Primate basal ganglia

The basal ganglia system is a major cerebral system that has only recently been recognized. In the past, part of it was presented as "motor" or "extrapyramidal", complementary to the corticospinal (pyramidal) system. Contrary to what was thought, the basal ganglia sytem has no direct output to the spinal cord. The motor effects are exerted through the motor cortex and the pyramidal system. The unilateral effects are thus controlateral. The basal ganglia system participates in much more than motor functions.

Definition and content

The basal ganglia,in the basal part of the brain, are a set of subcortical cerebral elements in interaction together and with parts of the thalamus and cortex. For history, see Basal ganglia. The term ganglion is not really adequate. Terminologia anatomica (1998), the international authority for anatomical naming retains "nuclei basales". The International Basal Ganglia Society (IBAGS) considers as basal ganglia, the striatum, the pallidum (with two nuclei), the substantia nigra (with two distincts parts) and the nucleus subthalamicus. To this is added the central complex (centre median-parafascicular) (Percheron et al. 1991, Parent and Parent, 2005) and for some the pedunculopontine complex (Mena-Segovia et al. 2004). This ensemble must not be seen as a collection but as a system. Connections are not simple "arrows" between "boxes". The exact patterns within and between elements are important.

Corticostriatal connection

The whole system starts as a major output of the cortex, about the same size as the corticopontine system opening the cerebellar system. The cortico-striatal connection represents a significant portion of the cortical output. Almost every part of the cortex, except for the primary visual and auditory cortices, send axons to the striatum. The origin ot the connection is in the pyramidal neurons of the layer V of the cortex. From the motor cortex at least, corticostriate contributors are collaterals of axons descending lower in the nervous system.In primates only, the majority of corticostriate axons are thin and unbranched until they arrive in the sensorimotor striatum (Parent and Parent,2006). The cortico-striate connection is not topologically simple as was initially described by Kemp and Powell were teh fortal lobe projected anteriofy,and the occipitotemporal lobes. this remains grossly true but the distribution is much more complex. One small cortical places can send terminal arborisations to several and distal striatal places (Goldman and Nauta, 1977, Selemon and Goldman-Rakic, 1985).

The corticostriate connection is the first in the chain where there is a strong reduction in numbers between emitter and receiver neurons (Percheron et al. 1987).This means that if each striatocortical neurons has its own message, this will be mixed or compressed leading to a lesser definition of the arrriving data.

Basal ganglia core

The basal ganglia core includes the striatum and its direct targets reached, through the striato-pallido-nigral bundle, the two nuclei of the pallidum and the substantia nigra.

Striatum

The striatum is a huge neuronal telencephalic mass located close to the lateral cerebral ventricles. In primates, it has four neuronal genera: spiny (96%), leptodendritic (2%), spidery (1%) neurons and microneurons(1%) . The dendritic arborisations of the spiny neurons are spherical. Their diameter depends on the animal species. Spines are of the same type than those of two other (telencephalic) acanthodendritic (acanthos means spine) genera, the pyramidal neurons of the cerebral cortex and the spiny neurons of the amygdala. Most of these spines synapse with cortical afferents. Their axons have abundant and dense initial axonal collateral participating in local circuitry. The further part is long and myelinated. The spiny neurons are GABAergic. The leptodendritic neurons (or Deiter's), stained for parvalbumin, have all the morphological properties of the pallidal neurons. The spidery neurons are specific to primates. They have a big soma and short dendritic and axonal branches. They are the cholinergic neurons of the primate, with a morphology entirely different from that of the cholinergic neurons of non-primates. They are the "tonically active neurons" or TANs

The long oblique split of the striatum by the internal capsule creates the classic division into putamen, caudate and fundus. In fact the striatum is a continuous mass having a toric topology. Th gross anatomical division does not to correspond exactly with the presently accepted anatomofunctional subdivision of the striatum in primates. There are several levels of organization of the striatum. One level of organisation is brought by the differentiated topographical endings of the corticostriatal axons. Endings of axons from the central region of the cortex, primary somatosensory, motor, premotor (Künzle 1975 and several other papers), accessory motor and anterior parietal constitute a sensorimotor territory (or sensorimotor striatum) essentially putaminal, but which does not cover the total extent of the putamen. Conversely it includes intracapsular fringes and the inferolateral border of the caudate . To this is opposed an associative territory, essentially caudate, above all orally and dorsally, but which does not cover the entire caudate volume. The separation between the two sensorimotor /associative territories may be clearcut and observed using calbinding immunochemistry (the sensorimotor territory being negative). The isolation of a third ventral striatal part often said qualified as "limbic" is more difficult. Only one part is distinctive, the "nucleus accumbens" having same morphological features but particular immunostaining. Above all, it selectively receives alone axons from the subiculum. Another level of organisation is that of "compartments". Histochemistry has indeed shown inhomogeneities with regards to the distribution of different molecules. The major compartment, the matrix as its name indicates is considered as the basic element.It contains contrasting islands or striosomes that contain opiate receptors (Pert, ) and stain for acetyl cholinesterase. This opposition, obvious in the head of the caudate, is not clear everywhere. Every striatal part has not distinct striosomes. These have no links to amygdalar afferents in primates. Striosomes would rather represent the insular segregation of particular frontal axonal endings (posterior orbitofrontal/anterior insula and mediofrontal/anterior cingulate cortex) (Eblen and Graybiel,1995). Matricial neurons are those contained in the matrix. Striosomal neurons are those contained the striosome. They have been opposed as sources of distinctive efferences, which will be shown below no to be true.

Pallido-nigral ensemble

This comprises the two nuclei of the pallidum and the pars lateralis and the pars reticulata of the "substantia" nigra (TA, yet not a substance but a nucleus). One noticeable property of this ensemble is that on one of its elements receives cortical afferents. By no ways has the pallidum the shape of a globe. Cecile and Oskar Vogt (1941) simplified the case by selecting pallidum, also offered by the Terminologia Anatomica (1998). They also proposed nigrum that may be replaced by nigra. The whole set is made up the same neuronal components. The majority is made up of large neurons, strongly stained for parvalbumin, having very large dendritic arborisations (much larger in primates than in rodents) with straight and thick dendrites of the leptodendritic family (Yelnik et al. 1987). Only the shape and direction of the dendritic arborizations differ in pallidum and nigra. The synaptology of the set is uncommon. The dendrites of the pallidal or nigral axons are entirely covered by synapses without any apposition of glia. More than 90% of synapses are from striatal origin (Di Figlia et al. 1982 ) In spite of the presence of various appendages at the distal extremity of the pallidal neurons (di Figlia et al. 1982, François et al. 1984) that could act as elements of local circuitry, there are weak or no functional interrelations between pallidal neurons (Bar-Gad et al 2003)

Lateral pallidum (external globus pallidus, GPe)

The lateral pallidum is very extended. It is flat and curved. In the pallidum, the threee-dimensional shape of arborisations is discoid and flat. The arborisations are parallel to one other and to the lateral border of the pallidum. They are thus perpendicular to the striatal afferences. As they have a very large extent, they may get contact with a large quantity of striatal axons. in addition to the striatopallidal afference it receives it receives a major connection from the subthalamic nucleus. It also receives dopaminegic afferences from the pars compacta.

Lateral pallidal neurons are often multitargets and may correspond to several hodotypes (neuronal varieties according to their targets). From Sato et al. (2000), in macaques, the striatal neurons which projects to three consecutive targets (medial pallidum, nigra reticulata and subthalamic nucleus) are 13,2%. The neurones projecting to the medial pallidum and subthalamic targets are 18,4%. Those projecting to the subthalamic nucleus and nigra reticulata 52,6%. The subthalamic nucleus is thus in 84,2% of the cases the target of lateral pallidal neurons . The lateral pallidal neurons however also sends axons in the other direction, that of the striatum in only 15.8%. The subthalamic nucleus is the priviledged target of the lateral pallidum from which it receives the majority of its afferences. Contrary to two other elements of the basal ganglia core, it is not a source of output from the system since its sends its axons only inside the basal ganglia. To some extent it may be seen as an inner regulator, forming along with the subthalamic nucleus a regulating circuit. Its mediator is GABA.

Medial pallidum (internal globus pallidus, GPi)

In addition to the massive striatopallidal connection, the medial pallidum receives a dopamine innervation from the nigra compacta. It sends its axons to the lateral region of the thalamus (VO), the pars media of the central complex (see below) and the pedunculopontine complex. The medial pallidum is not the equivalent of the entopeduncular nucleus of nonprimate. This indeed do not have a separate territory in the thalamus as it ends together with nigral afferences. In this respect the entopeduncular nucleus is rather a lateral intracapsular part of the nigra.

Nigra pars lateralis (SNl)

The two parts of the nigra that belong to the basal ganglia core are the pars lateralis and the pars reticulata receiving a dense projection from the striato-pallido-nigral bundle and having the same structure as that of pallidal neurons. The nigral neurons are also sparsely branched and long (Yelnik, et al. 1987). The difference between pallidal and nigral neurons is only in the three-dimensional extension of their dendritic arborizations (François et al. 1987). Nigral dendrites however, as well as pallidal, tend to be perpendicular to the arriving stiatal axons. The particular synaptology is also the same. The pars lateralis is the most lateral part of the nigra.It is frequently not considered separately as the main difference from the pars reticulata is that it sends axons to the superior colliculus (François et al. 1984). This yet a sufficient reason.

Nigra pars reticulata (SNr)

In addition to the massive striatopallidal connection, the nigra reticulata receives a dopamine innervation from the nigra compacta and glutamatergic axons from the pars parafascicularis of the central complex. It sends nigro-thalamic axons. There is no conspicuous nigrothalamic bundle. Axons arrive medially to pallidal afferences to the anterior most and medial part of the lateral region of the thalamus the nucleus ventralis anterior (VA, differentiated from VO receiving pallidal afferences).

Striato-pallidonigral connection

The striato-pallidonigral connection is a very particular one in the whole brain. It engages a considerable number of fine striatal axons (see Percheron et al. 1984). The striato-pallido-nigral bundle is made up of very numerous thin, fewly myelinated axons from the striatal spiny neurons. It strongly stains for iron using Perls technique.

Hodology to targets

There have been disputes concerning the distribution of striatal axons to the different targets. During last decades most reasoning was based on an opposition between a direct and indirect circuit. This was founded on selected anatomical connections. The lack of references to the fact that quoted data had been acquired on nonprimate or primate species made things confuse. The basal ganglia system still changes between the platyrhinians and the cercopithecidae. A recent study in macaque (Levesque and Parent et al. 2005) has drastically changed the situation. Spiny neurons have generally several targets. This is not the fact of an archaic pattern since this is found in 90% of the cases in macaque monkeys versus 63,6% in the rat. Virtually all striatal axons have the lateral pallidum (the most voluminous) as a first target. 24/27 axons project to the three consecutive targets, lateral pallidum, medial pallidum and nigra (lateralis and reticulata). There are no striatal axons projecting to the single medial pallidum, single nigra or both. The only difference in the axonal hodology of matricial and striosomal axons is that striosomal axons cross the whole lateral to medial extent of the nigra. They emit 4 to 6 (in macaques) vertical collateral, forming vertical columns entering deep inside the pars reticulata. The matrical neurons emit more sparsely branched axons. This general pattern of connectivity raises new problems. The main mediator of the striato-pallidonigral system is GABA but with comediators. Since Haber and Elde (1981),it is known that the lateral pallidum stains for met-enkephalin, the medial for substance and /or dynorphin and the nigra for both. This means that a single axons is able to concentrate different comediators depending on the target. This considerably modifies several decades old schemes.

Geometry of the connection

This connection is a further reduction in the number of transmitter to receiver neurons, strongly reducing the precision of the arriving message. The geometry of the connection between striatal axons and pallidonigral dendrites is very particular.The pallidal dendritic arborisations are very large discoidal. There principal plane is perpendicular to others. They are all parallel to the lateral border of the pallidum (Yelnik et al. 1984) and thus are perpendicular to the axis of the afferences (Percheron et al. 1984). Since the pallidal discoidal discs are thin they are crossed only for a short distance by striatal axons. These however emit perpendicular branches participating to flat bands parallel to the lateral border.

Synaptology and interpretation

The synaptologyof the striato- pallidonigral connection is so pecliar as to be recognized easily. Pallidonigral dendrites are entirely covered with synapses without any apposition of glia. More than 90% of the synapses are of striatal origin.

Nigra pars compacta (SNc) and nearby dopaminergic elements

Sensu stricto, the pars compacta is a part of the core of basal ganglia core since it receives directly synapses from striatal axons through the striatopallidonigral bundle. The long ventral dendrites of the pars compacta indeed plunge deep in the pars reticulata where they receive synapses from the bundle. However, its constitution contrasts with the rest of the nigra. Aging leads to its blackening, by deposit of melanin, visible by naked eye. This is the origin of the name of the ensemble 'substantia nigra' meaning black substance. The densely distributed neurons of the pars compacta are have larger and thicker dendritic arborizations than those of the pars reticulata and lateralis. This is also the case for neurons located more dorsally and posteriorly in the tegmentum that did not form true nuclei. The "cell groups A8 and A10" are spread inside the peduncule (François et al. 1999). They are not known to receives striatal afferences and are not in topographical position to do so. The dopaminergic ensemble is thus not homogeneous. This is another major difference with the pallidonigral ensemble. The efferent dopaminergic connection attract (at least in physiopathological models) the attention more than the input. This explains its intermediate position in our plan. The dopaminergic neurons have been the source of a considerable literature. They end intensively in the striatum and also in almost all elements of the basal ganglia system: pallidum,nigra, subthalamic nucleus. The role of these dopaminergic neurons

Regulators of the basal ganglia core

Subthalamic nucleus, or corpus Lyuisi

As indicated by its name0, the subthalamic nucleus is located below the thalamus, dorsally to the substantia nigra and medial to internal cpasule. The subthalamic nucleus is of homogeneous aspect and lenticular inrorm ,in transverse sections. It is made up of a particular neuronal species having rather long ellipsoid dendritic arborisations mimicking the shape of the whole nucleus (Yelnik and Percheron,1979). There are also about 7,5% of GABA microneurons participating in the local circuitry (Levesque and Parent 2005). The subthalamic nucleus receives its main afference from the lateral nucleus of the pallidum. Another afference comes from the cerebral cortex particularly from the motor cortex (which is too neglected in the models). Subthalamic axons leave the nucleus dorsally.Their targets are at first the elements of the core of the basal ganglia: the substantia nigra medially and the medial and lateral nuclei of the pallidum lateraly. The main afference of the nucleus is the lateral nucleus of the pallidum (external segment of the globus pallidus (GPe) with which it makes a tight regulatory loop ( STN-GPe circuit). It utilizes the excitatory neurotransmitter glutamate. This gives it a particular interest since the striatopallidal, and the pallido-subthalamic connections are inhibitory (GABA). The intervention of its lesions resulting in hemiballismus is known for long. The role subthalamic nucleus is over exploited in models. Stereotactic stimulation of the nucleus suppress most of the symptoms of the Parkinson' syndrome particularly dyskinesia induced by dopatherapy.

Central complex (C)

The central complex is the so-called centre-médian- parafascicular complex. In upper primates, starting from the cercopithecidae, it is in fact made up not of two but of three parts with their own neuronal species (Fenelon et al. 1994). From there,two opposed interpretations were proposed concerning the belonging of the intermediate part: either to the centre médian(the Vogts, 1941) or to the parafascicular nucleus (Niimi et al. 1960). This is undecidable. It has thus been proposed to group the three elements together in the regio Centralis, since it belongs to classical nuclei and to name them from medially to laterally: n. centralis pars parafascicularis, pars media and pars paralateralis. The whole is parvalbumin rich. The first two medial parts are acetylcholinesterase rich. They are the source of the major, centralo-striatal, part of the thalamo-striatal connection, with glutamate as the mediator. The main afference of the pars media is the medial pallidum. This pars media sends axons to the matrix compartment of the sensorimotor striatum through an important bundle (François et al. 1991). The pars media is a part of the subcortical Nauta-Mehler's circuit (striatum-medial pallidum-pars media-striatum). The pars parafascicularis receives afferences from the substantia nigra and the superior colliculus. The pars parafascicularis sends axons to the associative striatum . The same sends also axons to the substantia nigra. There are thus strong interconnections of the complex with the basal ganglia. The pars paralateralis has essentially cortical relation particularly with the motor cortex. The structure of the complex is different from that of the close intralaminar formation. It has different connections. This leads today to remove the central complex from intralaminar elements and to link it to the basal ganglia complex. It may be classified among the regulators of the core. There are few physiological data. For Matsumoto et al. (2001) the axons of the complex would supply striatal neurons with information about behaviorally significant sensory events.

Pedunculopontine complex

The pedunculopontine complex is not a primary part of the basal ganglia. It is a part of the reticulate formation having strong interrelations with the basal ganglia system. As indicated by its name, it is located at the junction between the pons and the cerebral peduncle, lateral to the decussation of the brachium conjunctivum. Mena-Segovia et al. (2004) have analysed the reason why this complex should be linked in a way or another to the basal ganglia systel. The complex receives direct afferences from the medial pallidum. One part of its axons are cholinergic. It sends axons to the pallidal territory of the lateral region VO. A review on its role in the system and in diseases is given by et al. 1999, Pahapill and Lozano (2000). Its stimulation alleviates akinesia independantly of dopaminergic mechanisms (Jenkinson et al. 2006)

Outputs of the basal ganglia system

Many connections of the basal ganglia are between elements of the basal ganglia. There are few output external targets. One is the superior colliculus, from the nigra lateralis. There are two major distinct output subsystems in direction to the thalamus and from there to the cortex.

Nigra lateralis to superior colliculus

The nigra lateralis made up of the same cell type than the pars reticulata differ by its targets. The connection with Graybiel, 1978 in the cat, Carpenter François et al.

Medial pallidum to thalamic VO and cortex

Axons from the pallidum to the thalamus form the ansa lenticularis and the fasciculus lenticularis, making in fact a single entity. The axons arrive at the medial face of the pallidum; from there, they cross the internal capsule where they form the comb system (Kamm system of Edinger, 1900). The axons arrives at the lateral border of the subthalamic nucleus. Passing above it they constitute the field H2 of Forel (1877). From there, they curve down towards the hypothalamus. At field H, they turn abruptly and go up in a dorsolateral direction (forming H1 field) and reach the ventral border of the thalamus. This is not the place for describing motor thalamic anatomy (see thalamus). The axons from the two output sources of the basal ganglia core to the thalamus, starting from cercopidae, are located without mixture in front of the the cerebellar territory (VIm or VL). Pallidal and nigral terminal arborisations do not mix. Pallidal axons have their own thalamic territory, everywhere separated from the cerebellar and from the nigral. To mark this separation the pallidal-receiving nucleus is named nucleus ventralis oralis (VO)(higher than Olsewski's VLo) in order to differentiate it from the nigral VA . The VO nucleus remains everywhere lateral in macaques and humans. It stained for calbindin and acetylcholinesterase. The axons ascend in the nucleus where they emit branches that widespread distribute "bunches" of axonal branches (Arrrechi-Bouchhiouia et al.1996,1997). The distribution is such that if any somatotopical organisation exists, it may only be poor. The thalamocortical neurons of VO go preferently to the supplementary motor cortex (SMA), to preSMA and to a lesser extent to the motor cortex. The pallidothalamic neurons also give branches to the pars media of the central complex (see above). This sends axons to the premotor, accessory motor cortex.

Nigra reticulata to thalamic VA and cortex

Axons go up dorsally without forming a clear bundle. They reach the inferior border of the thalamus. The nigral territory (VA) is medial to the pallidal. It is crossed by the mammillothalamic bundle.In monkey the nucleus is usually divided into a magnocellular part, medial and close to the mammillothalamic bundle, and a pars mediocellularis.In human, the majority of the nucleus is composed of the magnocellular component. In any case in macaques the afferences from the nigra do not care about these cytoarchitectonic subdivision.In addition to the nigral afference, VA receives axons from the tectum (superior colliculus) and from the amygdala (basal complex). Thalamocortical axons from VA send their axons to a particular set made up of the oculomotor cortex (FEF and SEF), the frontal and the cingular cortex. This indicates that this output subsystem likely participate in visuomotor circuits.

Models of the basal ganglia system

The description done above is anatomical and follows a simple topological hierarchical rule. Systemic representations very frequently use the "box-and-arrow model" in which boxes are elements and arrows connections.This rigidifies the boxes (all presupposed to be homogeneous and close) and the connections with no cardinal (no defined numbers of axons) and no topological varieties. One of the most famous model (Albin et al. that they confessed later to have been too simplist) selected two criteria: the inhibitory/excitatory character and the mediator involved, without no consideration about real anatomical trajectories or geometries. The cortex was one box. For the thalamus only a VA/VL complex was used.The following model (in several forms of Alexander and Crutcher ),often said to be the same as the preceding, which is only partly thr case. It is based on some true anatomical connections to describe x distinct loops. The first problem is that it does not fit with corticostriatal anatomy (see above). As repeatedly proven, the corticostriate connection does not follow the Kemp and Powell topography ( ). Among the proposed separate loops (that are not loops but circuits) few have a possible reality. .

References

• Arecchi-Bouchhioua P, Yelnik J, Francois C, Percheron G, Tande D.(1996) 3-D tracing of biocytin-labelled pallido-thalamic axons in the monkey. Neuroreport.7:981-984.id=PMID 8804035
• Arrechi-Bouchhioua, P., Yelnik, J., Percheron, G., Tande, D. (1997) Three dimensional morphology and distribution of pallidal axons projecting to both the lateral region of the thalamus and the central complex in primate. Brain Res. 754:311-314 id=PMID 9134990
• Bar-Gad, I, Heimer, G., Ritov, Y, Bergman, H. (2003) Functional correlations between neighbouring neurons in the primate globus pallidus are weak or non existent. J. Neurosci.23:4012-4016 id=PIMB 12764036
• Bar-Gad, I, Morris,G., Bergman, H. (2003) Information processing, dimensionality, reduction and reinforcement in the basal ganglia. Progr. Neurobiol.71:439-477
• Cossette, M., Lecomte, F., Parent, A. (2005) Morphology and distribution of dopaminergic intrinsic to the human striatum. J.Chem. Neuroanat.,29: 1-11
• diFiglia, M., Pasik, P., Pasik, T. (1982) A Golgi and ultrastructural study of the monkey globus pallidus. J. Comp.Neurol. 212:53-75
• author= Eblen, F, Graybiel;, A.M. (1995) title=Highly restricted origin of prefrontal cortical inputs to striosomes in monkeys.| journal= J. Neurosci.| issue=15 | pages=5999-6013 | year=1995 | id=PIMB 7766184
• Fenelon, G., Percheron, G., Parent, A., Sadikot, Fenelon, G., Yelnik, J. (1991) Topography of the projection of the central complex of the thalamus to the sensorimotor striatal territory in monkeys. J. C. Neurol. 305: 17-34 id=PIMB 1709648
• Fenelon, G. Yelnik, J., François, C. Percheron, G. (1994) Central complex of the thalamus: a quantitative analysis of neuronal morphology. J. Comp. Neurol. 342: 463-479 id=PIMB 8021346
• Francois C, Percheron G, Yelnik J.(1984) Localization of nigrostriatal, nigrothalamic and nigrotectal neurons in ventricular coordinates in macaques.Neuroscience.13:61-76.id=PMID 6387531
• François, C., Percheron, G., Parent, A., Sadikot, Fenelon, G., Yelnik, J (1991) Topography of the projection from the central complex of the thalamus to the sensorimotor striatal territory in monkey. J. Comp. Neurol. 305:17-34
• François, C., Tande, D., Yelnik, J., and Hirsch, E.| title=Distribution and morphology of nigral axons projecting to the thalamus in primates.| journal=J. Comp. Neurol.| issue=447 | pages=249-260 | year=2002 | id=PMID 119984819 }}
• François, C., Tande, D., Yelnik, J., Hirsh, E.C. (2002) Distribution and morphology of nigral axons projecting to the thalamus in primates. J.Comp. Neurol. 447:249-260 PMID 119984819.
• Goldman, P.S. and Nauta, W.J. (1977) An intricately patterned prefronto-caudate projection in the rhesus monkey. J. Comp.Neurol. 72:369-386 id=PIMB401836
• Haber, S. and Elde, R. (1981) Correlation between Met-enkephalin and sustance P immunoreactivity in the primate globus pallidus. Neurosci. 6:1291-1297
• Jenkinson, N., Nandi, D., Oram, R., Stein, J.F., Aziz, T.Z. (2006) Pedunculopontine nucleus electric stimulation alleviates akinesia independantly of dopaminergic mechanisms. Neuroreport 17:639-641
• Kimura, M., Yamada, H. and Matsumoto title= Tonically active neurons in the striatum encode motivational contexts of actions. ((2003)). Brain and develop.issue=25: S20–S23. PMID. {{cite journal}}: Check date values in: |year= (help); Missing or empty |title= (help); Missing pipe in: |author= (help)CS1 maint: multiple names: authors list (link) CS1 maint: year (link)
• Künzle, H. (1975) Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. an autoradiographic studyin Macaca fascicularis. Brain. Res. 88:195-209 id=PMID 50112
• Levesque, M., Bédard, A., Cossette, M., Parent, A. (2003) Novel aspets of the chimical anatomy of the striatum and its efferent projections. . Chem. Neuroanat. 26: 271-281
• Levesque, M. and Parent, A. (2005) The striatofugal fiber system in primates:a reevaluation of its organization based on single-axon tracing studies. PNAS.102:
• Levesque, J.C. and Parent, A; (2005) GABAergic interneurons in human subthalamic nucleus. Mov. Disord. 20:574-584
• Matsumoto, N., Minamimoto, T, Graybiel, A.M, Kimura, M. (2001) Neurons in the thalmic CN-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J. Neurophysiol. 85: 960-976
• Munro-Davies, L.E., Winter, J., Aziz, T.Z., Stein, J.F (1999) The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia. Exp. Brain Res. 129: 511-517
• Niimi, K., Katayama, K., Kanaseki, T., Morimoto, K. (1960) Studies on the derivation of the centre median of Luys. Tokushima J. Exp. Med. 2: 261-268
• Pahapill, P.A. and Lozano, A. M. (2000) The pedunculopontine nucleus and Parkinson's disease. Brain, 123:1767-1783
• Parent, M. and Parent, M. (2005) Single-axon tracing and three dimensional reconstruction of centre median-parafascicular thalamic neurons in primates. J. Comp. Neurol. 481-127-144
• Parent, M. and Parent, M. (2006) Single-axon tracing study of corticostriatal projections arising from primary motor cortex in primates. J. Comp. Neuro.496: 202-213 PMID16538675
• Percheron et al 1987 numbers
• Percheron, G. (2003) Thalamus. In The human nervous system. Paxinos, G. and Mai, J. eds) Elsevier, Amsterdam
• Sato, F., Lavallée, P., Levesque, M. and Parent, A. (2000) Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. J. Comp. Neurol. 417: 17-31
• Selemon, L.D. and Goldman Rakic, P.S. (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci. 5: 776-794
• Terminologia anatomica (1998) Thieme, Stuttgart
• Vogt, C. and O. (1941)
• Yelnik, J., François, C., Percheron, G., Heyner, S. (1987) Golgi study of the primate substantia nigra. I. Quanttitative morphology and typology of nigral neurons. J. Comp. Neurol. 265: 455-472
• Yelnik, J., François, Percheron, G., Tandé, D. (1991) Morphological taxonomy of the neurons of the primate striatum. J. Comp. Neurol. 313:273 .
• Yelnik, J. and Percheron, G. (1979) Subthalamic neurons in primates: a quantitative and comparative analysis. Neuroscience 4:1717-1743

See also

• Nervous system