent Membrane Potential Oscillations of Rat Striatal Fast-Spiking Interneurons. Journal of Physiology, 549, 121-130.

[35]   Hidaka, S. and Totterdell, S. (2001) Ultrastructural Features of the Nitric Oxide Synthase-Containing Interneurons in the Nucleus Accumbens and Their Relationship with Tyrosine Hydroxylase-Containing Terminals. Journal of Comparative Neurology, 431, 139-154.

[36]   Taverna, S., van Dongen, Y.C., Groenewegen, H.J. and Pennartz, C.M. (2004) Direct Physiological Evidence for Synaptic Connectivity between Medium-Sized Spiny Neurons in Rat Nucleus Accumbens in Situ. Journal of Neurophysiology, 91, 1111-1121. http://dx.doi.org/10.1152/jn.00892.2003

[37]   Chuhma, N., Zhang, H., Masson, J., Zhuang, X., Sulzer, D., Hen, R. and Rayport, S. (2004) Dopamine Neurons Mediate a Fast Excitatory Signal via Their Glutamatergic Synapses. Neuroscience, 24, 972-981.

[38]   Floresco, S.B., Tse, M.T. and Ghods-Sharifi, S. (2008) Dopaminergic and Glutamatergic Regulation of Effort-and Delay-Based Decision Making. Neuropsychopharmacology, 33, 1966-1979.

[39]   Gorelova, N., Seamans, J.K. and Yang, C.R. (2002) Mechanisms of Dopamine Activation of Fast-Spiking Interneurons that Exert Inhibition in Rat Prefrontal Cortex. Journal of Neurophysiology, 88, 3150-3166.

[40]   Hjelmstad, G.O. (2004) Dopamine Excites Nucleus Accumbens Neurons through the Differential Modulation of Glutamate and GABA Release. Neuroscience, 24, 8621-8628.

[41]   Datla, K.P., Ahier, R.G., Young, A.M., Gray, J.A. and Joseph, M.H. (2002) Conditioned Appetitive Stimulus Increases Extracellular Dopamine in the Nucleus Accumbens of the Rat. European Journal of Neuroscience, 16, 1987-1993.

[42]   Gruber, A.J., Solla, S.A., Surmeier, D.J. and Houk, J.C. (2003) Modulation of Striatal Single Units by Expected Reward: A Spiny Neuron Model Displaying Dopamine-Induced Bistability. Journal of Neurophysiology, 90, 1095-1114. http://dx.doi.org/10.1152/jn.00618.2002

[43]   Homayoun, H. and Moghaddam, B. (2009) Differential Representation of Pavlovian-Instrumental Transfer by Prefrontal Cortex Subregions and Striatum. European Journal of Neuroscience, 29, 1461-1476.

[44]   Koene, R.A. and Hasselmo, M.E. (2005) An Integrate-and-Fire Model of Prefrontal Cortex Neuronal Activity during Performance of Goal-Directed Decision Making. Cerebral Cortex, 15, 1964-1981.

[45]   St Onge, J.R., Ahn, S., Phillips, A.G. and Floresco, S.B. (2012) Dynamic Fluctuations in Dopamine Efflux in the Prefrontal Cortex and Nucleus Accumbens during Risk-Based Decision Making. Journal of Neuroscience, 32, 16880-16891. http://dx.doi.org/10.1523/JNEUROSCI.3807-12.2012

[46]   Bandyopadhyay, S. and Hablitz, J.J. (2007) Dopaminergic Modulation of Local Network Activity in Rat Prefrontal Cortex. Journal of Neurophysiology, 97, 4120-4128. http://dx.doi.org/10.1152/jn.00898.2006

[47]   Kroner, S., Krimer, L.S., Lewis, D.A. and Barrionuevo, G. (2007) Dopamine Increases Inhibition in the Monkey Dorsolateral Prefrontal Cortex through Cell Type-Specific Modulation of Interneurons. Cerebral Cortex, 17, 1020-1032.

[48]   Schoenbaum, G., Chiba, A.A. and Gallanger, M. (2000) Changes in Functional Connectivity in Orbitofrontal Cortex and Basolateral Amygdala during Learning and Reversal Training. Journal of Neuroscience, 20, 5179-5189.

[49]   Zeeb, F.D. and Winstanley, C.A. (2013) Functional Disconnection of the Orbitofrontal Cortex and Basolateral Amygdale Impairs Acquisition of a Rat Gambling Task and Disrupts Animals’ Ability to Alter Decision-Making Behavior after Reinforcer Devaluation. Journal of Neuroscience, 33, 6434-6443.