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Cortico-Subthalamic Projections In The Rat

Year 2010, Volume: 27 Issue: 1, 4 - 11, 25.01.2012

Abstract

The subthalamic nucleus (STN) is a key structure in the basal ganglia and plays a major role in the pathogenesis of Parkinson’s disease. The STN is a popular target for deep brain stimulation (DBS). DBS of the STN improves motor symptoms. Unfortunately, also negative stimulation induced side-effects on behavior and cognition can occur. These side-effects are thought to be caused by direct stimulation of the associative and limbic pathways that run through the STN. In the primate, three functionally segregated parts are clearly described within the STN: a dorsolateral motor part, a medial limbic part and a ventrolateral associative part. In the rodent however, these subdivisions are not well defined. In this review we describe all anterograde cortico-subthalamic tracer studies to map the rodent STN. As a result, a crude functional subdivision in the rodent STN can be made. The lateral two thirds of the STN receive input from the motor and pre-motor cortex, sparing the medial tip. The medial third receives input from the anterior cingulated, the prelimbic and the agranular insular cortices. There is little evidence for a ventrolateral-dorsomedial subdivision of the medial STN. We conclude that, even though the functional subdivisions are not as clear cut as in the primate STN, a partial anatomical subdivision is present in the rodent STN

References

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  • Benazzouz, A., Breit, S., Koudsie, A., Pollak, P., Krack, P., Benabid, A.L., 2002. Intraoperative microrecordings of the subthalamic nucleus in Parkinson’s disease. Mov. Disord. 17 Suppl 3, S145-149.
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  • Berendse, H.W., Groenewegen, H.J., 1991. The connections of the medial part of the subthalamic nucleus in the rat: evidence for a parallel organization. The basal ganglia III New York: Plenum 89-98.
  • Bergman, H., Wichmann, T., Karmon, B., DeLong, M.R., 1994. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 72, 507-520.
  • Canteras, N.S., Shammah-Lagnado, S.J., Silva, B.A., Ricardo, J.A., 1988. Somatosensory inputs to the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res. 458, 53-64.
  • Canteras, N.S., Shammah-Lagnado, S,J., Silva, B.A., Ricardo, J.A., 1990. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res. 513, 43-59.
  • Carpenter, M.B., Carleton, S.C., Keller, J.T., Conte, P., 1981. Connections of the subthalamic nucleus in the monkey. Brain Res. 224, 1-29.
  • Degos, B., Deniau, J.M., Le Cam, J., Mailly, P., Maurice, N., 2008. Evidence for a direct subthalamo-cortical loop circuit in the rat. Eur. J. Neurosci. 27, 2599-2610.
  • Donoghue, J.P., Wise, S.P., 1982. The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J. Comp. Neurol. 212, 76-88.
  • Dostrovsky, J.O., Lozano, A.M., 2002. Mechanisms of deep brain stimulation. Mov. Disord. 17 Suppl 3, S63-68.
  • Fujimoto, K., Kita, H., 1993. Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res. 609, 185-192.
  • Gerfen, C.R., 1985. The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J. Comp. Neurol. 236, 454-476.
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  • Monakow, K.H., Akert, K., Kunzle, H., 1978. Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp. Brain Res. Experimentelle Hirnforschung. 33, 395-403.
  • Nambu, A., Takada, M., Inase, M., Tokuno, H., 1996. Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area. J. Neurosci. 16, 2671-2683.
  • Nambu, A., Tokuno, H., Hamada, I., Kita, H., Imanishi, M., Akazawa, T., Ikeuchi, Y., Hasegawa, N., 2000. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J. Neurophysiol. 84, 289-300.
  • Nambu, A., Tokuno, H., Inase, M., Takada, M., 1997. Corticosubthalamic input zones from forelimb representations of the dorsal and ventral divisions of the premotor cortex in the macaque monkey: comparison with the input zones from the primary motor cortex and the supplementary motor area. Neuroscience letters. 239,13-16.
  • Nambu, A., Tokuno, H., Takada, M., 2002. Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci. Res. 43, 111-117.
  • Ni, Z.G., Bouali-Benazzouz, R., Gao, D.M., Benabid, A.L., Benazzouz, A., 2001. Time-course of changes in firing rates and firing patterns of subthalamic nucleus neuronal activity after 6-OHDA-induced dopamine depletion in rats. Brain Res. 899, 142-147.
  • Orieux, G., Francois, C., Feger, J., Hirsch, E.C., 2002. Consequences of dopaminergic denervation on the metabolic activity of the cortical neurons projecting to the subthalamic nucleus in the rat. J. Neurosci. 22, 8762-8770.
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  • Reiner, A., Veenman, C.L., Medina, L., Jiao, Y., Del Mar, N., Honig, M.G., 2000. Pathway tracing using biotinylated dextran amines. J. Neurosci. methods. 103, 23-37.
  • Ricardo, J.A., 1980. Efferent connections of the subthalamic region in the rat. I. The subthalamic nucleus of Luys. Brain Res. 202, 257-271.
  • Rodriguez-Oroz, M.C., Zamarbide, I., Guridi, J., Palmero, M.R., Obeso, J.A., 2004. Efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease 4 years after surgery: double blind and open label evaluation. J. Neurol., J. Neurosurg., J. Psychiat. 75, 1382-1385.
  • Rouzaire-Dubois, B., Scarnati, E., 1985. Bilateral corticosubthalamic nucleus projections: an electrophysiological study in rats with chronic cerebral lesions. Neurosci. 15, 69-79.
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  • Temel, Y., Blokland, A., Steinbusch, H.W., Visser-Vandewalle, V., 2005. The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog. Neurobiol. 76, 393-413.
  • Temel, Y., Kessels, A., Tan, S., Topdag, A., Boon, P., Visser-Vandewalle, V., 2006. Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism Relat D. 12, 265-272.
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Year 2010, Volume: 27 Issue: 1, 4 - 11, 25.01.2012

Abstract

References

  • Afsharpour, S., 1985. Topographical projections of the cerebral cortex to the subthalamic nucleus. The J. Comp. Neurol. 236, 14-28.
  • Benazzouz, A., Breit, S., Koudsie, A., Pollak, P., Krack, P., Benabid, A.L., 2002. Intraoperative microrecordings of the subthalamic nucleus in Parkinson’s disease. Mov. Disord. 17 Suppl 3, S145-149.
  • Berendse, H.W., Groenewegen, H.J., 1990. Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J. Comp. Neurol. 299, 187-228.
  • Berendse, H.W., Groenewegen, H.J., 1991. The connections of the medial part of the subthalamic nucleus in the rat: evidence for a parallel organization. The basal ganglia III New York: Plenum 89-98.
  • Bergman, H., Wichmann, T., Karmon, B., DeLong, M.R., 1994. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 72, 507-520.
  • Canteras, N.S., Shammah-Lagnado, S.J., Silva, B.A., Ricardo, J.A., 1988. Somatosensory inputs to the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res. 458, 53-64.
  • Canteras, N.S., Shammah-Lagnado, S,J., Silva, B.A., Ricardo, J.A., 1990. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res. 513, 43-59.
  • Carpenter, M.B., Carleton, S.C., Keller, J.T., Conte, P., 1981. Connections of the subthalamic nucleus in the monkey. Brain Res. 224, 1-29.
  • Degos, B., Deniau, J.M., Le Cam, J., Mailly, P., Maurice, N., 2008. Evidence for a direct subthalamo-cortical loop circuit in the rat. Eur. J. Neurosci. 27, 2599-2610.
  • Donoghue, J.P., Wise, S.P., 1982. The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J. Comp. Neurol. 212, 76-88.
  • Dostrovsky, J.O., Lozano, A.M., 2002. Mechanisms of deep brain stimulation. Mov. Disord. 17 Suppl 3, S63-68.
  • Fujimoto, K., Kita, H., 1993. Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res. 609, 185-192.
  • Gerfen, C.R., 1985. The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J. Comp. Neurol. 236, 454-476.
  • Gradinaru, V., Mogri, M., Thompson, K.R., Henderson, J.M., Deisseroth, K., 2009. Optical Deconstruction of Parkinsonian Neural Circuitry. Science (New York, NY.2009).
  • Groenewegen, H.J., Berendse, H.W., 1990. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J. Comp. Neurol. 294, 607-622.
  • Hall, R.D., Lindholm, E.P., 1974. Organization of the motor and somatosensory neocortex in the albino rat. . Brain Res. 66, 23-38.
  • Hamani, C., Saint-Cyr, J.A., Fraser, J., Kaplitt, M., Lozano, A.M., 2004. The subthalamic nucleus in the context of movement disorders. Brain. 127, 4-20.
  • Hameleers, R., Temel, Y., Visser-Vandewalle, V., 2006. History of the corpus luysii: 1865-1995. Arch. Neurol. 63, 1340-1342.
  • Hardman, C.D., Henderson, J.M., Finkelstein, D.I., Horne, M.K., Paxinos, G., Halliday, G.M., 2002. Comparison of the basal ganglia in rats, marmosets, macaques, baboons, and humans: volume and neuronal number for the output, internal relay, and striatal modulating nuclei. J. Comp. Neurol. 445, 238-255.
  • Heimer, L., Alheid, G.F., Zahm, D.S., 1995. Basal ganglia. In: The rat nervous system (Paxinos, G., ed), pp 579-628: Academic Press Inc., San Diego.
  • Jurgens, U., 1984. The efferent and afferent connections of the supplementary motor area. Brain Res. 300, 63-81.
  • Kita, H., Kitai, S.T., 1987. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. Comp. Neurol. 260, 435-452.
  • Kitai, S.T., Deniau, J.M., 1981. Cortical inputs to the subthalamus: intracellular analysis. Brain Res. 214, 411-415.
  • Kleiner-Fisman, G., Herzog, J., Fisman, D.N., Tamma, F., Lyons, K.E., Pahwa, R., Lang, A.E., Deuschl, G., 2006. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov. Disord. 21 Suppl 14, S290-304.
  • Kolomiets, B.P., Deniau, J.M., Mailly, P., Menetrey, A., Glowinski, J., Thierry, A.M., 2001. Segregation and convergence of information flow through the cortico-subthalamic pathways. J. Neurosci. 21, 5764-5772.
  • Krack, P., Batir, A., Van Blercom, N., Chabardes, S., Fraix, V., Ardouin, C., Koudsie, A., Limousin, P.D., Benazzouz, A., LeBas, J.F., Benabid, A.L., Pollak, P., 2003. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N.E.J.M. 349, 1925-1934.
  • Kunzle, H., 1978. An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in macaca fascicularis. Brain, behavior and evolution. 15, 185-234.
  • Leichnetz, G.R., Hardy, S.G., Carruth, M.K., 1987. Frontal projections to the region of the oculomotor complex in the rat: a retrograde and anterograde HRP study. J. Comp. Neurol. 263, 387-399.
  • Magill, P.J., Bolam, J.P., Bevan, M.D., 2000. Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J. Neurosci. 20, 820-833.
  • Magill, P.J., Sharott, A., Bevan, M.D., Brown, P., Bolam, J.P., 2004. Synchronous unit activity and local field potentials evoked in the subthalamic nucleus by cortical stimulation. J. Neurophysiol. 92, 700-714.
  • Maurice, N., Deniau, J.M., Glowinski, J., Thierry, A.M., 1998. Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J. Neurosci. 18, 9539-9546.
  • Monakow, K.H., Akert, K., Kunzle, H., 1978. Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp. Brain Res. Experimentelle Hirnforschung. 33, 395-403.
  • Nambu, A., Takada, M., Inase, M., Tokuno, H., 1996. Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area. J. Neurosci. 16, 2671-2683.
  • Nambu, A., Tokuno, H., Hamada, I., Kita, H., Imanishi, M., Akazawa, T., Ikeuchi, Y., Hasegawa, N., 2000. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J. Neurophysiol. 84, 289-300.
  • Nambu, A., Tokuno, H., Inase, M., Takada, M., 1997. Corticosubthalamic input zones from forelimb representations of the dorsal and ventral divisions of the premotor cortex in the macaque monkey: comparison with the input zones from the primary motor cortex and the supplementary motor area. Neuroscience letters. 239,13-16.
  • Nambu, A., Tokuno, H., Takada, M., 2002. Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci. Res. 43, 111-117.
  • Ni, Z.G., Bouali-Benazzouz, R., Gao, D.M., Benabid, A.L., Benazzouz, A., 2001. Time-course of changes in firing rates and firing patterns of subthalamic nucleus neuronal activity after 6-OHDA-induced dopamine depletion in rats. Brain Res. 899, 142-147.
  • Orieux, G., Francois, C., Feger, J., Hirsch, E.C., 2002. Consequences of dopaminergic denervation on the metabolic activity of the cortical neurons projecting to the subthalamic nucleus in the rat. J. Neurosci. 22, 8762-8770.
  • Parent, A., Hazrati, L.N., 1995. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Rev. 20, 91-127.
  • Parent, A., Hazrati, L.N., 1995. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res. Rev. 20, 128-154.
  • Paxinos, G., Watson, C., (eds) 1986. The rat brain in stereotaxic coordinates. New York: Acadmic Press.
  • Paxinos, G., Watson, C., (eds.) 1998. The rat brain in stereotaxic coordinates New York: Academic Press.
  • Paxinos, G., Watson, C., (eds.) 2005. The rat brain in stereotaxic coordinates New York: Academic Press.
  • Reiner, A., Veenman, C.L., Medina, L., Jiao, Y., Del Mar, N., Honig, M.G., 2000. Pathway tracing using biotinylated dextran amines. J. Neurosci. methods. 103, 23-37.
  • Ricardo, J.A., 1980. Efferent connections of the subthalamic region in the rat. I. The subthalamic nucleus of Luys. Brain Res. 202, 257-271.
  • Rodriguez-Oroz, M.C., Zamarbide, I., Guridi, J., Palmero, M.R., Obeso, J.A., 2004. Efficacy of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease 4 years after surgery: double blind and open label evaluation. J. Neurol., J. Neurosurg., J. Psychiat. 75, 1382-1385.
  • Rouzaire-Dubois, B., Scarnati, E., 1985. Bilateral corticosubthalamic nucleus projections: an electrophysiological study in rats with chronic cerebral lesions. Neurosci. 15, 69-79.
  • Strafella, A.P., Vanderwerf, Y., Sadikot, A.F., 2004. Transcranial magnetic stimulation of the human motor cortex influences the neuronal activity of subthalamic nucleus. Eur. J. Neurosci. 20, 2245-2249.
  • Sugimoto, T., Hattori, T., Mizuno, N., Itoh, K., Sato, M., 1983. Direct projections from the centre median-parafascicular complex to the subthalamic nucleus in the cat and rat. J. Comp. Neurol. 214, 209-216.
  • Temel, Y., Blokland, A., Steinbusch, H.W., Visser-Vandewalle, V., 2005. The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog. Neurobiol. 76, 393-413.
  • Temel, Y., Kessels, A., Tan, S., Topdag, A., Boon, P., Visser-Vandewalle, V., 2006. Behavioural changes after bilateral subthalamic stimulation in advanced Parkinson disease: a systematic review. Parkinsonism Relat D. 12, 265-272.
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There are 66 citations in total.

Details

Primary Language English
Journal Section Basic Medical Sciences
Authors

Marcus Janssen

Veerle Visser-vandewalle This is me

Yasin Temel

Publication Date January 25, 2012
Submission Date July 12, 2010
Published in Issue Year 2010 Volume: 27 Issue: 1

Cite

APA Janssen, M., Visser-vandewalle, V., & Temel, Y. (2012). Cortico-Subthalamic Projections In The Rat. Journal of Experimental and Clinical Medicine, 27(1), 4-11. https://doi.org/10.5835/jecm.v27i1.1354
AMA Janssen M, Visser-vandewalle V, Temel Y. Cortico-Subthalamic Projections In The Rat. J. Exp. Clin. Med. January 2012;27(1):4-11. doi:10.5835/jecm.v27i1.1354
Chicago Janssen, Marcus, Veerle Visser-vandewalle, and Yasin Temel. “Cortico-Subthalamic Projections In The Rat”. Journal of Experimental and Clinical Medicine 27, no. 1 (January 2012): 4-11. https://doi.org/10.5835/jecm.v27i1.1354.
EndNote Janssen M, Visser-vandewalle V, Temel Y (January 1, 2012) Cortico-Subthalamic Projections In The Rat. Journal of Experimental and Clinical Medicine 27 1 4–11.
IEEE M. Janssen, V. Visser-vandewalle, and Y. Temel, “Cortico-Subthalamic Projections In The Rat”, J. Exp. Clin. Med., vol. 27, no. 1, pp. 4–11, 2012, doi: 10.5835/jecm.v27i1.1354.
ISNAD Janssen, Marcus et al. “Cortico-Subthalamic Projections In The Rat”. Journal of Experimental and Clinical Medicine 27/1 (January 2012), 4-11. https://doi.org/10.5835/jecm.v27i1.1354.
JAMA Janssen M, Visser-vandewalle V, Temel Y. Cortico-Subthalamic Projections In The Rat. J. Exp. Clin. Med. 2012;27:4–11.
MLA Janssen, Marcus et al. “Cortico-Subthalamic Projections In The Rat”. Journal of Experimental and Clinical Medicine, vol. 27, no. 1, 2012, pp. 4-11, doi:10.5835/jecm.v27i1.1354.
Vancouver Janssen M, Visser-vandewalle V, Temel Y. Cortico-Subthalamic Projections In The Rat. J. Exp. Clin. Med. 2012;27(1):4-11.