Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

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

Research Article

Two Distinct Neuronal Populations in the Rat Parafascicular Nucleus Oppositely Encode the Engagement in Stimulus-driven Reward-seeking

Author(s): Mehdi Sicre, Frederic Ambroggi and Julie Meffre*

Volume 22, Issue 9, 2024

Published on: 01 February, 2024

Page: [1551 - 1565] Pages: 15

DOI: 10.2174/1570159X22666240131114225

Price: $65

Abstract

Background: The thalamus is a phylogenetically well-preserved structure. Known to densely contact cortical regions, its role in the transmission of sensory information to the striatal complex has been widely reconsidered in recent years.

Methods: The parafascicular nucleus of the thalamus (Pf) has been implicated in the orientation of attention toward salient sensory stimuli. In a stimulus-driven reward-seeking task, we sought to characterize the electrophysiological activity of Pf neurons in rats.

Results: We observed a predominance of excitatory over inhibitory responses for all events in the task. Neurons responded more strongly to the stimulus compared to lever-pressing and reward collecting, confirming the strong involvement of the Pf in sensory information processing. The use of long sessions allowed us to compare neuronal responses to stimuli between trials when animals were engaged in action and those when they were not. We distinguished two populations of neurons with opposite responses: MOTIV+ neurons responded more intensely to stimuli followed by a behavioral response than those that were not. Conversely, MOTIV- neurons responded more strongly when the animal did not respond to the stimulus. In addition, the latency of excitation of MOTIV- neurons was shorter than that of MOTIV+ neurons.

Conclusion: Through this encoding, the Pf could perform an early selection of environmental stimuli transmitted to the striatum according to motivational level.

Keywords: Parafascicular nucleus, thalamic nuclei, PSTHs, neuronal populations, reward-seeking, MOTIV+ neurons.

Graphical Abstract
[1]
Ariens-Kappers, C.; Huber, G.; Crosby, E. The comparative anatomy of the nervous system of vertebrates, including man; Macmillan: New York, NY, 1936.
[2]
Butler, A.B. The evolution of the dorsal thalamus of jawed vertebrates, including mammals: Cladistic analysis and a new hypothesis. Brain Res. Brain Res. Rev., 1994, 19(1), 29-65.
[http://dx.doi.org/10.1016/0165-0173(94)90003-5] [PMID: 8167659]
[3]
James, M.H.; Charnley, J.L.; Levi, E.M.; Jones, E.; Yeoh, J.W.; Smith, D.W.; Dayas, C.V. Orexin-1 receptor signalling within the ventral tegmental area, but not the paraventricular thalamus, is critical to regulating cue-induced reinstatement of cocaine-seeking. Int. J. Neuropsychopharmacol., 2011, 14(5), 684-690.
[http://dx.doi.org/10.1017/S1461145711000423] [PMID: 21447232]
[4]
Rikhye, R.V.; Wimmer, R.D.; Halassa, M.M. Toward an integrative theory of thalamic function. Annu. Rev. Neurosci., 2018, 41(1), 163-183.
[http://dx.doi.org/10.1146/annurev-neuro-080317-062144] [PMID: 29618284]
[5]
Van der Werf, Y.D.; Witter, M.P.; Groenewegen, H.J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Brain Res. Rev., 2002, 39(2-3), 107-140.
[http://dx.doi.org/10.1016/S0165-0173(02)00181-9] [PMID: 12423763]
[6]
Redgrave, P.; Prescott, T.J.; Gurney, K. The basal ganglia: A vertebrate solution to the selection problem? Neuroscience, 1999, 89(4), 1009-1023.
[http://dx.doi.org/10.1016/S0306-4522(98)00319-4] [PMID: 10362291]
[7]
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]
[8]
Alexander, G.E.; DeLong, M.R.; Strick, P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci., 1986, 9(1), 357-381.
[http://dx.doi.org/10.1146/annurev.ne.09.030186.002041] [PMID: 3085570]
[9]
McHaffie, J.; Stanford, T.; Stein, B.; Coizet, V.; Redgrave, P. Subcortical loops through the basal ganglia. Trends Neurosci., 2005, 28(8), 401-407.
[http://dx.doi.org/10.1016/j.tins.2005.06.006] [PMID: 15982753]
[10]
Redgrave, P.; Vautrelle, N.; Reynolds, J.N.J. Functional properties of the basal ganglia’s re-entrant loop architecture: Selection and reinforcement. Neuroscience, 2011, 198, 138-151.
[http://dx.doi.org/10.1016/j.neuroscience.2011.07.060] [PMID: 21821101]
[11]
Redgrave, P.; Gurney, K. The short-latency dopamine signal: A role in discovering novel actions? Nat. Rev. Neurosci., 2006, 7(12), 967-975.
[http://dx.doi.org/10.1038/nrn2022] [PMID: 17115078]
[12]
Ding, J.B.; Guzman, J.N.; Peterson, J.D.; Goldberg, J.A.; Surmeier, D.J. Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron, 2010, 67(2), 294-307.
[http://dx.doi.org/10.1016/j.neuron.2010.06.017] [PMID: 20670836]
[13]
English, D.F.; Ibanez-Sandoval, O.; Stark, E.; Tecuapetla, F.; Buzsáki, G.; Deisseroth, K.; Tepper, J.M.; Koos, T. GABAergic circuits mediate the reinforcementrelated signals of striatal cholinergic interneurons. Nat. Neurosci., 2012, 15(1), 123-130.
[http://dx.doi.org/10.1038/nn.2984] [PMID: 22158514]
[14]
Doig, N.M.; Magill, P.J.; Apicella, P.; Bolam, J.P.; Sharott, A. Cortical and thalamic excitation mediate the multiphasic responses of striatal cholinergic interneurons to motivationally salient stimuli. J. Neurosci., 2014, 34(8), 3101-3117.
[http://dx.doi.org/10.1523/JNEUROSCI.4627-13.2014] [PMID: 24553950]
[15]
Mandelbaum, G.; Taranda, J.; Haynes, T.M.; Hochbaum, D.R.; Huang, K.W.; Hyun, M.; Umadevi Venkataraju, K.; Straub, C.; Wang, W.; Robertson, K.; Osten, P.; Sabatini, B.L. Distinct cortical thalamic striatal circuits through the parafascicular nucleus. Neuron, 2019, 102(3), 636-652.e7.
[http://dx.doi.org/10.1016/j.neuron.2019.02.035] [PMID: 30905392]
[16]
Matsumoto, N.; Minamimoto, T.; Graybiel, A.M.; Kimura, M. Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J. Neurophysiol., 2001, 85(2), 960-976.
[http://dx.doi.org/10.1152/jn.2001.85.2.960] [PMID: 11160526]
[17]
Bradfield, L.A.; Bertran-Gonzalez, J.; Chieng, B.; Balleine, B.W. The thalamostriatal pathway and cholinergic control of goal-directed action: Interlacing new with existing learning in the striatum. Neuron, 2013, 79(1), 153-166.
[http://dx.doi.org/10.1016/j.neuron.2013.04.039] [PMID: 23770257]
[18]
Do-Monte, F.H.; Minier-Toribio, A.; Quiñones-Laracuente, K.; Medina-Colón, E.M.; Quirk, G.J. Thalamic regulation of sucrose seeking during unexpected reward omission. Neuron, 2017, 94(2), 388-400.e4.
[http://dx.doi.org/10.1016/j.neuron.2017.03.036] [PMID: 28426970]
[19]
Díaz-Hernández, E.; Contreras-López, R.; Sánchez-Fuentes, A.; Rodríguez-Sibrían, L.; Ramírez-Jarquín, J.O.; Tecuapetla, F. The thalamostriatal projections contribute to the initiation and execution of a sequence of movements. Neuron, 2018, 100(3), 739-752.e5.
[http://dx.doi.org/10.1016/j.neuron.2018.09.052] [PMID: 30344045]
[20]
Meffre, J.; Sicre, M.; Diarra, M.; Marchessaux, F.; Paleressompoulle, D.; Ambroggi, F. Orexin in the posterior paraventricular thalamus mediates hungerrelated signals in the nucleus accumbens core. Curr. Biol., 2019, 29(19), 3298-3306.e4.
[http://dx.doi.org/10.1016/j.cub.2019.07.069] [PMID: 31543448]
[21]
Hamlin, A.S.; Clemens, K.J.; Choi, E.A.; McNally, G.P. Paraventricular thalamus mediates context induced reinstatement (renewal) of extinguished reward seeking. Eur. J. Neurosci., 2009, 29(4), 802-812.
[http://dx.doi.org/10.1111/j.1460-9568.2009.06623.x] [PMID: 19200064]
[22]
Jones, E.G.; Leavitt, R.Y. Retrograde axonal transport and the demonstration of nonspecific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J. Comp. Neurol., 1974, 154(4), 349-377.
[http://dx.doi.org/10.1002/cne.901540402] [PMID: 4132969]
[23]
Smith, Y.; Raju, D.V.; Pare, J.F.; Sidibe, M. The thalamostriatal system: A highly specific network of the basal ganglia circuitry. Trends Neurosci., 2004, 27(9), 520-527.
[http://dx.doi.org/10.1016/j.tins.2004.07.004] [PMID: 15331233]
[24]
Smith, Y.; Surmeier, D.J.; Redgrave, P.; Kimura, M. Thalamic contributions to basal ganglia related behavioral switching and reinforcement. J. Neurosci., 2011, 31(45), 16102-16106.
[http://dx.doi.org/10.1523/JNEUROSCI.4634-11.2011] [PMID: 22072662]
[25]
Berendse, H.W.; Groenewegen, H.J. Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J. Comp. Neurol., 1990, 299(2), 187-228.
[http://dx.doi.org/10.1002/cne.902990206] [PMID: 2172326]
[26]
Berendse, H.W.; Groenewegen, H.J. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience, 1991, 42(1), 73-102.
[http://dx.doi.org/10.1016/0306-4522(91)90151-D] [PMID: 1713657]
[27]
Groenewegen, H.J.; Berendse, H.W. The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei. Trends Neurosci., 1994, 17(2), 52-57.
[http://dx.doi.org/10.1016/0166-2236(94)90074-4] [PMID: 7512768]
[28]
Minamimoto, T.; Kimura, M. Participation of the thalamic CM-Pf complex in attentional orienting. J. Neurophysiol., 2002, 87(6), 3090-3101.
[http://dx.doi.org/10.1152/jn.2002.87.6.3090] [PMID: 12037210]
[29]
Kimura, M.; Minamimoto, T.; Matsumoto, N.; Hori, Y. Monitoring and switching of cortico-basal ganglia loop functions by the thalamo-striatal system. Neurosci. Res., 2004, 48(4), 355-360.
[http://dx.doi.org/10.1016/j.neures.2003.12.002] [PMID: 15041188]
[30]
Minamimoto, T.; Hori, Y.; Kimura, M. Neuroscience: Complementary process to response bias in the centromedian nucleus of the thalamus. Science, 2005, 308(5729), 1798-1801.
[31]
Minamimoto, T.; Hori, Y.; Yamanaka, K.; Kimura, M. Neural signal for counteracting preaction bias in the centromedian thalamic nucleus. Front. Syst. Neurosci., 2014, 8(JAN), 3.
[http://dx.doi.org/10.3389/fnsys.2014.00003] [PMID: 24478641]
[32]
du Hoffmann, J.; Kim, J.J.; Nicola, S.M. An inexpensive drivable cannulated microelectrode array for simultaneous unit recording and drug infusion in the same brain nucleus of behaving rats. J. Neurophysiol., 2011, 106(2), 1054-1064.
[http://dx.doi.org/10.1152/jn.00349.2011] [PMID: 21613588]
[33]
Sicre, M.; Meffre, J.; Louber, D.; Ambroggi, F. The nucleus accumbens core is necessary for responding to incentive but not instructive stimuli. J. Neurosci., 2020, 40(6), 1332-1343.
[http://dx.doi.org/10.1523/JNEUROSCI.0194-19.2019] [PMID: 31862857]
[34]
Ghazizadeh, A.; Fields, H.L.; Ambroggi, F. Isolating eventrelated neuronal responses by deconvolution. J. Neurophysiol., 2010, 104(3), 1790-1802.
[http://dx.doi.org/10.1152/jn.00389.2010] [PMID: 20631219]
[35]
Ambroggi, F.; Ghazizadeh, A.; Nicola, S.M.; Fields, H.L. Roles of nucleus accumbens core and shell in incentive-cue responding and behavioral inhibition. J. Neurosci., 2011, 31(18), 6820-6830.
[http://dx.doi.org/10.1523/JNEUROSCI.6491-10.2011] [PMID: 21543612]
[36]
McGinty, V.B.; Lardeux, S.; Taha, S.A.; Kim, J.J.; Nicola, S.M. Invigoration of reward seeking by cue and proximity encoding in the nucleus accumbens. Neuron, 2013, 78(5), 910-922.
[http://dx.doi.org/10.1016/j.neuron.2013.04.010] [PMID: 23764290]
[37]
Wilson, C.J.; Chang, H.T.; Kitai, S.T. Origins of post synaptic potentials evoked in spiny neostriatal projection neurons by thalamic stimulation in the rat. Exp. Brain Res., 1983, 51(2), 217-226.
[http://dx.doi.org/10.1007/BF00237197] [PMID: 6194007]
[38]
Mouroux, M.; Féger, J. Evidence that the parafascicular projection to the subthalamic nucleus is glutamatergic. Neuroreport, 1993, 4(6), 613-615.
[http://dx.doi.org/10.1097/00001756-199306000-00002] [PMID: 8102257]
[39]
Beatty, J.A.; Sylwestrak, E.L.; Cox, C.L. Two distinct populations of projection neurons in the rat lateral parafascicular thalamic nucleus and their cholinergic responsiveness. Neuroscience, 2009, 162(1), 155-173.
[http://dx.doi.org/10.1016/j.neuroscience.2009.04.043] [PMID: 19393292]
[40]
Mendez-Rodriguez, B.S.; Arias-Garcia, M.A.; Tapia, D.; Laville, A.; Bargas, J.; Galarraga, E. Firing differences between adult intralaminar thalamo-striatal neurons. Neuroscience, 2021, 458, 153-165.
[http://dx.doi.org/10.1016/j.neuroscience.2020.12.032] [PMID: 33428968]
[41]
Chen, B.; Xu, C.; Wang, Y.; Lin, W.; Wang, Y.; Chen, L.; Cheng, H.; Xu, L.; Hu, T.; Zhao, J.; Dong, P.; Guo, Y.; Zhang, S.; Wang, S.; Zhou, Y.; Hu, W.; Duan, S.; Chen, Z. A disinhibitory nigra-parafascicular pathway amplifies seizure in temporal lobe epilepsy. Nat. Commun., 2020, 11(1), 923.
[http://dx.doi.org/10.1038/s41467-020-14648-8] [PMID: 32066723]
[42]
Minamimoto, T.; Hori, Y.; Kimura, M. Roles of the thalamic CM-PF complex—basal ganglia circuit in externally driven rebias of action. Brain Res. Bull., 2009, 78(2-3), 75-79.
[http://dx.doi.org/10.1016/j.brainresbull.2008.08.013] [PMID: 18793702]
[43]
Krout, K.E.; Loewy, A.D.; Westby, G.W.M.; Redgrave, P. Superior colliculus projections to midline and intralaminar thalamic nuclei of the rat. J. Comp. Neurol., 2001, 431(2), 198-216.
[http://dx.doi.org/10.1002/1096-9861(20010305)431:2<198:AID-CNE1065>3.0.CO;2-8] [PMID: 11170000]
[44]
Krauthamer, G.M.; Krol, J.G.; Grunwerg, B.S. Effect of superior colliculus lesions on sensory unit responses in the intralaminar thalamus of the rat. Brain Res., 1992, 576(2), 277-286.
[http://dx.doi.org/10.1016/0006-8993(92)90691-2] [PMID: 1515921]
[45]
Paré, D.; Smith, Y.; Parent, A.; Steriade, M. Projections of brainstem core cholinergic and non-cholinergic neurons of cat to intralaminar and reticular thalamic nuclei. Neuroscience, 1988, 25(1), 69-86.
[http://dx.doi.org/10.1016/0306-4522(88)90007-3] [PMID: 3393287]
[46]
Sidibé, M.; Smith, Y. Thalamic inputs to striatal interneurons in monkeys: Synaptic organization and colocalization of calcium binding proteins. Neuroscience, 1999, 89(4), 1189-1208.
[http://dx.doi.org/10.1016/S0306-4522(98)00367-4] [PMID: 10362307]
[47]
Lapper, S.R.; Bolam, J.P. Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience, 1992, 51(3), 533-545.
[http://dx.doi.org/10.1016/0306-4522(92)90293-B] [PMID: 1488113]
[48]
Raju, D.V.; Shah, D.J.; Wright, T.M.; Hall, R.A.; Smith, Y. Differential synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats. J. Comp. Neurol., 2006, 499(2), 231-243.
[http://dx.doi.org/10.1002/cne.21099] [PMID: 16977615]
[49]
Witten, I.B.; Lin, S.C.; Brodsky, M.; Prakash, R.; Diester, I.; Anikeeva, P.; Gradinaru, V.; Ramakrishnan, C.; Deisseroth, K. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science, 2010, 330(6011), 1677-1681.
[50]
Assous, M.; Kaminer, J.; Shah, F.; Garg, A.; Koós, T.; Tepper, J.M. Differential processing of thalamic information via distinct striatal interneuron circuits. Nat. Commun., 2017, 8(1), 15860.
[http://dx.doi.org/10.1038/ncomms15860] [PMID: 28604688]
[51]
Assous, M.; Tepper, J.M. Excitatory extrinsic afferents to striatal interneurons and interactions with striatal microcircuitry. Eur. J. Neurosci., 2019, 49(5), 593-603.
[52]
Yun, I.A.; Wakabayashi, K.T.; Fields, H.L.; Nicola, S.M. The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J. Neurosci., 2004, 24(12), 2923-2933.
[http://dx.doi.org/10.1523/JNEUROSCI.5282-03.2004] [PMID: 15044531]
[53]
Ambroggi, F.; Ishikawa, A.; Fields, H.L.; Nicola, S.M. Basolateral amygdala neurons facilitate rewardseeking behavior by exciting nucleus accumbens neurons. Neuron, 2008, 59(4), 648-661.
[http://dx.doi.org/10.1016/j.neuron.2008.07.004] [PMID: 18760700]

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