Topography of claustrum and insula projections to medial prefrontal and anterior cingulate cortices of the common marmoset (Callithrix jacchus)

David H. Reser, Piotr Majka, Shakira Snell, Jonathan M.H. Chan, Kirsty Watkins, Katrina Worthy, Maria Del Mar Quiroga, Marcello G.P. Rosa

Research output: Contribution to journalArticleResearchpeer-review

19 Citations (Scopus)

Abstract

The claustrum has been the subject of intense research interest in recent years, driven in large part by its extensive connections with various regions of the cerebral cortex and by hypotheses surrounding its possible role in multimodal sensory and/or sensory–emotional integration. Here we employed neuroanatomical tracers to map projections from the claustrum–insular region to the medial prefrontal and anterior cingulate cortex of the common marmoset (Callithrx jacchus). These areas were selected based on their identification as “hub” areas of the default mode and cortical salience networks, respectively. Microinjections of fluorescent tracers, along with gold-nanoparticle-conjugated cholera toxin B-subunit and biotinylated dextran amine, were placed in subdivisions of the anterior cingulate area 24b/c and in medial prefrontal areas 32 and 32V. The resulting distribution of transported label showed rostral-caudal and dorsal-ventral topographic arrangement of claustrum connections and clear rostral-caudal topography of insular projections. Medial prefrontal connections were restricted mainly to a ventromedial strip located in the rostral half of the claustrum, with a second, smaller patch of cells in the caudal, ventrolateral portion. In contrast, injections into area 24 yielded dense, widespread connections from the dorsal claustrum, extending along its entire rostral-caudal length. Projections from the “classical” agranular, disgranular, and granular insular areas were sparse or nonexistent in areas 32 and 32V, with progressively increasing connections observed in more caudal tracer injections (i.e., in subdivisions of area 24). Transported label was observed in rostral peri-insular areas orbital periallocortex, orbital proisocortex, and insular proisocortex following all prefrontal injections. These data provide a structural connectivity foundation for interpretation of functional imaging studies, which often indicate activity in the “anterior insula” that may arise, in part, from claustrum and/or peri-insular projections to the anterior cingulate and medial prefrontal cortices.
Original languageEnglish
Pages (from-to)1421-1441
Number of pages21
JournalJournal of Comparative Neurology
Volume525
Issue number6
DOIs
Publication statusPublished - 15 Apr 2017

Keywords

  • cingulate cortex
  • medial prefrontal cortex
  • claustrum
  • resting state networks
  • marmoset
  • neuroanatomy
  • connections

Cite this

@article{045cd7e770ba486a9dad51246b339f37,
title = "Topography of claustrum and insula projections to medial prefrontal and anterior cingulate cortices of the common marmoset (Callithrix jacchus)",
abstract = "The claustrum has been the subject of intense research interest in recent years, driven in large part by its extensive connections with various regions of the cerebral cortex and by hypotheses surrounding its possible role in multimodal sensory and/or sensory–emotional integration. Here we employed neuroanatomical tracers to map projections from the claustrum–insular region to the medial prefrontal and anterior cingulate cortex of the common marmoset (Callithrx jacchus). These areas were selected based on their identification as “hub” areas of the default mode and cortical salience networks, respectively. Microinjections of fluorescent tracers, along with gold-nanoparticle-conjugated cholera toxin B-subunit and biotinylated dextran amine, were placed in subdivisions of the anterior cingulate area 24b/c and in medial prefrontal areas 32 and 32V. The resulting distribution of transported label showed rostral-caudal and dorsal-ventral topographic arrangement of claustrum connections and clear rostral-caudal topography of insular projections. Medial prefrontal connections were restricted mainly to a ventromedial strip located in the rostral half of the claustrum, with a second, smaller patch of cells in the caudal, ventrolateral portion. In contrast, injections into area 24 yielded dense, widespread connections from the dorsal claustrum, extending along its entire rostral-caudal length. Projections from the “classical” agranular, disgranular, and granular insular areas were sparse or nonexistent in areas 32 and 32V, with progressively increasing connections observed in more caudal tracer injections (i.e., in subdivisions of area 24). Transported label was observed in rostral peri-insular areas orbital periallocortex, orbital proisocortex, and insular proisocortex following all prefrontal injections. These data provide a structural connectivity foundation for interpretation of functional imaging studies, which often indicate activity in the “anterior insula” that may arise, in part, from claustrum and/or peri-insular projections to the anterior cingulate and medial prefrontal cortices.",
keywords = "cingulate cortex, medial prefrontal cortex, claustrum, resting state networks, marmoset, neuroanatomy, connections",
author = "Reser, {David H.} and Piotr Majka and Shakira Snell and Chan, {Jonathan M.H.} and Kirsty Watkins and Katrina Worthy and {Del Mar Quiroga}, Maria and Rosa, {Marcello G.P.}",
year = "2017",
month = "4",
day = "15",
doi = "10.1002/cne.24009",
language = "English",
volume = "525",
pages = "1421--1441",
journal = "Journal of Comparative Neurology",
issn = "0021-9967",
publisher = "Wiley-Blackwell",
number = "6",

}

Topography of claustrum and insula projections to medial prefrontal and anterior cingulate cortices of the common marmoset (Callithrix jacchus). / Reser, David H.; Majka, Piotr; Snell, Shakira; Chan, Jonathan M.H.; Watkins, Kirsty; Worthy, Katrina; Del Mar Quiroga, Maria; Rosa, Marcello G.P.

In: Journal of Comparative Neurology, Vol. 525, No. 6, 15.04.2017, p. 1421-1441.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Topography of claustrum and insula projections to medial prefrontal and anterior cingulate cortices of the common marmoset (Callithrix jacchus)

AU - Reser, David H.

AU - Majka, Piotr

AU - Snell, Shakira

AU - Chan, Jonathan M.H.

AU - Watkins, Kirsty

AU - Worthy, Katrina

AU - Del Mar Quiroga, Maria

AU - Rosa, Marcello G.P.

PY - 2017/4/15

Y1 - 2017/4/15

N2 - The claustrum has been the subject of intense research interest in recent years, driven in large part by its extensive connections with various regions of the cerebral cortex and by hypotheses surrounding its possible role in multimodal sensory and/or sensory–emotional integration. Here we employed neuroanatomical tracers to map projections from the claustrum–insular region to the medial prefrontal and anterior cingulate cortex of the common marmoset (Callithrx jacchus). These areas were selected based on their identification as “hub” areas of the default mode and cortical salience networks, respectively. Microinjections of fluorescent tracers, along with gold-nanoparticle-conjugated cholera toxin B-subunit and biotinylated dextran amine, were placed in subdivisions of the anterior cingulate area 24b/c and in medial prefrontal areas 32 and 32V. The resulting distribution of transported label showed rostral-caudal and dorsal-ventral topographic arrangement of claustrum connections and clear rostral-caudal topography of insular projections. Medial prefrontal connections were restricted mainly to a ventromedial strip located in the rostral half of the claustrum, with a second, smaller patch of cells in the caudal, ventrolateral portion. In contrast, injections into area 24 yielded dense, widespread connections from the dorsal claustrum, extending along its entire rostral-caudal length. Projections from the “classical” agranular, disgranular, and granular insular areas were sparse or nonexistent in areas 32 and 32V, with progressively increasing connections observed in more caudal tracer injections (i.e., in subdivisions of area 24). Transported label was observed in rostral peri-insular areas orbital periallocortex, orbital proisocortex, and insular proisocortex following all prefrontal injections. These data provide a structural connectivity foundation for interpretation of functional imaging studies, which often indicate activity in the “anterior insula” that may arise, in part, from claustrum and/or peri-insular projections to the anterior cingulate and medial prefrontal cortices.

AB - The claustrum has been the subject of intense research interest in recent years, driven in large part by its extensive connections with various regions of the cerebral cortex and by hypotheses surrounding its possible role in multimodal sensory and/or sensory–emotional integration. Here we employed neuroanatomical tracers to map projections from the claustrum–insular region to the medial prefrontal and anterior cingulate cortex of the common marmoset (Callithrx jacchus). These areas were selected based on their identification as “hub” areas of the default mode and cortical salience networks, respectively. Microinjections of fluorescent tracers, along with gold-nanoparticle-conjugated cholera toxin B-subunit and biotinylated dextran amine, were placed in subdivisions of the anterior cingulate area 24b/c and in medial prefrontal areas 32 and 32V. The resulting distribution of transported label showed rostral-caudal and dorsal-ventral topographic arrangement of claustrum connections and clear rostral-caudal topography of insular projections. Medial prefrontal connections were restricted mainly to a ventromedial strip located in the rostral half of the claustrum, with a second, smaller patch of cells in the caudal, ventrolateral portion. In contrast, injections into area 24 yielded dense, widespread connections from the dorsal claustrum, extending along its entire rostral-caudal length. Projections from the “classical” agranular, disgranular, and granular insular areas were sparse or nonexistent in areas 32 and 32V, with progressively increasing connections observed in more caudal tracer injections (i.e., in subdivisions of area 24). Transported label was observed in rostral peri-insular areas orbital periallocortex, orbital proisocortex, and insular proisocortex following all prefrontal injections. These data provide a structural connectivity foundation for interpretation of functional imaging studies, which often indicate activity in the “anterior insula” that may arise, in part, from claustrum and/or peri-insular projections to the anterior cingulate and medial prefrontal cortices.

KW - cingulate cortex

KW - medial prefrontal cortex

KW - claustrum

KW - resting state networks

KW - marmoset

KW - neuroanatomy

KW - connections

UR - http://www.ncbi.nlm.nih.gov/pubmed/27038224

U2 - 10.1002/cne.24009

DO - 10.1002/cne.24009

M3 - Article

VL - 525

SP - 1421

EP - 1441

JO - Journal of Comparative Neurology

JF - Journal of Comparative Neurology

SN - 0021-9967

IS - 6

ER -