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The afferent and efferent connections of the ventromedial thalamic nucleus in the rat
Abstract
Abstract The afferent and efferent connections of the ventromedial (VM) nucleus of the thalamus in the rat were studied by experiments using the methods of retrograde cell marking by horseradish peroxidase (HRP) and anterograde fiber tracing by autoradiography. Tritiated amino acids deposited microelectrophoretically into VM label a cortical projection that is distributed to a sharply defined superficial portion of layer I of almost the entire extent of the ipsilateral neocortex. The labeling is most dense at frontal cortical levels, where fibers radiate through the deeper layers to terminate in the outer one‐quarter of layer I throughout all neocortex rostral to the genu of the corpus callosum. A lesser number of labeled fibers extends caudally in a supracallosal location to innervate parieto‐occipital cortical areas. Labeled collaterals ascend through the cortical layers to reach layer I, where grains in the superficial portion are found in a gradually decreasing rostrocaudal gradient of density that reaches the caudal pole of the hemisphere. Coronal sections at most levels contain a band of labeling in layer I that extends uninterrupted from the callosal sulcus at the midline to the banks of the rhinal sulcus laterally. Caudal retrosplenial and ventral temporal areas appear to be the only sectors of neocortex spared by the ubiquitous projection. Evidence for additional terminal distribution in deeper layers is found only in the dorsal and lateral sectors of the cortex rostral to the genu where sparsely labeled bands appear in layers III and V. The nearly exclusive distribution of VM's cortical afferents to layer I is compared and contrasted with multilaminar distributions of other “unspecific” cortical afferent fibers. HRP injected into VM labels neurons in a variety of structures at levels ranging from the frontal cortex to caudal medulla. Cell labelling in the globus pallidus, deep layers of the superior colliculus, cerebellar nuclei and the substantia nigra, pars reticulata suggest that VM is a point of convergence for several components of the extrapyramidal motor system. The nigrothalamic projection is topographic: medial and lateral districts of the pars reticulata are connected to medial and lateral districts of VM, respectively. A dorsal‐ventral association may also obtain. Cell labeling in the prefrontal cortex, the cortex along the rhinal sulcus, the lateral habenular nucleus, tegmental and medullary reticular formations, and parabrachial nuclei indicates that VM also receives projections from more heterogeneous sources.
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“The lateral habenula (LHb) is an epithalamic structure mediating communication between the forebrain and monoaminergic systems in the midbrain and hindbrain [38,39].”
From Deep brain stimulation for depression. (2022) · cites this paper as [38]
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“However, there are also less important projections to the ventromedial, dorsomedial, intralaminar, and ventral lateral geniculate regions (Graybiel 1974; Faull and Carman 1978; Herkenham 1979, 1986; Haroian et al. 1981; Sugimoto et al. 1981; Groenewegen 1988; Aumann et al. 1994, 1996; Sakai et al. 1996).”
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“…ventromedial and intralaminar/midline thalamic nuclei (e.g. Faull & Mehler, 1978; Beckstead et al., 1979; Gerfen et al., 1982; for reviews, see Groenewegen & Berendse, 1994; Gerfen & Wilson, 1996) that have widespread access to the cortex (Herkenham, 1979; Herkenham, 1980; Arbuthnott et al., 1990).”
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“Herkenham (1979) postulated that in the rat the nucleus ventro-medialis thalami is the exclusive pathway to the cortex.”
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“Of the thalamic nuclei surrounding VBC, the centrolateral, ventromedial, and posterior nuclei are believed to project to SmI (Jones and Leavitt 1974; McDaniel et al. 1978; White and D'Amicis 1977; Herkenham 1979; Kristt and Silverman, in preparation) and may have been partially affected during lesioning.”
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“The nucleus VM also receives inputs from the deep layers of the superior colliculus and the deep mesencephalic nucleus (Herkenham, 1979; Krout et al., 2001), brainstem structures known to receive inputs from the MI whisker region (Hattox et al., 2002).”
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Inhibitory nigral influence on cerebellar evoked responses in the rat ventromedial thalamic nucleus
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“Since this thalamic area is also known to receive a cerebellar input from the deep cerebellar nuclei, including the fastigial, interpositus, and dentatus (Angaut and Bowsher 1970; Kievit and Kuypers 1972; Chan-Palay 1977; Faull and Carman 1978; Haroian et al. 1981; Herkenham 1979; Kultas-Ilinsky et al. 1980a, b; Sugim…”
Proceedings of the British Pharmacological Society
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“Projections of PPN neurons to the ventromedial thalamus also have been reported ( Herkenham 1979 ).”
The Contribution of Thalamic Nuclei in Salience Processing
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“Midline thalamic nuclei receiving hypothalamic and brainstem inputs connect with widespread cortical areas (Herkenham, 1979; Kuramoto et al., 2015).”
BackgroundMedial Parabrachial Nucleus Is Essential in Controlling Wakefulness in Rats
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“PB neurons projected densely to midline and intralaminar thalamic nuclei of the rat (Herkenham, 1979; Krout and Loewy, 2000).”
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Thalamic projections to the hippocampal and entorhinal areas in the cat
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“VM neurons form an axon terminal field characterized by swellings that travel along cortical layer 1 (Herkenham, 1979; Arbuthnott et al., 1990; Rubio-Garrido et al., 2009; Cruikshank et al., 2012).”
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Thalamic input to motor cortex facilitates goal-directed action initiation
Takahashi, N., Moberg, S., Zolnik, T. A., Catanese, J., Sachdev, R. N. S., Larkum, M. E., & Jaeger, D. (2021) · Current Biology · doi:10.1016/j.cub.2021.06.089 · Cited by 60
“Additionally, it receives inputs from the cerebellar nuclei and other subcortical structures, notably the superior colliculus.(32,33) The thalamocortical projection from VM to cortical motor areas has been suggested to contribute to subcortical control of cortical activity during periods of movement preparation and in…”
Kilpatrick, I. C., & Phillipson, O. T. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90309-x · Cited by 49
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“These stereotaxic coordinates correspond to the medial agranular field of the motor cortex (Donoghue and Wise 1982; Brecht et al. 2004), which both projects to and receives input from the BZ and CZ of the rat motor thalamus (Herkenham 1979; Kincaid and Wilson 1996; Kuramoto et al. 2009).”
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Involvement of dopamine in circling responses to muscimol depends on intranigral site of injection
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Layer VII and the gray matter trajectories of corticocortical axons in rats
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Visceral region in the rat primary somatosensory cortex identified by vagal evoked potential
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“…Nakashima et al., 2000) as well as the intralaminar nuclei (Berendse and Groenewegen, 1991), the ventrolateral nucleus (VL) (Aldes, 1988) and the ventromedial nucleus (VM) (Herkenham, 1979; Desbois and Villanueva, 2001), have been excluded from the candidate list for the RVAprojecting nucleus.”
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“We also examined receptor status at several other DCN projection sites, including the red nucleus, pontine nuclei, and ventral thalamus (Flumerfelt et al., 1973; Caughell and Flumerfelt, 1977; Faull and Carman, 1978; Herkenham, 1979; Haroian et al., 1981; Flumerfelt and Hrycyshyn, 1985; Angaut et al., 1986; Border et…”
BackgroundAfferent connections of the subparafascicular area in rat
Wang, J., Palkovits, M., Usdin, T. B., & Dobolyi, A. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.11.010 · Cited by 40
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“Anatomically, it is well established that BG thalamic recipient nuclei, such as the ventral medial nucleus, which receive inputs from the SNr, innervate the superficial cortical layers [66] and therefore might have a more prominent action on neurons lying in superficial layers.”
Jeljeli, M., Strazielle, C., Caston, J., & Lalonde, R. (2003) · Neuroscience Research · doi:10.1016/s0168-0102(03)00224-4 · Cited by 43
Miller, P. J., & Záborszky, L. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6522 · Cited by 43
“ventromedial, and ventrolateral thalamic nuclei, which are known to project to the anterior cingulate, to the medial precentral areas, and especially to the frontal motor cortex, areas that were all damaged by the two large injections into the frontal cortex (1, 15, 22, 34, 41, 46, 48, 70).”
Klockgether, T., Schwarz, M., Turski, L., & Sontag, K. ‐. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-06-01702.1986 · Cited by 43
“…thalamic nucleus (VM) is characterized by its extensive neocortical projection and its complex afferentation, consisting of converging inputs from several brain regions that are supposed to be involved in motor control (Chevalier and Deniau, 1982; Herkenham, 1979; MacLeod and James, 1984).”
BackgroundResultInfluentialOrganization of the zona incerta in the macaque: A nissl and golgi study
Ma, T. P., Hu, X., Anavi, Y., & Rafols, J. A. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903200302 · Cited by 43
Connections of the mediodorsal nucleus of the thalamus in the tree shrew. I. Afferent connections
Sapawi, R. R., & Divac, I. (1978) · Neuroscience Letters · doi:10.1016/0304-3940(78)90165-9 · Cited by 43
Consolazione, A., Priestley, J. V., & Cuello, A. C. (1984) · Brain Research · doi:10.1016/0006-8993(84)90113-6 · Cited by 42
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“The ipsilateral thalamus was sectioned coronally at 60 lm to confirm the presence of retrogradely labeled neurons in the ventrolateral, ventromedial, and other nuclei that project to rat MI (Herkenham 1979; Aldes 1988; Mitchell and Cauller 2001).”
MethodBilateral tectal projection of single nigrostriatal dopamine cells in the rat
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Neurochemical Anatomy of Movement Disorders
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Miller, R. L., Knuepfer, M. M., Wang, M. H., Denny, G. O., Gray, P. A., & Loewy, A. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.05.049 · Cited by 40
Direct cortical projections to the parabrachial nucleus in the cat
Yasui, Y., Itoh, K., Takada, M., Mitani, A., Kaneko, T., & Mizuno, N. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902340106 · Cited by 40
The organization of thalamic projections to the parietal cortex of the Virginia opossum
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Cognitive consilience: Primate non-primary neuroanatomical circuits underlying cognition
Solari (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00065 · Cited by 41
Nociceptive Processing by Anterior Cingulate Pyramidal Neurons
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“…autoradiographic localization of labeled terminals (Herkenham 1978); however, other MITN project to layer I, including the ventromedial nucleus (Herkenham 1979; Minciacchi et al. 1986), centrolateral nucleus (Cunningham and Levay 1986), and parafascicular nucleus (Royce and Mourey 1985; Royce…”
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Ebner, F. F., & Kaas, J. H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00024-3 · Cited by 38
Short-term Plasticity in Thalamocortical Pathways: Cellular Mechanisms and Functional Roles
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Organization of the Thalamocortical Complex and its Relation to Sensory Processes
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Novel targets in deep brain stimulation for movement disorders
Baumgartner, A. J., Thompson, J. A., Kern, D. S., & Ojemann, S. G. (2022) · Neurosurgical Review · doi:10.1007/s10143-022-01770-y · Cited by 39
“As an important modulator of motor output, the GABAergic projection neurons in the SNr mainly facilitate the inhibition and disinhibition of motor thalamic nuclei and the superior colliculus [81, 82].”
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Ultrastructure of degenerating cerebellothalamic terminals in the ventral medial nucleus of the cat
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“Although the latter two groups of investigators maintain that the fastigial nucleus is the main source of cerebellar afferents to the VM in the cat, the possibility has not been ruled out that other cerebellar nuclei contribute to this projection as well (Chan-Palay, 1977; Herkenham, 1979).”
BackgroundMethodKlockgether, T., Schwarz, M., Turski, L., Wolfarth, S., & Sontag, K. ‐. (1985) · Experimental Brain Research · doi:10.1007/bf00235872 · Cited by 37
“1980) pathway arising from the substantia nigra, pars reticulata (SNR), one of the output stations of the basal ganglia (Beckstead et al. 1979; Bentivoglio et al. 1979; Clavier et al. 1976; Herkenham 1979).”
InfluentialMonconduit, L., & Villanueva, L. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04160.x · Cited by 36
“Desbois & Villanueva, 2001), sparing the prefrontal cortices that are targets of neurons located within the medial aspect of the VM (Herkenham, 1979; Deniau et al., 1994).”
BackgroundMethodInfluentialSerotoninergic projections from the dorsal raphe nucleus to the nucleus submedius in the rat and cat
Matsuzaki, S., Takada, M., Li, Y.-Q., Tokuno, H., & Mizuno, N. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90509-e · Cited by 36
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Basal ganglia outflow pathways and circling behaviour in the rat
Leigh, P. N., Reavill, C. A., Jenner, P. G., & MARSDEN, C. D. (1983) · Journal of Neural Transmission · doi:10.1007/bf01249122 · Cited by 36
“The efferent projections from VM thalamus pass predominantly to the cerebral cortex (Herkenham, 1979) with slight evidence of projections to the midbrain reticular formation.”
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Layer 1 of somatosensory cortex: an important site for input to a tiny cortical compartment
Ledderose, J. M. T., Zolnik, T. A., Toumazou, M., Trimbuch, T., Rosenmund, C., Eickholt, B. J., Jaeger, D., Larkum, M. E., & Sachdev, R. N. S. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad371 · Cited by 39
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Colocalization of mu-opioid receptors and activated G-proteins in rat cingulate cortex.
Vogt, L. J., Sim‐Selley, L. J., Childers, S. R., Wiley, R. G., & Vogt, B. A. (2001) · PubMed · Cited by 34
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Anatomy and Development of Multispecific Thalamocortical Axons
Clascá, F., Porrero, C., Galazo, M. J., Rubio‐Garrido, P., & Evangelio, M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801393-9.00004-9 · Cited by 33
Developmental divergence of sensory stimulus representation in cortical interneurons
Kästli, R., Vighagen, R., van der Bourg, A., Argunşah, A. Ö., Iqbal, A., Voigt, F. F., Kirschenbaum, D. S., Aguzzi, A., Helmchen, F., & Karayannis, T. (2020) · Nature Communications · doi:10.1038/s41467-020-19427-z · Cited by 37
Striatal dopamine and glutamate receptors modulate methamphetamine-induced cortical Fos expression
Gross, N. B., & Marshall, J. F. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.04.023 · Cited by 33
Nitric oxide synthase-containing projections to the ventrobasal thalamus in the rat
Usunoff, K. G., Kharazia, V., Valtschanoff, J. G., Schmidt, H. H. H. W., & Weinberg, R. J. (1999) · Anatomy and Embryology · doi:10.1007/s004290050278 · Cited by 33
“For example, the spread of the tracer into the ventromedial nucleus in R1663 produced anterograde labeling of thalamocortical terminals in layer I of the cerebral cortex ( Herkenham 1979 ).”
BackgroundSharp, F. R. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902240207 · Cited by 33
Mango, D., Bonito-Oliva, A., Ledonne, A., Nisticò, R., Castelli, V., Giorgi, M., Sancesario, G., Fisone, G., Berretta, N., & Mercuri, N. B. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.08.010 · Cited by 33
Mango, D., Bonito-Oliva, A., Ledonne, A., Cappellacci, L., Petrelli, R., Nisticò, R., Berretta, N., Fisone, G., & Mercuri, N. B. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.08.022 · Cited by 32
“Thus, the inhibition exerted by MSNs on SNpr GABAergic neurons promotes the activity of glutamatergic thalamic neurons, maintaining an excitatory synaptic drive to the cerebral cortex (Beckstead and Frankfurter, 1982; Bodor et al., 2008; Chuhma et al., 2011; Deniau et al., 1978; Herkenham, 1979; Nishimura et al., 1997…”
Regulation of cerebello-cortical transmission in the rat ventromedial thalamic nucleus
MacLeod, N. K., & James, T. A. (1984) · Experimental Brain Research · doi:10.1007/bf00235285 · Cited by 32
“The VM has additionally been shown by neuroanatomical tracing methods to receive inputs from Globus Pallidus, Superior Colliculus, Mesencephalic Reticular Formation and the Entopeduncular Nucleus ( Herkenham 1979 ).”
BackgroundMethodResultInfluentialA GABA immunocytochemical study of rat motor thalamus: Light and electron microscopic observations
Sawyer, S. F., Martone, M. E., & Groves, P. M. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90152-e · Cited by 32
Pritzel, M., & Huston, J. P. (1981) · Behavioural Brain Research · doi:10.1016/0166-4328(81)90007-3 · Cited by 32
Thalamic commissural connections in the cat
Rinvik, E. (1984) · Neuroscience Letters · doi:10.1016/0304-3940(84)90041-7 · Cited by 32
Starr, M. S., & Kilpatrick, I. C. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90074-9 · Cited by 32
Minciacchi, D., Bentivoglio, M., Molinari, M., Kultas‐Ilinsky, K., Ilinsky, I. A., & Macchi, G. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902520107 · Cited by 31
Topical Review: Basal Ganglia: Functional Anatomy and Physiology. Part 1
Afifi, A. K. (1994) · Journal of Child Neurology · doi:10.1177/088307389400900306 · Cited by 33
Delfs, J. M., Ciaramitaro, V. M., Soghomonian, J., & Chesselet, M. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00470-x · Cited by 31
Collateral projection from the substantia nigra to the striatum and superior colliculus in the rat
Takada, M., Li, Z. K., & Hattori, T. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90258-8 · Cited by 31
Chesselet, M., Chéramy, A., Romo, R., Desban, M., & Glowinski, J. (1983) · Experimental Brain Research · doi:10.1007/bf00237203 · Cited by 31
“The increased (3H)-DA release occurring in the ipsilateral striatum could be mediated through direct pathways to the SN (Herkenham 1979) or the CN (Royce 1978; Herkenham 1979; Sato et al.”
InfluentialEfferent Connections of the Habenular Nuclei in the Rat
Herkenham, M. A., & Nauta, W. J. H. (1979) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-7920-1_17 · Cited by 30
Haque, T., Yamamoto, S., Masuda, Y., Kato, T., Sato, F., Uchino, K., Oka, A., Nakamura, M., Takeda, R., Ono, T., et al. (2010) · Brain Research · doi:10.1016/j.brainres.2010.05.034 · Cited by 30
“Similar patterns of jaw-movements have been reported in the monkey after stimulations of the MIoro (Hatanaka et al., 2005) or stimulations of the primary face motor cortex (Huang et al., 1989).”
BackgroundInfluentialMuramatsu, S., Yoshida, M., & Nakamura, S. (1990) · Neuroscience Research · doi:10.1016/0168-0102(90)90011-3 · Cited by 30
Rubio‐Garrido, P., Pérez-de-Manzo, F., & Clascá, F. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.036 · Cited by 30
Metadata
- Authors
- Herkenham, M.
- Affiliations
- Massachusetts Institute of Technology (US)
- Corresponding author
- Herkenham, Miles
- ORCID
- Herkenham, Miles
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1979-02
- Volume
- 183
- Issue
- 3
- Pages
- 487-517
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2000437871
- Cited by
- 477
- References
- 69
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 6 · 2023: 2 · 2022: 5 · 2021: 6 · 2020: 5 · 2019: 2 · 2018: 7 · 2017: 7 · 2016: 8 · 2015: 4 · 2014: 6 · 2013: 3 · 2012: 6
- FWCI
- 15.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- ventromedial thalamic nucleus, extrapyramidal system, globus pallidus, substantia nigra pars reticulata, superior colliculus, cerebellar nuclei, lateral habenula, reticular formation
- MeSH terms
- Animals, Autoradiography, Brain Mapping, Cerebral Cortex, Electrophysiology, Female, Globus Pallidus, Horseradish Peroxidase, Male, Neural Pathways, Substantia Nigra, Thalamic Nuclei, Rats
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