Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Inhibitory Pedunculopontine Neurons Gate Dopamine-Mediated Motor Actions of Unsigned Valence

Author(s): Sirin Zhang, Juan Mena-Segovia and Nadine K. Gut*

Volume 22, Issue 9, 2024

Published on: 11 September, 2023

Page: [1540 - 1550] Pages: 11

DOI: 10.2174/1570159X21666230911103520

Price: $65

Abstract

Background: The pedunculopontine nucleus (PPN) maintains a bidirectional connectivity with the basal ganglia that supports their shared roles in the selection and execution of motor actions. Previous studies identified a role for PPN neurons in goal-directed behavior, but the cellular substrates underlying this function have not been elucidated. We recently revealed the existence of a monosynaptic GABAergic input from the PPN that inhibits dopamine neurons of the substantia nigra. Activation of this pathway interferes with the execution of learned motor sequences when the actions are rewarded, even though the inhibition of dopamine neurons did not shift the value of the action, hence suggesting executive control over the gating of behavior.

Objective: To test the attributes of the inhibition of dopamine neurons by the PPN in the context of goal-directed behavior regardless of whether the outcome is positively or negatively reinforced.

Methods: We delivered optogenetic stimulation to PPN GABAergic axon terminals in the substantia nigra during a battery of behavioral tasks with positive and negative valence.

Results: Inhibition of dopamine neurons by PPN optogenetic activation during an appetitive task impaired the initiation and overall execution of the behavioral sequence without affecting the consumption of reward. During an active avoidance task, the same activation impaired the ability of mice to avoid a foot shock, but their escape response was unaffected. In addition, responses to potential threats were significantly attenuated.

Conclusion: Our results show that PPN GABAergic neurons modulate learned, goal-directed behavior of unsigned valence without affecting overall motor behavior.

« Previous Next »
Graphical Abstract

[1]
Marsden, C.D. The mysterious motor function of the basal ganglia: The Robert Wartenberg Lecture. Neurology, 1982, 32(5), 514-539.
[http://dx.doi.org/10.1212/WNL.32.5.514] [PMID: 7200209]
[2]
Yin, H.H. The basal ganglia in action. Neuroscientist, 2017, 23(3), 299-313.
[http://dx.doi.org/10.1177/1073858416654115] [PMID: 27306757]
[3]
Hikosaka, O.; Kim, H.F.; Yasuda, M.; Yamamoto, S. Basal ganglia circuits for reward value-guided behavior. Annu. Rev. Neurosci., 2014, 37(1), 289-306.
[http://dx.doi.org/10.1146/annurev-neuro-071013-013924] [PMID: 25032497]
[4]
Dudman, J.T.; Krakauer, J.W. The basal ganglia: From motor commands to the control of vigor. Curr. Opin. Neurobiol., 2016, 37, 158-166.
[http://dx.doi.org/10.1016/j.conb.2016.02.005] [PMID: 27012960]
[5]
Redgrave, P.; Rodriguez, M.; Smith, Y.; Rodriguez-Oroz, M.C.; Lehericy, S.; Bergman, H.; Agid, Y.; DeLong, M.R.; Obeso, J.A. Goal-directed and habitual control in the basal ganglia: Implications for Parkinson’s disease. Nat. Rev. Neurosci., 2010, 11(11), 760-772.
[http://dx.doi.org/10.1038/nrn2915] [PMID: 20944662]
[6]
Hikosaka, O.; Ghazizadeh, A.; Griggs, W.; Amita, H. Parallel basal ganglia circuits for decision making. J. Neural Transm. (Vienna), 2018, 125(3), 515-529.
[http://dx.doi.org/10.1007/s00702-017-1691-1] [PMID: 28155134]
[7]
Schultz, W. Reward functions of the basal ganglia. J. Neural Transm. (Vienna), 2016, 123(7), 679-693.
[http://dx.doi.org/10.1007/s00702-016-1510-0] [PMID: 26838982]
[8]
Rice, M.E.; Patel, J.C.; Cragg, S.J. Dopamine release in the basal ganglia. Neuroscience, 2011, 198, 112-137.
[http://dx.doi.org/10.1016/j.neuroscience.2011.08.066] [PMID: 21939738]
[9]
Haber, S.N. The place of dopamine in the cortico-basal ganglia circuit. Neuroscience, 2014, 282, 248-257.
[http://dx.doi.org/10.1016/j.neuroscience.2014.10.008] [PMID: 25445194]
[10]
Jin, X.; Costa, R.M. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature, 2010, 466(7305), 457-462.
[http://dx.doi.org/10.1038/nature09263] [PMID: 20651684]
[11]
Jin, X.; Tecuapetla, F.; Costa, R.M. Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences. Nat. Neurosci., 2014, 17(3), 423-430.
[http://dx.doi.org/10.1038/nn.3632] [PMID: 24464039]
[12]
da Silva, J.A.; Tecuapetla, F.; Paixão, V.; Costa, R.M. Dopamine neuron activity before action initiation gates and invigorates future movements. Nature, 2018, 554(7691), 244-248.
[http://dx.doi.org/10.1038/nature25457] [PMID: 29420469]
[13]
Bakhurin, K.I.; Li, X.; Friedman, A.D.; Lusk, N.A.; Watson, G.D.R.; Kim, N.; Yin, H.H. Opponent regulation of action performance and timing by striatonigral and striatopallidal pathways. eLife, 2020, 9, e54831.
[http://dx.doi.org/10.7554/eLife.54831] [PMID: 32324535]
[14]
Kravitz, A.V.; Freeze, B.S.; Parker, P.R.L.; Kay, K.; Thwin, M.T.; Deisseroth, K.; Kreitzer, A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature, 2010, 466(7306), 622-626.
[http://dx.doi.org/10.1038/nature09159] [PMID: 20613723]
[15]
Bartholomew, R.A.; Li, H.; Gaidis, E.J.; Stackmann, M.; Shoemaker, C.T.; Rossi, M.A.; Yin, H.H. Striatonigral control of movement velocity in mice. Eur. J. Neurosci., 2016, 43(8), 1097-1110.
[http://dx.doi.org/10.1111/ejn.13187] [PMID: 27091436]
[16]
Schultz, W.; Dayan, P.; Montague, P.R. A neural substrate of prediction and reward. Science, 1997, 275(5306), 1593-1599.
[http://dx.doi.org/10.1126/science.275.5306.1593] [PMID: 9054347]
[17]
Watabe-Uchida, M.; Eshel, N.; Uchida, N. Neural circuitry of reward prediction error. Annu. Rev. Neurosci., 2017, 40(1), 373-394.
[http://dx.doi.org/10.1146/annurev-neuro-072116-031109] [PMID: 28441114]
[18]
Lerner, T.N.; Holloway, A.L.; Seiler, J.L. Dopamine, updated: Reward prediction error and beyond. Curr. Opin. Neurobiol., 2021, 67, 123-130.
[http://dx.doi.org/10.1016/j.conb.2020.10.012] [PMID: 33197709]
[19]
Cohen, J.Y.; Haesler, S.; Vong, L.; Lowell, B.B.; Uchida, N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature, 2012, 482(7383), 85-88.
[http://dx.doi.org/10.1038/nature10754] [PMID: 22258508]
[20]
Tsutsui-Kimura, I.; Matsumoto, H.; Uchida, N.; Watabe-Uchida, M. Distinct temporal difference error signals in dopamine axons in three regions of the striatum in a decision-making task. ELife, 2020, 9, e62390.
[http://dx.doi.org/10.7554/eLife.62390] [PMID: 33345774]
[21]
Parker, N.F.; Cameron, C.M.; Taliaferro, J.P.; Lee, J.; Choi, J.Y.; Davidson, T.J.; Daw, N.D.; Witten, I.B. Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target. Nat. Neurosci., 2016, 19(6), 845-854.
[http://dx.doi.org/10.1038/nn.4287] [PMID: 27110917]
[22]
Moss, M.M.; Zatka-Haas, P.; Harris, K.D.; Carandini, M.; Lak, A. Dopamine axons in dorsal striatum encode contralateral visual stimuli and choices. J. Neurosci., 2021, 41(34), 7197-7205.
[http://dx.doi.org/10.1523/JNEUROSCI.0490-21.2021] [PMID: 34253628]
[23]
Galtieri, D.J.; Estep, C.M.; Wokosin, D.L.; Traynelis, S.; Surmeier, D.J. Pedunculopontine glutamatergic neurons control spike patterning in substantia nigra dopaminergic neurons. eLife, 2017, 6, e30352.
[http://dx.doi.org/10.7554/eLife.30352] [PMID: 28980939]
[24]
Lavoie, B.; Parent, A. Pedunculopontine nucleus in the squirrel monkey: Cholinergic and glutamatergic projections to the substantia nigra. J. Comp. Neurol., 1994, 344(2), 232-241.
[http://dx.doi.org/10.1002/cne.903440205] [PMID: 7915727]
[25]
Clarke, P.B.S.; Hommer, D.W.; Pert, A.; Skirboll, L.R. Innervation of substantia nigra neurons by cholinergic afferents from pedunculopontine nucleus in the rat: Neuroanatomical and electrophysiological evidence. Neuroscience, 1987, 23(3), 1011-1019.
[http://dx.doi.org/10.1016/0306-4522(87)90176-X] [PMID: 3437988]
[26]
Gould, E.; Woolf, N.J.; Butcher, L.L. Cholinergic projections to the substantia nigra from the pedunculopontine and laterodorsal tegmental nuclei. Neuroscience, 1989, 28(3), 611-623.
[http://dx.doi.org/10.1016/0306-4522(89)90008-0] [PMID: 2710334]
[27]
Gut, N.K.; Yilmaz, D.; Kondabolu, K.; Huerta-Ocampo, I.; Mena-Segovia, J. Selective inhibition of goal-directed actions in the mesencephalic locomotor region. BioRxiv, 2022.
[http://dx.doi.org/10.1101/2022.01.18.476772]
[28]
Josset, N.; Roussel, M.; Lemieux, M.; Lafrance-Zoubga, D.; Rastqar, A.; Bretzner, F. Distinct contributions of mesencephalic locomotor region nuclei to locomotor control in the freely behaving mouse. Curr. Biol., 2018, 28(6), 884-901.e3.
[http://dx.doi.org/10.1016/j.cub.2018.02.007] [PMID: 29526593]
[29]
Roseberry, T.K.; Lee, A.M.; Lalive, A.L.; Wilbrecht, L.; Bonci, A.; Kreitzer, A.C. Cell-type-specific control of brainstem locomotor circuits by basal ganglia. Cell, 2016, 164(3), 526-537.
[http://dx.doi.org/10.1016/j.cell.2015.12.037] [PMID: 26824660]
[30]
Caggiano, V.; Leiras, R.; Goñi-Erro, H.; Masini, D.; Bellardita, C.; Bouvier, J.; Caldeira, V.; Fisone, G.; Kiehn, O. Midbrain circuits that set locomotor speed and gait selection. Nature, 2018, 553(7689), 455-460.
[http://dx.doi.org/10.1038/nature25448] [PMID: 29342142]
[31]
Dautan, D.; Kovács, A.; Bayasgalan, T.; Diaz-Acevedo, M.A.; Pal, B.; Mena-Segovia, J. Modulation of motor behavior by the mesencephalic locomotor region. Cell Rep., 2021, 36(8), 109594.
[http://dx.doi.org/10.1016/j.celrep.2021.109594] [PMID: 34433068]
[32]
Masini, D.; Kiehn, O. Targeted activation of midbrain neurons restores locomotor function in mouse models of parkinsonism. Nat. Commun., 2022, 13(1), 504.
[http://dx.doi.org/10.1038/s41467-022-28075-4] [PMID: 35082287]
[33]
Gut, N.K.; Mena-Segovia, J. Midbrain cholinergic neurons signal negative feedback to promote behavioral flexibility. Trends Neurosci., 2022, 45(7), 502-503.
[http://dx.doi.org/10.1016/j.tins.2022.04.005] [PMID: 35534340]
[34]
Dautan, D.; Huerta-Ocampo, I.; Gut, N.K.; Valencia, M.; Kondabolu, K.; Kim, Y.; Gerdjikov, T.V.; Mena-Segovia, J. Cholinergic midbrain afferents modulate striatal circuits and shape encoding of action strategies. Nat. Commun., 2020, 11(1), 1739.
[http://dx.doi.org/10.1038/s41467-020-15514-3] [PMID: 32269213]
[35]
MacLaren, D.A.A.; Markovic, T.; Clark, S.D. Assessment of sensorimotor gating following selective lesions of cholinergic pedunculopontine neurons. Eur. J. Neurosci., 2014, 40(10), 3526-3537.
[http://dx.doi.org/10.1111/ejn.12716] [PMID: 25208852]
[36]
Ruan, Y.; Li, K.Y.; Zheng, R.; Yan, Y.Q.; Wang, Z.X.; Chen, Y.; Liu, Y.; Tian, J.; Zhu, L.Y.; Lou, H.F.; Yu, Y.Q.; Pu, J.L.; Zhang, B.R. Cholinergic neurons in the pedunculopontine nucleus guide reversal learning by signaling the changing reward contingency. Cell Rep., 2022, 38(9), 110437.
[http://dx.doi.org/10.1016/j.celrep.2022.110437] [PMID: 35235804]
[37]
Xiao, C.; Cho, J.R.; Zhou, C.; Treweek, J.B.; Chan, K.; McKinney, S.L.; Yang, B.; Gradinaru, V. Cholinergic mesopontine signals govern locomotion and reward through dissociable midbrain pathways. Neuron, 2016, 90(2), 333-347.
[http://dx.doi.org/10.1016/j.neuron.2016.03.028] [PMID: 27100197]
[38]
Blaha, C.D.; Winn, P. Modulation of dopamine efflux in the striatum following cholinergic stimulation of the substantia nigra in intact and pedunculopontine tegmental nucleus-lesioned rats. J. Neurosci., 1993, 13(3), 1035-1044.
[http://dx.doi.org/10.1523/JNEUROSCI.13-03-01035.1993] [PMID: 8441002]
[39]
Dautan, D.; Souza, A.S.; Huerta-Ocampo, I.; Valencia, M.; Assous, M.; Witten, I.B.; Deisseroth, K.; Tepper, J.M.; Bolam, J.P.; Gerdjikov, T.V.; Mena-Segovia, J. Segregated cholinergic transmission modulates dopamine neurons integrated in distinct functional circuits. Nat. Neurosci., 2016, 19(8), 1025-1033.
[http://dx.doi.org/10.1038/nn.4335] [PMID: 27348215]
[40]
Yoo, J.H.; Zell, V.; Wu, J.; Punta, C.; Ramajayam, N.; Shen, X.; Faget, L.; Lilascharoen, V.; Lim, B.K.; Hnasko, T.S. Activation of pedunculopontine glutamate neurons is reinforcing. J. Neurosci., 2017, 37(1), 38-46.
[http://dx.doi.org/10.1523/JNEUROSCI.3082-16.2016] [PMID: 28053028]
[41]
Estakhr, J.; Abazari, D.; Frisby, K.; McIntosh, J.M.; Nashmi, R. Differential control of dopaminergic excitability and locomotion by cholinergic inputs in mouse substantia nigra. Curr. Biol., 2017, 27(13), 1900-1914.e4.
[http://dx.doi.org/10.1016/j.cub.2017.05.084] [PMID: 28648825]
[42]
Wilson, D.I.G.; MacLaren, D.A.A.; Winn, P. Bar pressing for food: Differential consequences of lesions to the anterior versus posterior pedunculopontine. Eur. J. Neurosci., 2009, 30(3), 504-513.
[http://dx.doi.org/10.1111/j.1460-9568.2009.06836.x] [PMID: 19614747]
[43]
MacLaren, D.A.A.; Wilson, D.I.G.; Winn, P. Updating of action–outcome associations is prevented by inactivation of the posterior pedunculopontine tegmental nucleus. Neurobiol. Learn. Mem., 2013, 102, 28-33.
[http://dx.doi.org/10.1016/j.nlm.2013.03.002] [PMID: 23567109]
[44]
Taylor, C.L.; Kozak, R.; Latimer, M.P.; Winn, P. Effects of changing reward on performance of the delayed spatial win-shift radial maze task in pedunculopontine tegmental nucleus lesioned rats. Behav. Brain Res., 2004, 153(2), 431-438.
[http://dx.doi.org/10.1016/j.bbr.2003.12.019] [PMID: 15265639]
[45]
Thompson, J.A.; Costabile, J.D.; Felsen, G. Mesencephalic representations of recent experience influence decision making. eLife, 2016, 5, e16572.
[http://dx.doi.org/10.7554/eLife.16572] [PMID: 27454033]
[46]
Okada, K.; Kobayashi, Y. Rhythmic firing of pedunculopontine tegmental nucleus neurons in monkeys during eye movement task. PLoS One, 2015, 10(6), e0128147.
[http://dx.doi.org/10.1371/journal.pone.0128147] [PMID: 26030664]
[47]
Tian, J.; Huang, R.; Cohen, J.Y.; Osakada, F.; Kobak, D.; Machens, C.K.; Callaway, E.M.; Uchida, N.; Watabe-Uchida, M. Distributed and mixed information in monosynaptic inputs to dopamine neurons. Neuron, 2016, 91(6), 1374-1389.
[http://dx.doi.org/10.1016/j.neuron.2016.08.018] [PMID: 27618675]
[48]
Skvortsova, V.; Palminteri, S.; Buot, A.; Karachi, C.; Welter, M.L.; Grabli, D.; Pessiglione, M. A causal role for the pedunculopontine nucleus in human instrumental learning. Curr. Biol., 2021, 31(5), 943-954.e5.
[http://dx.doi.org/10.1016/j.cub.2020.11.042] [PMID: 33352119]
[49]
Norton, A.B.W.; Jo, Y.S.; Clark, E.W.; Taylor, C.A.; Mizumori, S.J.Y. Independent neural coding of reward and movement by pedunculopontine tegmental nucleus neurons in freely navigating rats. Eur. J. Neurosci., 2011, 33(10), 1885-1896.
[http://dx.doi.org/10.1111/j.1460-9568.2011.07649.x] [PMID: 21395868]
[50]
Okada, K.; Toyama, K.; Inoue, Y.; Isa, T.; Kobayashi, Y. Different pedunculopontine tegmental neurons signal predicted and actual task rewards. J. Neurosci., 2009, 29(15), 4858-4870.
[http://dx.doi.org/10.1523/JNEUROSCI.4415-08.2009] [PMID: 19369554]
[51]
Hong, S.; Hikosaka, O. Pedunculopontine tegmental nucleus neurons provide reward, sensorimotor, and alerting signals to midbrain dopamine neurons. Neuroscience, 2014, 282, 139-155.
[http://dx.doi.org/10.1016/j.neuroscience.2014.07.002] [PMID: 25058502]
[52]
Pan, W.X.; Hyland, B.I. Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. J. Neurosci., 2005, 25(19), 4725-4732.
[http://dx.doi.org/10.1523/JNEUROSCI.0277-05.2005] [PMID: 15888648]
[53]
Kobayashi, Y.; Inoue, Y.; Yamamoto, M.; Isa, T.; Aizawa, H. Contribution of pedunculopontine tegmental nucleus neurons to performance of visually guided saccade tasks in monkeys. J. Neurophysiol., 2002, 88(2), 715-731.
[http://dx.doi.org/10.1152/jn.2002.88.2.715] [PMID: 12163524]
[54]
Menegas, W.; Akiti, K.; Amo, R.; Uchida, N.; Watabe-Uchida, M. Dopamine neurons projecting to the posterior striatum reinforce avoidance of threatening stimuli. Nat. Neurosci., 2018, 21(10), 1421-1430.
[http://dx.doi.org/10.1038/s41593-018-0222-1] [PMID: 30177795]
[55]
Ungless, M.A.; Argilli, E.; Bonci, A. Effects of stress and aversion on dopamine neurons: Implications for addiction. Neurosci. Biobehav. Rev., 2010, 35(2), 151-156.
[http://dx.doi.org/10.1016/j.neubiorev.2010.04.006] [PMID: 20438754]
[56]
Matsumoto, M.; Hikosaka, O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature, 2009, 459(7248), 837-841.
[http://dx.doi.org/10.1038/nature08028] [PMID: 19448610]
[57]
Tsutsui-Kimura, I.; Uchida, N.; Watabe-Uchida, M. Dynamical management of potential threats regulated by dopamine and direct- and indirect-pathway neurons in the tail of the striatum. bioRxiv, 2022.
[http://dx.doi.org/10.1101/2022.02.05.479267]
[58]
Poulin, J.F.; Caronia, G.; Hofer, C.; Cui, Q.; Helm, B.; Ramakrishnan, C.; Chan, C.S.; Dombeck, D.A.; Deisseroth, K.; Awatramani, R. Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches. Nat. Neurosci., 2018, 21(9), 1260-1271.
[http://dx.doi.org/10.1038/s41593-018-0203-4] [PMID: 30104732]
[59]
Ko, D.; Wanat, M.J. Phasic dopamine transmission reflects initiation vigor and exerted effort in an action- and region-specific manner. J. Neurosci., 2016, 36(7), 2202-2211.
[http://dx.doi.org/10.1523/JNEUROSCI.1279-15.2016] [PMID: 26888930]
[60]
Augustin, S.M.; Loewinger, G.C.; O’Neal, T.J.; Kravitz, A.V.; Lovinger, D.M. Dopamine D2 receptor signaling on iMSNs is required for initiation and vigor of learned actions. Neuropsychopharmacology, 2020, 45(12), 2087-2097.
[http://dx.doi.org/10.1038/s41386-020-00799-1] [PMID: 32811899]
[61]
Wassum, K.M.; Ostlund, S.B.; Maidment, N.T. Phasic mesolimbic dopamine signaling precedes and predicts performance of a self-initiated action sequence task. Biol. Psychiatry, 2012, 71(10), 846-854.
[http://dx.doi.org/10.1016/j.biopsych.2011.12.019] [PMID: 22305286]
[62]
Markowitz, J.E.; Gillis, W.F.; Jay, M.; Wood, J.; Harris, R.W.; Cieszkowski, R.; Scott, R.; Brann, D.; Koveal, D.; Kula, T.; Weinreb, C.; Osman, M.A.M.; Pinto, S.R.; Uchida, N.; Linderman, S.W.; Sabatini, B.L.; Datta, S.R. Spontaneous behaviour is structured by reinforcement without explicit reward. Nature, 2023, 614(7946), 108-117.
[http://dx.doi.org/10.1038/s41586-022-05611-2] [PMID: 36653449]
[63]
Beierholm, U.; Guitart-Masip, M.; Economides, M.; Chowdhury, R.; Düzel, E.; Dolan, R.; Dayan, P. Dopamine modulates reward-related vigor. Neuropsychopharmacology, 2013, 38(8), 1495-1503.
[http://dx.doi.org/10.1038/npp.2013.48] [PMID: 23419875]
[64]
Mazzoni, P.; Hristova, A.; Krakauer, J.W. Why don’t we move faster? Parkinson’s disease, movement vigor, and implicit motivation. J. Neurosci., 2007, 27(27), 7105-7116.
[http://dx.doi.org/10.1523/JNEUROSCI.0264-07.2007] [PMID: 17611263]
[65]
Mohebi, A.; Pettibone, J.R.; Hamid, A.A.; Wong, J.M.T.; Vinson, L.T.; Patriarchi, T.; Tian, L.; Kennedy, R.T.; Berke, J.D. Dissociable dopamine dynamics for learning and motivation. Nature, 2019, 570(7759), 65-70.
[http://dx.doi.org/10.1038/s41586-019-1235-y] [PMID: 31118513]
[66]
Zénon, A.; Devesse, S.; Olivier, E. Dopamine manipulation affects response vigor independently of opportunity cost. J. Neurosci., 2016, 36(37), 9516-9525.
[http://dx.doi.org/10.1523/JNEUROSCI.4467-15.2016] [PMID: 27629704]
[67]
Van Wouwe, N.C.; Claassen, D.O.; Neimat, J.S.; Kanoff, K.E.; Wylie, S.A. Dopamine selectively modulates the outcome of learning unnatural action-valence associations. J. Cogn. Neurosci., 2017, 29(5), 816-826.
[http://dx.doi.org/10.1162/jocn_a_01099] [PMID: 28129053]
[68]
Koob, G.F. Hedonic valence, dopamine and motivation. Mol. Psychiatry, 1996, 1(3), 186-189.
[PMID: 9118342]
[69]
Hamid, A.A.; Pettibone, J.R.; Mabrouk, O.S.; Hetrick, V.L.; Schmidt, R.; Vander Weele, C.M.; Kennedy, R.T.; Aragona, B.J.; Berke, J.D. Mesolimbic dopamine signals the value of work. Nat. Neurosci., 2016, 19(1), 117-126.
[http://dx.doi.org/10.1038/nn.4173] [PMID: 26595651]
[70]
Cui, G.; Jun, S.B.; Jin, X.; Pham, M.D.; Vogel, S.S.; Lovinger, D.M.; Costa, R.M. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature, 2013, 494(7436), 238-242.
[http://dx.doi.org/10.1038/nature11846] [PMID: 23354054]
[71]
Tecuapetla, F.; Jin, X.; Lima, S.Q.; Costa, R.M. Complementary contributions of striatal projection pathways to action initiation and execution. Cell, 2016, 166(3), 703-715.
[http://dx.doi.org/10.1016/j.cell.2016.06.032] [PMID: 27453468]
[72]
Syed, E.C.J.; Grima, L.L.; Magill, P.J.; Bogacz, R.; Brown, P.; Walton, M.E. Action initiation shapes mesolimbic dopamine encoding of future rewards. Nat. Neurosci., 2016, 19(1), 34-36.
[http://dx.doi.org/10.1038/nn.4187] [PMID: 26642087]
[73]
Menegas, W.; Bergan, J.F.; Ogawa, S.K.; Isogai, Y.; Umadevi Venkataraju, K.; Osten, P.; Uchida, N.; Watabe-Uchida, M. Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass. eLife, 2015, 4, e10032.
[http://dx.doi.org/10.7554/eLife.10032] [PMID: 26322384]
[74]
Akiti, K.; Tsutsui-Kimura, I.; Xie, Y.; Mathis, A.; Markowitz, J.E.; Anyoha, R.; Datta, S.R.; Mathis, M.W.; Uchida, N.; Watabe-Uchida, M. Striatal dopamine explains novelty-induced behavioral dynamics and individual variability in threat prediction. Neuron, 2022, 110(22), 3789-3804.e9.
[http://dx.doi.org/10.1016/j.neuron.2022.08.022] [PMID: 36130595]
[75]
Gangarossa, G.; Castell, L.; Castro, L.; Tarot, P.; Veyrunes, F.; Vincent, P.; Bertaso, F.; Valjent, E. Contrasting patterns of ERK activation in the tail of the striatum in response to aversive and rewarding signals. J. Neurochem., 2019, 151(2), 204-226.
[http://dx.doi.org/10.1111/jnc.14804] [PMID: 31245856]
[76]
Crego, A.C.G. Štoček, F.; Marchuk, A.G.; Carmichael, J.E.; van der Meer, M.A.A.; Smith, K.S. Complementary control over habits and behavioral vigor by phasic activity in the dorsolateral striatum. J. Neurosci., 2020, 40(10), 2139-2153.
[http://dx.doi.org/10.1523/JNEUROSCI.1313-19.2019] [PMID: 31969469]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy