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Thalamic afferents emphasize the different functions of macaque precuneate areas

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Abstract

We studied the thalamic afferents to cortical areas in the precuneus using injections of retrograde fluorescent neuronal tracers in four male macaques (Macaca fascicularis). Six injections were within the limits of cytoarchitectural area PGm, one in area 31 and one in area PEci. Precuneate areas shared strong input from the posterior thalamus (lateral posterior nucleus and pulvinar complex) and moderate input from the medial, lateral, and intralaminar thalamic regions. Area PGm received strong connections from the subdivisions of the pulvinar linked to association and visual function (the medial and lateral nuclei), whereas areas 31 and PEci received afferents from the oral division of the pulvinar. All three cytoarchitectural areas also received input from subdivisions of the lateral thalamus linked to motor function (ventral lateral and ventral anterior nuclei), with area PEci receiving additional input from a subdivision linked to somatosensory function (ventral posterior lateral nucleus). Finally, only PGm received substantial limbic association afferents, mainly via the lateral dorsal nucleus. These results indicate that area PGm integrates information from visual association, motor and limbic regions of the thalamus, in line with a hypothesized role in spatial cognition, including navigation. By comparison, dorsal precuneate areas (31 and PEci) are more involved in sensorimotor functions, being akin to adjacent areas of the dorsal parietal cortex.

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Abbreviations

AD:

Anterior Dorsal

AM:

Anterior Medial

AV:

Anterior Ventral

LD:

Lateral Dorsal

MD:

Medial Dorsal

MDdc:

Medial Dorsal, densocellular part

MDmc:

Medial Dorsal, magnocellular part

MDmc/pc:

Medial Dorsal, magnocellular/parvocellular part

MDmf:

Medial Dorsal, multiform part

MDpc:

Medial Dorsal, parvocellular part

VA:

Ventral Anterior

VAdc:

Ventral Anterior, densocellular part

VAmc:

Ventral Anterior, magnocellular part

VApc/dc:

Ventral Anterior, parvocellular/densocellular part

VL:

Ventral Lateral

VLc:

Ventral Lateral, caudal

VLm:

Ventral Lateral, medial

VLo:

Ventral Lateral, oral

VLps:

Ventral Lateral, postrema

VPI:

Ventral Posterior Inferior

VPL:

Ventral Posterior Lateral

VPLc:

Ventral Posterior Lateral, caudal

VPLo:

Ventral Posterior Lateral, oral

VPM:

Ventral Posterior Medial

VPMpc:

Ventral Posterior Medial, parvocellular

X:

Area X

CL:

Central Lateral

CM:

Centromedian

Csl:

Central superior lateral

Li:

Limitans

Pcn:

Paracentral

PF:

Parafascicular

SG:

Suprageniculate

Cdc:

Central densocellular

Cif:

Central inferior

Cim:

Central intermediate

Clc:

Central latocellular

Cs:

Central superior

Pa:

Paraventricular

Pt:

Paratenial

Re:

Reuniens

LP:

Lateral Posterior

Pul:

Pulvinar

Pul.i:

Pulvinar, inferior subdivision

Pul.l:

Pulvinar, lateral subdivision

Pul.m:

Pulvinar, medial subdivision

Pul.o:

Pulvinar, oral (anterior) subdivision

GLd:

Lateral geniculate body, dorsal division

GMmc:

Medial geniculate body, magnocellular division

GMpc:

Medial geniculate body, parvocellular division

Hlpc:

Lateral habenula, parvocellular division

Hm:

Medial habenula

R:

Reticular

Sm:

Stria medullaris

STN:

Subthalamic nucleus

THI:

Habenulo-interpendicular tract

SPL:

Superior parietal lobule

dr PGm:

Area PGm, dorsorostral sector

vc PGm:

Area PGm, ventrocaudal sector

V6:

Area V6

V6Ad:

Area V6A, dorsal portion

V6Av:

Area V6A, ventral portion

PEc:

Area PEc

PE:

Area PE

PEci:

Area PE, cingulate portion

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Acknowledgements

We thank K. E. Richardson, M. Verdosci, and F. Campisi for expert technical assistance and C. Cranfield for proofreading the manuscript.

Funding

Australian Research Council (CE140100007, DE120102883, DP140101968), National Health and Medical Research Council (1020839, 1082144), European Union Grant FP7-ICT 217077-EYESHOTS, FP7-PEOPLE-2011-IOF 300452 (S.B.), H2020-MSCA-734227-PLATYPUS and Ministero dell’Università e della Ricerca (2015AWSW2Y_001, 2017KZNZLN), and Fondazione del Monte di Bologna e Ravenna, Italy.

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Correspondence to Sophia Bakola.

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Gamberini, M., Passarelli, L., Impieri, D. et al. Thalamic afferents emphasize the different functions of macaque precuneate areas. Brain Struct Funct 225, 853–870 (2020). https://doi.org/10.1007/s00429-020-02045-2

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  • DOI: https://doi.org/10.1007/s00429-020-02045-2

Keywords

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