Elsevier

Neuroscience

Volume 146, Issue 3, 25 May 2007, Pages 1371-1387
Neuroscience

Systems neuroscience
Thalamocortical and the dual pattern of corticothalamic projections of the posterior parietal cortex in macaque monkeys

https://doi.org/10.1016/j.neuroscience.2007.02.033Get rights and content

Abstract

The corticothalamic projection includes a main, modulatory projection from cortical layer VI terminating with small endings whereas a less numerous, driving projection from layer V forms giant endings. Such dual pattern of corticothalamic projections is well established in rodents and cats for many cortical areas. In non-human primates (monkeys), it has been reported for the primary sensory cortices (A1, V1, S1), the motor and premotor cortical areas and, in the parietal lobe, also for area 7. The present study aimed first at refining the cytoarchitecture parcellation of area 5 into the sub-areas PE and PEa and, second, establishing whether area 5 also exhibits this dual pattern of corticothalamic projection and what is its precise topography. To this aim, the tracer biotinylated dextran amine (BDA) was injected in area PE in one monkey and in area PEa in a second monkey. Area PE sends a major projection terminating with small endings to the thalamic lateral posterior nucleus (LP), ventral posterior lateral nucleus (VPL), medial pulvinar (PuM) and, but fewer, to ventral lateral posterior nucleus, dorsal division (VLpd), central lateral nucleus (CL) and center median nucleus (CM), whereas giant endings formed restricted terminal fields in LP, VPL and PuM. For area PEa, the corticothalamic projection formed by small endings was found mainly in LP, VPL, anterior pulvinar (PuA), lateral pulvinar (PuL), PuM and, to a lesser extent, in ventral posterior inferior nucleus (VPI), CL, mediodorsal nucleus (MD) and CM. Giant endings originating from area PEa formed restricted terminal fields in LP, VPL, PuA, PuM, MD and PuL. Furthermore, the origin of the thalamocortical projections to areas PE and PEa was established, exhibiting clusters of neurons in the same thalamic nuclei as above, in other words predominantly in the caudal thalamus. Via the giant endings CT projection, areas PE and PEa may send feedforward, transthalamic projections to remote cortical areas in the parietal, temporal and frontal lobes contributing to polysensory and sensorimotor integration, relevant for visual guidance of reaching movements for instance.

Section snippets

Experimental procedures

The present study was conducted on two adult macaque monkeys (one Macaca mulatta and one Macaca fascicularis), 3 and 4 years old and weighing 3 and 4 kg. Surgical procedures and animal care were conducted in accordance with the Guide for Care and Use of Laboratory Animals (ISBN 0-309-05377-3; 1996) and were approved by local (Swiss) veterinary authorities. Experimental procedures were designed to minimize the animals’ pain and suffering.

Localization of injections sites

Area PE occupies the surface of rostral superior parietal lobule whereas area PEa is located in the upper bank of the IPS (Paxinos et al., 2000). The distinction between areas PE and PEa is based on cytoarchitectonic criteria as initially defined in Nissl material by Pandya and Seltzer (1982) and reported later in other studies (Seltzer and Pandya 1984, Seltzer and Pandya 1986, Matelli et al 1998). In line with these data (Pandya and Seltzer, 1982), Nissl-stained sections adjacent to the

Location of injection sites

Two distinct sub-areas of the posterior parietal cortex were injected in the superior parietal lobule. The region injected in the anterior bank of IPS corresponds to area PEa (named also area 5v) whereas the region injected in the anterior bank surface of IPS is area PE (named also area 5d), as referred to in previous studies (Pandya and Seltzer 1982, Seltzer and Pandya 1984, Seltzer and Pandya 1986, Matelli et al 1998).

Topography of TC projections

The distributions and relative proportions of labeled cells in different

Conclusion

In conclusion, the present study supports the notion that area 5 in the macaque monkey comprises two cytoarchitectonally distinct sub-areas, PE and PEa, as assessed in Nissl- and SMI-32 stained material. The areas PE and PEa have largely comparable patterns of TC and CT projections, mainly with the caudal thalamus, more specifically with the nuclei LP, PuM and VPL. The thalamic territories projecting to areas PE and PEa overlap to a significant extent, as much as those directed to the two

Acknowledgments

The authors wish to thank technical assistance of Véronique Moret, Georgette Fischer, Françoise Tinguely, Christine Roulin and Veronika Streit (histology), Josef Corpataux, Bernard Bapst, Laurent Bossy and Bernard Morandi (animal housekeeping), Laurent Monney (informatics).

Grant Sponsors: Swiss National Science Foundation, grants No. 31-61857.00, 310000-110005 (E.M.R.), Novartis Foundation; The Swiss National Science Foundation Centre of Competence in Research (NCCR) on “Neural plasticity and

References (96)

  • E.M. Rouiller et al.

    Morphology of corticothalamic terminals arising from the auditory cortex of the rat: A Phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study

    Hear Res

    (1991)
  • E.M. Rouiller et al.

    A comparative analysis of the morphology of corticothalamic projections in mammals

    Brain Res Bull

    (2000)
  • E.M. Rouiller et al.

    The dual pattern of corticothalamic projection of the premotor cortex in macaque monkeys

    Thalamus Related System

    (2003)
  • E.M. Rouiller et al.

    The dual pattern of corticothalamic projection of the primary auditory cortex in macaque monkey

    Neurosci Lett

    (2004)
  • H. Sakata et al.

    Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey

    Brain Res

    (1973)
  • K. Simonyan et al.

    Cortico-cortical projections of the motor cortical larynx area in the rhesus monkey

    Brain Res

    (2002)
  • O. Taktakishvili et al.

    Posterior parietal cortex projections to the ventral lateral and some association thalamic nuclei in Macaca mulatta

    Brain Res Bull

    (2002)
  • Y.M. Tsang et al.

    Motor neurons are rich in non-phosphorylated neurofilaments: cross-species comparison and alterations in ALS

    Brain Res

    (2000)
  • J.A. Winer et al.

    Origins of medial geniculate body projections to physiologically defined zones of rat primary auditory cortex

    Hear Res

    (1999)
  • C. Acuna et al.

    Lateral-posterior and pulvinar reaching cells-comparison with parietal area 5a: a study in behaving Macaca nemestrina monkeys

    Exp Brain Res

    (1990)
  • C. Baleydier et al.

    Segregated thalamocortical pathways to inferior parietal and inferotemporal cortex in macaque monkey

    Vis Neurosci

    (1992)
  • H. Burton et al.

    Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: projections in the vicinity of the central sulcus

    J Comp Neurol

    (1995)
  • H. Burton et al.

    The posterior thalamic region and its cortical projection in New World and Old World monkeys

    J Comp Neurol

    (1976)
  • J. Bourassa et al.

    Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: A single-fibre study using biocytin as an anterograde tracer

    Eur J Neurosci

    (1995)
  • R. Caminiti et al.

    Early coding of reaching: frontal and parietal association connections of parieto-occipital cortex

    Eur J Neurosci

    (1999)
  • M.J. Campbell et al.

    Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex

    J Comp Neurol

    (1989)
  • C. Cappe et al.

    Anatomical support for a role of the thalamo-cortical pathway in the multisensory integration in monkeys

    (2005)
  • D.F. Cooke et al.

    Complex movements evoked by microstimulation of the ventral intraparietal area

    Proc Natl Acad Sci U S A

    (2003)
  • C. Darian-Smith et al.

    Thalamic projections to sensorimotor cortex in the macaque monkey: use of multiple retrograde fluorescent tracers

    J Comp Neurol

    (1990)
  • C. Darian-Smith et al.

    Comparing thalamocortical and corticothalamic microstructure and spatial reciprocity in the macaque ventral posterolateral nucleus (VPLc) and medial pulvinar

    J Comp Neurol

    (1999)
  • J. DeFelipe et al.

    Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex

    J Neurophysiol

    (1986)
  • G. Ettlinger et al.

    Changes in tactile discrimination and in visual reaching after successive and simultaneous bilateral posterior parietal ablations in the monkey

    J Neurol Neurosurg Psychiatry

    (1962)
  • M. Fabre-Thorpe et al.

    Role of the extra-geniculate pathway in visual guidanceII. Effects of lesioning the pulvinar-lateral posterior thalamic complex in the cat

    Exp Brain Res

    (1986)
  • S. Feig et al.

    Corticocortical communication via the thalamus: Ultrastructural studies of corticothalamic projections from area 17 to the lateral posterior nucleus of the cat and inferior pulvinar nucleus of the owl monkey

    J Comp Neurol

    (1998)
  • E.P. Gardner et al.

    Neurophysiology of prehension: I. Posterior parietal cortex and object-oriented hand behaviors

    J Neurophysiol

    (2006)
  • F.A. Geneser-Jensen et al.

    Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig. IEntorhinal area, parasubiculum, and presubiculum

    Zellforsch Mikrosk Anat

    (1971)
  • S. Geuna

    Appreciating the difference between design-based and model-based sampling strategies in quantitative morphology of the nervous system

    J Comp Neurol

    (2000)
  • M. Giguere et al.

    Mediodorsal nucleus: Areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys

    J Comp Neurol

    (1988)
  • J. Graham et al.

    Subcortical projections of six visual cortical areas in the owl monkey, Aotus trivirgatus

    J Comp Neurol

    (1979)
  • R.W. Guillery

    Anatomical evidence concerning the role of the thalamus in corticocortical communication: A brief review

    J Anat

    (1995)
  • N. Hatanaka et al.

    Thalamocortical and intracortical connections of monkey cingulate motor areas

    J Comp Neurol

    (2003)
  • P.V. Hoogland et al.

    Organization of the projections from barrel cortex to thalamus in mice studied with Phaseolus vulgaris-leucoagglutinin and HRP

    Exp Brain Res

    (1987)
  • P.V. Hoogland et al.

    Ultrastructure of giant and small thalamic terminals of cortical origin: A study of the projections from the barrel cortex in mice using Phaseolus vulgaris leuco-agglutinin (PHA-L)

    Exp Brain Res

    (1991)
  • E.G. Jones et al.

    Differential thalamic relationships of sensory-motor and parietal cortical fields in monkeys

    J Comp Neurol

    (1979)
  • E.G. Jones et al.

    Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei

    Eur J Neurosci

    (1989)
  • E.G. Jones

    Correlation and revised nomenclature of ventral nuclei in the thalamus of human and monkey

    Stereotact Funct Neurosurg 54–

    (1990)
  • E.G. Jones

    The thalamus

    (1985)
  • J.H. Kaas et al.

    The somatotopic organization of the ventroposterior thalamus of the squirrel monkey, Saimiri sciuereus

    J Comp Neurol

    (1984)
  • Cited by (66)

    • The role of plasticity in the recovery of consciousness

      2022, Handbook of Clinical Neurology
      Citation Excerpt :

      In turn, each cortical area is reciprocally connected to thalamic neurons located in specific nuclei. The massive reciprocal feedback from the cortex to the thalamus (Cappe et al., 2007; Aggleton et al., 2014) suggests that the central processing of sensory information is far more intricate than the traditional notion of feed-forward processing. Moreover, corticothalamic projections contribute to the neuronal circuitry involved in adjusting the activity patterns of thalamic neurons during sleep and wakefulness (Destexhe et al., 2007).

    • Effective connectivity and spatial selectivity-dependent fMRI changes elicited by microstimulation of pulvinar and LIP

      2021, NeuroImage
      Citation Excerpt :

      Microstimulation in the dPul elicited BOLD activity that was largely consistent with the reciprocal connections with visuomotor and polymodal cortical regions known from anatomical tracer studies in monkeys (Kaas and Lyon, 2007; Shipp, 2003). Thus, the extensive activity along the superior temporal sulcus (e.g. MT, MST, FST, TPO, PGa, TE, TEO), including anterior STS (IPa, TAa) (Yeterian and Pandya, 1991, 1989), posterior parietal cortex (e.g. LOP, LIP, MIP, VIP, 7a) (Asanuma et al., 1985; Cappe et al., 2009, 2007), frontal cortex (e.g. 8A/B, 45, 46), insula (Romanski et al., 1997), cingulate and premotor cortices (Baleydier and Mauguiere, 1985) was expected. The effective connectivity of dPul is conceptually in line with a number of recording and lesion studies in monkeys and humans that highlight its critical contribution to higher-order visual, oculomotor and skeletomotor functions involving spatial attention (Arend et al., 2008a; Fiebelkorn et al., 2019; Karnath et al., 2002; Petersen et al., 1987; Rafal et al., 2004; Van der Stigchel et al., 2010), decision making and action selection (Dominguez-Vargas et al., 2017; Komura et al., 2013; M. Wilke et al., 2010; Wilke et al., 2013) and sensorimotor transformations for visually-guided reaching and grasping (Mundinano et al., 2018; Schneider et al., 2020; M. Wilke et al., 2010; Wilke et al., 2018, 2017).

    • A multisensory perspective onto primate pulvinar functions

      2021, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      PMm is also interconnected with somatosensory and proprioceptive posterior parietal areas PE and PEa, as well as with the dorsal premotor cortex (Acuña et al., 1990; Cappe et al., 2009a; Impieri et al., 2018; Morel et al., 2005; Romanski et al., 1997; Schmahmann and Pandya, 1990). Last but not least, PMm is characterized by strong connections with the parietal, temporal and prefrontal cortex (Asanuma et al., 1985; Bos and Benevento, 1975; Cappe et al., 2007; Cappe et al., 2009a; Clower et al., 2001; Hardy and Lynch, 1992). It has connections with TE, MST, LIP, VIP, and more generally with both the superior parietal and the inferior parietal cortices (Baizer et al., 1993; Baleydier and Morel, 1992; Webster et al., 1993).

    • Synchronisation of Neural Oscillations and Cross-modal Influences

      2020, Trends in Cognitive Sciences
      Citation Excerpt :

      The synchronisation of neural oscillations likely facilitates information transfer across sensory cortices by linking information in local and large-scale brain networks [2,15,63,90,91]. As noted earlier, at least three distinct types of anatomical pathways may support cross-modal influences: indirect input from higher order multimodal cortical areas (e.g., IPS, STS, and PFC); connections through multimodal subcortical regions (e.g., superior colliculus and the pulvinar nucleus of the thalamus) [10–12]; and possibly direct lateral connections between unimodal cortices [13]. Depending on the nature of the stimulation and/or the tasks, different pathways may come into play and, in some cases, interact.

    • 1.33 - Visual-Motor Integration in the Primate Brain

      2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
    View all citing articles on Scopus
    View full text