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
Perspective

The Subthalamic Nucleus: A Hub for Sensory Control via Short Three- Lateral Loop Connections with the Brainstem?

Author(s): Racha Al Tannir, Arnaud Pautrat, Jérôme Baufreton, Paul G. Overton and Veronique Coizet*

Volume 21, Issue 1, 2023

Published on: 18 July, 2022

Page: [22 - 30] Pages: 9

DOI: 10.2174/1570159X20666220718113548

Abstract

The subthalamic nucleus (STN) is classically subdivided into sensori-motor, associative and limbic regions, which is consistent with the involvement of this structure in not only motor control, but also in cognitive and emotional tasks. However, the function of the sensory inputs to the STN’s sensori-motor territory is comparatively less well explored, although sensory responses have been reported in this structure. There is still a paucity of information regarding the characteristics of that subdivision and its potential functional role in basal ganglia processing and more widely in associated networks. In this perspective paper, we summarize the type of sensory stimuli that have been reported to activate the STN, and describe the complex sensory properties of the STN and its anatomical link to a sensory network involving the brainstem, characterized in our recent work. Analyzing the sensory input to the STN led us to suggest the existence of previously unreported threelateral subcortical loops between the basal ganglia and the brainstem which do not involve the cortex. Anatomically, these loops closely link the STN, the substantia nigra pars reticulata and various structures from the brainstem such as the superior colliculus and the parabrachial nucleus. We also discuss the potential role of the STN in the control of sensory activity in the brainstem and its possible contribution to favoring sensory habituation or sensitization over brainstem structures to optimize the best selection of action at a given time.

Keywords: Subthalamic nucleus, brainstem, sensory processing, three-lateral loops, sensory control, basal ganglia, action selection.

« Previous Next »
[1]
Gillies, A.; Arbuthnott, G. Computational models of the basal ganglia. Mov. Disord., 2000, 15(5), 762-770.
[http://dx.doi.org/10.1002/1531-8257(200009)15:5<762:AID-MDS1002>3.0.CO;2-2] [PMID: 11009178]
[2]
Parent, A.; Hazrati, L.N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Brain Res. Rev., 1995, 20(1), 91-127.
[http://dx.doi.org/10.1016/0165-0173(94)00007-C] [PMID: 7711769]
[3]
Baunez, C.; Robbins, T.W. Bilateral lesions of the subthalamic nucleus induce multiple deficits in an attentional task in rats. Eur. J. Neurosci., 1997, 9(10), 2086-2099.
[http://dx.doi.org/10.1111/j.1460-9568.1997.tb01376.x] [PMID: 9421169]
[4]
Baunez, C.; Amalric, M.; Robbins, T.W. Enhanced food-related motivation after bilateral lesions of the subthalamic nucleus. J. Neurosci., 2002, 22(2), 562-568.
[http://dx.doi.org/10.1523/JNEUROSCI.22-02-00562.2002] [PMID: 11784803]
[5]
Uslaner, J.M.; Robinson, T.E. Subthalamic nucleus lesions increase impulsive action and decrease impulsive choice - mediation by enhanced incentive motivation? Eur. J. Neurosci., 2006, 24(8), 2345-2354.
[http://dx.doi.org/10.1111/j.1460-9568.2006.05117.x] [PMID: 17074055]
[6]
Darbaky, Y.; Baunez, C.; Arecchi, P.; Legallet, E.; Apicella, P. Reward-related neuronal activity in the subthalamic nucleus of the monkey. Neuroreport, 2005, 16(11), 1241-1244.
[http://dx.doi.org/10.1097/00001756-200508010-00022] [PMID: 16012357]
[7]
Lardeux, S.; Pernaud, R.; Paleressompoulle, D.; Baunez, C. Beyond the reward pathway: Coding reward magnitude and error in the rat subthalamic nucleus. J. Neurophysiol., 2009, 102(4), 2526-2537.
[http://dx.doi.org/10.1152/jn.91009.2008] [PMID: 19710371]
[8]
Lardeux, S.; Paleressompoulle, D.; Pernaud, R.; Cador, M.; Baunez, C. Different populations of subthalamic neurons encode cocaine vs. sucrose reward and predict future error. J. Neurophysiol., 2013, 110(7), 1497-1510.
[http://dx.doi.org/10.1152/jn.00160.2013] [PMID: 23864369]
[9]
Buot, A.; Welter, M.L.; Karachi, C.; Pochon, J-B.; Bardinet, E.; Yelnik, J.; Mallet, L. Processing of emotional information in the human subthalamic nucleus. J. Neurol. Neurosurg. Psychiatry, 2013, 84(12), 1331-1338.
[http://dx.doi.org/10.1136/jnnp-2011-302158] [PMID: 23100448]
[10]
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]
[11]
Monchi, O.; Petrides, M.; Strafella, A.P.; Worsley, K.J.; Doyon, J. Functional role of the basal ganglia in the planning and execution of actions. Ann. Neurol., 2006, 59(2), 257-264.
[http://dx.doi.org/10.1002/ana.20742] [PMID: 16437582]
[12]
Isoda, M.; Hikosaka, O. Role for subthalamic nucleus neurons in switching from automatic to controlled eye movement. J. Neurosci., 2008, 28(28), 7209-7218.
[http://dx.doi.org/10.1523/JNEUROSCI.0487-08.2008] [PMID: 18614691]
[13]
Jahanshahi, M.; Obeso, I.; Rothwell, J.C.; Obeso, J.A. A fronto-striato-subthalamic-pallidal network for goal-directed and habitual inhibition. Nat. Rev. Neurosci., 2015, 16(12), 719-732.
[http://dx.doi.org/10.1038/nrn4038] [PMID: 26530468]
[14]
Narayanan, N.S.; Wessel, J.R.; Greenlee, J.D.W. The fastest way to stop: Inhibitory control and IFG-STN hyperdirect connectivity. Neuron, 2020, 106(4), 549-551.
[http://dx.doi.org/10.1016/j.neuron.2020.04.017] [PMID: 32437650]
[15]
Criaud, M.; Anton, J-L.; Nazarian, B.; Longcamp, M.; Metereau, E.; Boulinguez, P.; Ballanger, B. The human basal ganglia mediate the interplay between reactive and proactive control of response through both motor inhibition and sensory modulation. Brain Sci., 2021, 11(5), 560.
[http://dx.doi.org/10.3390/brainsci11050560] [PMID: 33925153]
[16]
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, 357-381.
[http://dx.doi.org/10.1146/annurev.ne.09.030186.002041] [PMID: 3085570]
[17]
Hamani, C.; Saint-Cyr, J.A.; Fraser, J.; Kaplitt, M.; Lozano, A.M. The subthalamic nucleus in the context of movement disorders. Brain, 2004, 127(Pt 1), 4-20.
[http://dx.doi.org/10.1093/brain/awh029] [PMID: 14607789]
[18]
Baunez, C.; Yelnik, J.; Mallet, L. Six questions on the subthalamic nucleus: Lessons from animal models and from stimulated patients. Neuroscience, 2011, 198, 193-204.
[http://dx.doi.org/10.1016/j.neuroscience.2011.09.059] [PMID: 22001680]
[19]
Pautrat, A.; Rolland, M.; Barthelemy, M.; Baunez, C.; Sinniger, V.; Piallat, B.; Savasta, M.; Overton, P.G.; David, O.; Coizet, V. Revealing a novel nociceptive network that links the subthalamic nucleus to pain processing. eLife, 2018, 7, e36607.
[http://dx.doi.org/10.7554/eLife.36607] [PMID: 30149836]
[20]
Hammond, C.; Deniau, J.M.; Rizk, A.; Feger, J. Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res., 1978, 151(2), 235-244.
[http://dx.doi.org/10.1016/0006-8993(78)90881-8] [PMID: 209862]
[21]
Matsumura, M.; Kojima, J.; Gardiner, T.W.; Hikosaka, O. Visual and oculomotor functions of monkey subthalamic nucleus. J. Neurophysiol., 1992, 67(6), 1615-1632.
[http://dx.doi.org/10.1152/jn.1992.67.6.1615] [PMID: 1629767]
[22]
Mirzaei, A.; Kumar, A.; Leventhal, D.; Mallet, N.; Aertsen, A.; Berke, J.; Schmidt, R. Sensorimotor processing in the basal ganglia leads to transient beta oscillations during behavior. J. Neurosci., 2017, 37(46), 11220-11232.
[http://dx.doi.org/10.1523/JNEUROSCI.1289-17.2017] [PMID: 29038241]
[23]
Hanajima, R.; Dostrovsky, J.O.; Lozano, A.M.; Hutchison, W.D.; Davis, K.D.; Chen, R.; Ashby, P. Somatosensory evoked potentials (SEPs) recorded from deep brain stimulation (DBS) electrodes in the thalamus and subthalamic nucleus (STN). Clin. Neurophysiol., 2004, 115(2), 424-434.
[http://dx.doi.org/10.1016/j.clinph.2003.09.027] [PMID: 14744585]
[24]
Pesenti, A.; Priori, A.; Locatelli, M.; Egidi, M.; Rampini, P.; Tamma, F.; Caputo, E.; Chiesa, V.; Barbieri, S. Subthalamic somatosensory evoked potentials in Parkinson’s disease. Mov. Disord., 2003, 18(11), 1341-1345.
[http://dx.doi.org/10.1002/mds.10519] [PMID: 14639678]
[25]
Trenado, C.; Elben, S.; Friggemann, L.; Groiss, S.J.; Vesper, J.; Schnitzler, A.; Wojtecki, L. Intraoperative localization of the subthalamic nucleus using long-latency somatosensory evoked potentials. Neuromodulation, 2018, 21(6), 582-587.
[http://dx.doi.org/10.1111/ner.12727] [PMID: 29164724]
[26]
Minks, E.; Jurák, P.; Chládek, J.; Chrastina, J.; Halámek, J.; Shaw, D.J.; Bareš, M. Mismatch negativity-like potential (MMN-like) in the subthalamic nuclei in Parkinson’s disease patients. J. Neural Transm. (Vienna), 2014, 121(12), 1507-1522.
[http://dx.doi.org/10.1007/s00702-014-1221-3] [PMID: 24809684]
[27]
Heldmann, M.; Münte, T.F.; Paracka, L.; Beyer, F.; Brüggemann, N.; Saryyeva, A.; Rasche, D.; Krauss, J.K.; Tronnier, V.M. Human subthalamic nucleus - Automatic auditory change detection as a basis for action selection. Neuroscience, 2017, 355, 141-148.
[http://dx.doi.org/10.1016/j.neuroscience.2017.05.008] [PMID: 28504196]
[28]
Belasen, A.; Youn, Y.; Gee, L.; Prusik, J.; Lai, B.; Ramirez-Zamora, A.; Rizvi, K.; Yeung, P.; Shin, D.S.; Argoff, C.; Pilitsis, J.G. The effects of mechanical and thermal stimuli on local field potentials and single unit activity in Parkinson’s disease patients. Neuromodulation, 2016, 19(7), 698-707.
[http://dx.doi.org/10.1111/ner.12453] [PMID: 27284636]
[29]
Heise, C.E.; Reyes, S. Mitrofanis, J. Sensory (nociceptive) stimulation evokes Fos expression in the subthalamus of hemiparkinsonian rats. Neurol. Res., 2008, 30(3), 277-284.
[http://dx.doi.org/10.1179/016164107X235455] [PMID: 17848208]
[30]
Luan, Y.; Tang, D.; Wu, H.; Gu, W.; Wu, Y.; Cao, J.L.; Xiao, C.; Zhou, C. Reversal of hyperactive subthalamic circuits differentially mitigates pain hypersensitivity phenotypes in parkinsonian mice. Proc. Natl. Acad. Sci. USA, 2020.
[http://dx.doi.org/10.1073/pnas.1916263117]
[31]
Mostofi, A.; Morgante, F.; Edwards, M.J.; Brown, P.; Pereira, E.A.C. Pain in Parkinson’s disease and the role of the subthalamic nucleus. Brain, 2021, 144(5), 1342-1350.
[http://dx.doi.org/10.1093/brain/awab001] [PMID: 34037696]
[32]
Coizet, V.; Graham, J.H.; Moss, J.; Bolam, J.P.; Savasta, M.; McHaffie, J.G.; Redgrave, P.; Overton, P.G. Short-latency visual input to the subthalamic nucleus is provided by the midbrain superior colliculus. J. Neurosci., 2009, 29(17), 5701-5709.
[http://dx.doi.org/10.1523/JNEUROSCI.0247-09.2009] [PMID: 19403836]
[33]
Cavdar, S.; Özgür, M.; Çakmak, Y.Ö.; Kuvvet, Y.; Kunt, S.K.; Sağlam, G. Afferent projections of the subthalamic nucleus in the rat: Emphasis on bilateral and interhemispheric connections. Acta Neurobiol. Exp. (Warsz.), 2018, 78(3), 251-263.
[http://dx.doi.org/10.21307/ane-2018-023] [PMID: 30295682]
[34]
Jackson, A.; Crossman, A.R. Nucleus tegmenti pedunculopontinus: Efferent connections with special reference to the basal ganglia, studied in the rat by anterograde and retrograde transport of horseradish peroxidase. Neuroscience, 1983, 10(3), 725-765.
[http://dx.doi.org/10.1016/0306-4522(83)90213-0] [PMID: 6646427]
[35]
McHaffie, J.G.; Stanford, T.R.; Stein, B.E.; 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]
[36]
Deniau, J.M.; Chevalier, G. The lamellar organization of the rat substantia nigra pars reticulata: Distribution of projection neurons. Neuroscience, 1992, 46(2), 361-377.
[http://dx.doi.org/10.1016/0306-4522(92)90058-A] [PMID: 1542412]
[37]
Hopkins, D.A.; Niessen, L.W. Substantia nigra projections to the reticular formation, superior colliculus and central gray in the rat, cat and monkey. Neurosci. Lett., 1976, 2(5), 253-259.
[http://dx.doi.org/10.1016/0304-3940(76)90156-7] [PMID: 19604767]
[38]
Schneider, J.S. Interactions between the basal ganglia, the pontine parabrachial region, and the trigeminal system in cat. Neuroscience, 1986, 19(2), 411-425.
[http://dx.doi.org/10.1016/0306-4522(86)90271-X] [PMID: 3774149]
[39]
Spann, B.M.; Grofova, I. Nigropedunculopontine projection in the rat: An anterograde tracing study with phaseolus vulgaris-leucoagglutinin (PHA-L). J. Comp. Neurol., 1991, 311(3), 375-388.
[http://dx.doi.org/10.1002/cne.903110308] [PMID: 1720145]
[40]
Tokuno, H.; Takada, M.; Ikai, Y.; Mizuno, N. Direct projections from the deep layers of the superior colliculus to the subthalamic nucleus in the rat. Brain Res., 1994, 639(1), 156-160.
[http://dx.doi.org/10.1016/0006-8993(94)91776-0] [PMID: 8180831]
[41]
Smith, Y.; Bevan, M.D.; Shink, E.; Bolam, J.P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience, 1998, 86(2), 353-387.
[PMID: 9881853]
[42]
McElvain, L.E.; Chen, Y.; Moore, J.D.; Brigidi, G.S.; Bloodgood, B.L.; Lim, B.K.; Costa, R.M.; Kleinfeld, D. Specific populations of basal ganglia output neurons target distinct brain stem areas while collateralizing throughout the diencephalon. Neuron, 2021, 109(10), 1721-1738.e4.
[http://dx.doi.org/10.1016/j.neuron.2021.03.017] [PMID: 33823137]
[43]
Sparks, D.L.; Nelson, J.S. Sensory and motor maps in the mammalian superior colliculus. Trends Neurosci., 1987, 10, 312-317.
[http://dx.doi.org/10.1016/0166-2236(87)90085-3]
[44]
Zhou, F.M.; Lee, C.R. Intrinsic and integrative properties of substantia nigra pars reticulata neurons. Neuroscience, 2011, 198, 69-94.
[http://dx.doi.org/10.1016/j.neuroscience.2011.07.061] [PMID: 21839148]
[45]
Magill, P.J.; Bolam, J.P.; Bevan, M.D. Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J. Neurosci., 2000, 20(2), 820-833.
[http://dx.doi.org/10.1523/JNEUROSCI.20-02-00820.2000] [PMID: 10632612]
[46]
Bolam, J.P. The functional organization of the basal ganglia: New insights from anatomical and physiological analyses.The basal ganglia VII; Nicholson, L.F.B.; Faull, R.L.N., Eds.; Plenum: New York, 2002, pp. 371-378.
[http://dx.doi.org/10.1007/978-1-4615-0715-4_37]
[47]
Chudasama, Y.; Baunez, C.; Robbins, T.W. Functional disconnection of the medial prefrontal cortex and subthalamic nucleus in attentional performance: Evidence for corticosubthalamic interaction. J. Neurosci. Neurosci., 2003, 23(13), 5477-5485.
[http://dx.doi.org/10.1523/JNEUROSCI.23-13-05477.2003]

Rights & Permissions Print Cite
Article Metrics
50
2
World Chronic Fatigue Syndrome Awareness Day
© 2024 Bentham Science Publishers | Privacy Policy