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Norepinephrinergic afferents and cytology of the macaque monkey midline, mediodorsal, and intralaminar thalamic nuclei

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Abstract

The midline and intralaminar thalamic nuclei (MITN), locus coeruleus (LC) and cingulate cortex contain nociceptive neurons. The MITN that project to cingulate cortex have a prominent innervation by norepinephrinergic axons primarily originating from the LC. The hypothesis explored in this study is that MITN neurons that project to cingulate cortex receive a disproportionately high LC input that may modulate nociceptive afferent flow into the forebrain. Ten cynomolgus monkeys were evaluated for dopamine-β hydroxylase (DBH) immunohistochemistry, and nuclei with moderate or high DBH activity were analyzed for intermediate neurofilament proteins, calbindin (CB), and calretinin (CR). Sections of all but DBH were thionin counterstained to assure precise localization in the mediodorsal and MITN, and cytoarchitecture was analyzed with neuron-specific nuclear binding protein. Moderate–high levels of DBH-immunoreactive (ir) axons were generally associated with high densities of CB-ir and CR-ir neurons and low levels of neurofilament proteins. The paraventricular, superior centrolateral, limitans and central nuclei had relatively high and evenly distributed DBH, the magnocellular mediodorsal and paracentral nuclei had moderate DBH-ir, and other nuclei had an even and low level of activity. Some nuclei also have heterogeneities in DBH-ir that raised questions of functional segregation. The anterior multiformis part of the mediodorsal nucleus but not middle and caudal levels had high DBH activity. The posterior parafascicular nucleus (Pf) was heterogeneous with the lateral part having little DBH activity, while its medial division had most DBH-ir axons and its multiformis part had only a small number. These findings suggest that the LC may regulate nociceptive processing in the thalamus. The well established role of cingulate cortex in premotor functions and the projections of Pf and other MITN to the limbic striatum suggests a specific role in mediating motor outflow for the LC-innervated nuclei of the MITN.

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Abbreviations

ACC:

Anterior cingulate cortex

AD:

Anterodorsal nucleus

AV:

Anteroventral nucleus

C:

Central nucleus of the thalamus

Cif:

Inferior part

Cl:

Lateral part

Cim:

Inferior medial part

Cs:

Superior part

Csl:

Superior lateral part

CB:

Calbindin

cgs:

Cingulate sulcus

CnMd (CM):

Centre medianum

CR:

Calretinin

DBH:

Dopamine-β hydroxylase

dPCC:

Dorsal posterior cingulate cortex

Hb:

Habenula

hit:

Habenulointerpeduncular tract

ir:

Immunoreactive

LD:

Laterodorsal nucleus

Li:

Limitans

MCC:

Midcingulate cortex

MD:

Mediodorsal nucleus and its divisions

MDdc:

Densocellular

MDmc:

Magnocellular

MDmf:

Multiformis

MDmfa:

Anterior multiformis part of MDmf

MDpc:

Parvocellularis

mtt:

Mammilothalamic tract

NeuN:

Neuron-specific nuclear binding protein

PCC:

Posterior cingulate cortex

Pcn:

Paracentral nucleus of the thalamus

Pf:

Parafascicular nucleus

Pfl:

Lateral part

Pfm:

Medial part

Pfmf:

Multiformis part

PGi:

Paragigantocellular nucleus of the reticular formation

Prt:

Pretectal nucleus

Pt:

Parataenial nucleus

Pulm:

Medial pulvinar nucleus

Pv:

Paraventricular nucleus

Re:

Reuniens

sc:

Superior colliculus

sm:

Stria medullaris

SMI32:

Antibody for nonphosphorylated intermediate neurofilaments

sPf:

Subparafascicular nucleus

VM:

Ventral medial (VLm of Olszewski)

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Acknowledgments

These studies were supported by the NIH-NINDS grant RO1-NS44222 (BAV) and the James S. McDonnel Foundation (220020078; PRH).

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Authors and Affiliations

  1. Cingulum NeuroSciences Institute and SUNY Upstate Medical University, 4435 Stephanie Drive, Manlius, NY, USA

    Brent A. Vogt & Leslie J. Vogt

  2. Department of Neuroscience, Mount Sinai School of Medicine, New York, NY, USA

    Patrick R. Hof

  3. Department of Physiology and Pharmacology, Wake Forest University School of Medicine, Winston-Salem, NC, USA

    David P. Friedman

  4. Department of Physical Therapy, Northeastern University, Boston, MA, USA

    Robert W. Sikes

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  1. Brent A. Vogt
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  2. Patrick R. Hof
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  5. Leslie J. Vogt
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Correspondence to Brent A. Vogt.

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Vogt, B.A., Hof, P.R., Friedman, D.P. et al. Norepinephrinergic afferents and cytology of the macaque monkey midline, mediodorsal, and intralaminar thalamic nuclei. Brain Struct Funct 212, 465–479 (2008). https://doi.org/10.1007/s00429-008-0178-0

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