Elsevier

Brain Research Reviews

Volume 22, Issue 2, August 1996, Pages 93-181
Brain Research Reviews

Review article
The primate motor thalamus

https://doi.org/10.1016/0165-0173(96)00003-3Get rights and content

Abstract

The functional parcellation of the motor thalamus of primates has suffered from serious historical and technical drawbacks, which have led to extreme confusion. This is a problem when thalamic stereotaxy is again being use clinically. The cause usually imputed is the historical conflict between two main schools, the Vogt and the ‘Anglo-American’ (Michigan), which used different nomenclatures. In fact, the reasons are more profound and serious. A combination of them led to: an archaic, rigid conception of the ‘thalamic nucleus’; overexploitation of cytoarchitectonic technique, comparative anatomy and cortical connections; underexploitation of subcortical afferent territories; recent misuse of these territories; hesitations in the use of the VA-VL system; and opposition between ventral (‘relay’) and dorsal (‘associative’) ‘nuclei’. Previous and current parcellations and nomenclatures for the lateral region finally appeared inappropriate. Before presenting a new parcellation and nomenclature for the lateral region, we explain why we did not adopt one of most common or of recently proposed nomenclatures, and were led to make our own. This is established according to rational and historically grounded rules. Precise definition of thalamic elements is provided. A thalamic ‘region’ is a gross topographic division corresponding to the former nuclei. A ‘territory’ is defined as the cerebral space filled by afferent endings from one source. When having a distinct topography in a region, a given territory makes a ‘subregion’. For each of the studied ‘motor’ territories a review was made of its known cortical projections. The thalamic space where neurons project to a given cortical target constitutes a ‘source space’. Topographical comparison of the sources spaces with territories reveals that there is often no coincidence between different (afferent or efferent) neuronal set spaces. It appears that source spaces are coincident in the pallidal and nigral territories but not in the cerebellar territory where two topographically distinct source spaces could be distinguished. A ‘thalamic nucleus’ is defined as the intersection of a thalamocortical source space with one territory. A rapid review of the general anatomy of the diencephalon is made. The (‘dorsal’) thalamus is divided into ‘allo-’ and ‘isothalamus’, the latter with ‘bushy’ and ‘microneurons’. The lateral region is isothalamic. The ‘motor thalamus’ makes the anterior part of the lateral region. The present work aims to analyse the functional anatomy of the ‘motor thalamus’ by using precise topography and three-dimensional analyses of the subcortical territories receiving from the cerebellar nuclei (part II), the medial nucleus of the pallidum (part III) and the pars reticulata and mixta of the substantia nigra (part IV). Large injections were used to obtain the maximal extent of each territory. A major deficiency of previous studies was inadequate cartography. Reliance on ventricular (CA-CP) landmarks observed by use of orthogonal teleradiography is mandatory. A study was made of intra- and interspecific variations and their effect on stereotactic and cartographic precision in macaques. All three subcortical motor afferent territories to the motor thalamus of macaques are examined in precise cartography with three dimensional reconstructions, rotations and ‘reslicing’. The motor thalamus is made up of three topographically distinct and separate territories: cerebellar, pallidal territory and nigral. They cover the entire anterior part of the lateral region. There is no polar subdivision without lower afferents in front of the pallidal and nigral territories and thus no reason for isolating a nucleus lateralis polaris or a polar VA. The cerebellar territory is continuous and dense, in front of the somesthetic nucleus and everywhere separate from it. It has a complex three-dimensional shape, strongly convex anteriorly. Its caudal portion is dorsal to the spmesthetic nucleus. In the lateral dimension it extends from the lateral region to the paralaminar region of the medial complex. The cerebellar territory, primarily dentate, also contains islands of axons from the interposed and fastigial nuclei, the vestibular nuclei and the spinothalamic tract. It corresponds to at least five previously isolated ‘cytoarchitectonic nuclei’. It cannot be seen as a single entity but contains distinct ventrolateral and a mediodorsal source spaces. Its complex three-dimensional shape, its particular intersection with different cytoarchitectonic nuclei and source spaces, can be simplified into two nuclei: nucleus lateralis intermedius lateralis (LIL) and nucleus intermedius mediodorsalis (LIM). The stereotacticians' ventralis intermedius (Vim) is discussed at length. Tremorosynchronous and kinesthetic neurons are essentially located ventrally and laterally. The intrathalamic topography observed in human patients indicates that the stereotacticians's target (where tremorosynchronous neurons are found) is within lateral cerebellar territory receiving cerebellar afferents and projecting to the motor cortex. The hypothesis that the nucleus interpositus could be particularly involved is presented. The nucleus lateralis intermedius lateralis (LIL) of the present study is equivalent in macaques to the stereotacticians' ‘V.im.e’, subject to interspecific differences. The pallidal territory is anterior to and separate from the cerebellar territory, in the oral part of the lateral region. It covers the whole ventrodorsal extent of the thalamus. It is crescent shaped, strongly curved in the anteroposterior dimension, and ends dorsally over the cerebellar territory. It is also curved in the mediolateral dimension following the lateral border of the thalamus. The territorial border does not coincide with cytoarchitectonic borders. The pallidal territory includes various cytoarchitectonic nuclei. Only the cloud-like ventral oral part is easily recognizable on purely cytoarchitectonic criteria. The others are cytoarchitectonically ill defined. The pallidal territory may be delineated using calbindin immunostaining. Other targets of the medial pallidum are the central (centre-médian-parafascicular) complex, the pedunculo-pontine complex and the lateral habenula. In relation to its afferent and efferent connections, the pallidal thalamus seems to be made up of a single piece and could be considered as the lateral oral subregion or nucleus (LO). The nigrothalamic connection has been ignored for a long time and remains undervalued. Precise topographic description shows that the nigral territory is much more extensive than usually thought. It is located medial to the pallidal territory, and as the most rostral of all three subcortical afferent territories, is named nucleus lateralis rostralis (LR). Orally the nigral territory covers the whole ventrodorsal extent of the lateral region of the thalamus. A posterior part ends ventrally and medially just in front of the central complex. A topographically distinct amygdalar coterritory forms a subdivision named nucleus Lateralis Rostralis pars medialis (LRM). A posterodorsal part ends in the anterior paralaminar part of the medial complex, in front of the cerebellar territory. Islands of nigral terminations are observed within the medial nucleus. Three dimensional studies and artificial reslicing shows a posteroanterior sequence of the lemniscal, cerebellar, pallidal and nigral territories. The three motor territories extend over the whole ventrodorsal extent of the dorsal region. There appears to be no opposition of ventral to dorsal nuclei. Nuclei of the lateral region are thus given the first adjective Lateralis. The second adjective is from the initial sequence devised by C. Vogt, caudalis-intermedius-oralis, to which we add rostralis. The lemniscal territory is named subregio Lateralis Caudalis with two pars: nucleus Lateralis Caudalis Lateralis (LCL) and nucleus Lateralis Caudalis Medialis (LCM) cerebellar territory is named subregio Lateralis Intermedia with two nuclei: nucleus Lateralis intermedius Lateralis (LIL), which is the main source to the motor cortex, and nucleus Lateralis Intremedius Medialis (LIM). The pallidal territory is subregio or nucleus Lateralis Oralis (LO). The nigral territory is subregio or nucleus Lateralis Rostralis (LR) with a particular pars made by the amygdalar coterritory (LRM). An atlas of the macaque motor thalamus, comprising twelve levels, is presented, with mean dimensions for Macaca mulatta. Boundaries are not primarily cytoarchitectonic but topographic territories and sources spaces. This produces a modified parcellation of the macaque thalamus. Each level is described and compared to Olszewski's equivalent level. The new atlas can be used confidently for stereotactic purpose in macaques of various species.

References (388)

  • J.M. Deniau et al.

    Patterns of termination of cerebellar and basal ganglia efferents in the rat thalamus. Strictly segregated and partly overlapping projections

    Neurosci. Lett.

    (1992)
  • R.W. Dykes

    Parallel processing of somatosensory information: a theory

    Brain Res. Rev.

    (1983)
  • R.W. Dykes et al.

    Regional segregation of neurons responding to quickly adaprating, deep and pacinian receptors within the thalamic ventroposte rior lateral and ventroposterior inferior nuclei in the squirrel monkey (Simiri sciureus)

    Neuroscience

    (1981)
  • R.J. Elble et al.

    Activity of muscle spindles, motor cortex and cerebellar nuclei during action tremor

    Brain Res.

    (1984)
  • G. Fénelon et al.

    Topographic distribution of pallidal neurons projecting to the thalamus in macaques

    Brain Res.

    (1990)
  • G. Fénelon et al.

    Topographic distribution of the neurons of the central complex (‘centre median-parafascicular complex’) and of other thalamic neurons projecting to the striatum in macaques

    Neuroscience

    (1991)
  • R. Fink et al.

    Two methods for selective impregnation of degenerating axons and their synaptic endings in the central nervous system

    Brain Res.

    (1967)
  • F. Afshar et al.

    Stereotaxic Atlas of the Human Brain-stem and Cerebellar Nuclei. A Variability Study

    (1978)
  • J.P. Aggleton et al.

    Projections of the amygdala to the thalamus in the cynomolgus monkey

    J. Comp. Neurol.

    (1984)
  • K. Akert

    Comparative anatomy of frontal cortex and thalamofrontal connections

  • D. Albe-Fessard et al.

    Thalamic unit activity in man

    E.E.G. Clin. Neurophysiol., Suppl.

    (1967)
  • D. Albe-Fessard et al.

    Activation of thalamocortical projections related to tremorogenic processes

  • D. Albe-Fessard et al.

    Origine des messages somato-sensitifs activant les cellules du cortex moteur chez le singe

    Exp. Brain Res.

    (1966)
  • G.I. Allen et al.

    Integration of cerebral and peripheral inputs by interpositus neurons in monkey

    Exp. Brain Res.

    (1977)
  • G.I. Allen et al.

    Convergence of cerebral inputs onto dentate neurons in monkey

    Exp. Brain Res.

    (1978)
  • M.E. Anderson et al.

    Activity of neurons in cerebellar-receiving and pallidal-receiving areas of the thalamus of the behaving monkey

    J. Neurophysiol.

    (1991)
  • J. Andrew et al.

    A Stereotaxic Atlas of the Human Thalamus and Adjacent Structures

    (1969)
  • J.B. Angevine et al.

    Limbic nuclei of thalamus and connections of limbic cortex

    Arch. Neurol.

    (1962)
  • R. Anner-Baratti et al.

    Neural correlates of isometric force in the ‘motor’ thalamus

    Exp. Brain Res.

    (1986)
  • A.V. Apkarian et al.

    Primate spinothalamic pathways: I. A quantitative study of the cells of origin of the spinothalamic pathway

    J. Comp. Neurol.

    (1989)
  • A.V. Apkarian et al.

    Primate spinothalamic pathways: II. The cells of origin of the dorsolateral and ventral spinothalamic pathways

    J. Comp. Neurol.

    (1989)
  • A.V. Apkarian et al.

    Primate spinothalamic pathways: III. Thalamic terminations of the dorsolateral and ventral spinothalamic pathways

    J. Comp. Neurol.

    (1989)
  • A.V. Apkarian et al.

    Squirrel monkey lateral thalamus. I. Somatic nociresponsive neurons and their relation to spinothalamic terminals

    J. Neurosci.

    (1994)
  • A.E. Applebaum et al.

    Nuclei in which functionally identified spinothalamic tract neurons terminate

    J. Comp. Neurol.

    (1979)
  • L.R. Aronson et al.

    The thalamic nuclei of Pithecus (Macacus) rhesus. II. Dorsal thalamus

    Arch. Neurol. Psychiatr.

    (1934)
  • Arrechi-Bouchhioua, P., Yelnik, J., François, C. and Percheron, G., Three-dimensional tracing of individual...
  • H. Asanuma et al.

    Peripheral input pathways to the monkey motor cortex

    Exp. Brain Res.

    (1980)
  • D. Atlas et al.

    Topography of the brain stem of the rhesus monkey with special reference to the diencephalon

    J. Comp. Neurol.

    (1937)
  • C. Baleydier et al.

    The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis

    Brain

    (1980)
  • H. Barbas et al.

    Diverse thalamic projections to the prefrontal cortex in the rhesus monkey

    J. Comp. Neurol.

    (1991)
  • H. Barbas et al.

    Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey

    J. Comp. Neurol.

    (1987)
  • R.R. Batton et al.

    Fastigial efferent projections in the monkey: an autoradiographic study

    J. Comp. Neurol.

    (1977)
  • J.G. Bjaalie

    Three-dimensional computer reconstructions in neuroanatomy: basic principles and methods for quantitative analysis

  • R.M. Becksteadt

    Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes

    Neuroscience

    (1983)
  • R.M. Becksteadt et al.

    The distribution and some morphological features of substantia nigra neurons that project to the thalamus, superior colliculus and pedunculopontine nucleus in the monkey

    Neuroscience

    (1982)
  • L.A. Benevento

    Stereotaxic coordinates for the rhesus monkey thalamus and mesencephalon referencing visual afferents and cytoarchitecture

    J. Himforsch.

    (1975)
  • L.A. Benevento et al.

    The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta)

    J. Comp. Neurol.

    (1975)
  • D.B. Bender

    Retinotopic organization of macaque pulvinar

    J. Neurophysiol.

    (1981)
  • D.L. Benson et al.

    Differential gene expression for glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase in basal gan glia, thalamus, and hypothalamus of the monkey

    J. Neurosci.

    (1991)
  • H. Bergman et al.

    The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of Parkinsonism

    J. Neurophysiol.

    (1994)
  • Cited by (0)

    View full text