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Brain Structure and Function

, Volume 220, Issue 2, pp 955–977 | Cite as

Possible anatomical pathways for short-latency multisensory integration processes in primary sensory cortices

  • Julia U. Henschke
  • Tömme Noesselt
  • Henning Scheich
  • Eike BudingerEmail author
Original Article

Abstract

Multisensory integration does not only recruit higher-level association cortex, but also low-level and even primary sensory cortices. Here, we will describe and quantify two types of anatomical pathways, a thalamocortical and a corticocortical that possibly underlie short-latency multisensory integration processes in the primary auditory (A1), somatosensory (S1), and visual cortex (V1). Results were obtained from Mongolian gerbils, a common model-species in neuroscience, using simultaneous injections of different retrograde tracers into A1, S1, and V1. Several auditory, visual, and somatosensory thalamic nuclei project not only to the primary sensory area of their own (matched) but also to areas of other (non-matched) modalities. The crossmodal output ratios of these nuclei, belonging to both core and non-core sensory pathways, vary between 0.4 and 63.5 % of the labeled neurons. Approximately 0.3 % of the sensory thalamic input to A1, 5.0 % to S1, and 2.1 % to V1 arise from non-matched nuclei. V1 has most crossmodal corticocortical connections, projecting strongest to S1 and receiving a similar amount of moderate inputs from A1 and S1. S1 is mainly interconnected with V1. A1 has slightly more projections to V1 than S1, but gets just faint inputs from there. Concerning the layer-specific distribution of the retrogradely labeled somata in cortex, V1 provides the most pronounced feedforward-type outputs and receives (together with S1) most pronounced feedback-type inputs. In contrast, A1 has most pronounced feedback-type outputs and feedforward-type inputs in this network. Functionally, the different sets of thalamocortical and corticocortical connections could underlie distinctive types of integration mechanisms for different modality pairings.

Keywords

Crossmodal Multimodal interplay Phase reset Rodent Stimulus detection 

Abbreviations

A1

Primary auditory cortex

APTV

Anterior pretectal nucleus, ventral division

AuD

Secondary auditory cortex, dorsal

AuV

Secondary auditory cortex, ventral

AV

Anteroventral thalamic nucleus

BIC

Brachium of the inferior colliculus

bsc

Brachium of the superior colliculus

cp

Cerebral peduncle

CPu

Caudate putamen

d

Dorsal

DLG

Dorsal lateral geniculate nucleus

ec

External capsule

FDA

Fluorescein-labeled dextran amine

fi

Fimbria hippocampus

hbc

Habenular commissure

HF

Hippocampus

HL

Hindlimb area

ic

Internal capsule

InG

Intermediate gray layer of the superior colliculus

InWh

Intermediate white layer of the superior colliculus

l

Lateral

LD

Laterodorsal thalamic nucleus

LP

Lateral posterior thalamic nucleus

m

Medial

M1/2

Primary/secondary motor cortex

MGB

Medial geniculate body

MGD/M/V

MGB, dorsal/medial/ventral division

ml

Medial lemniscus

MV

Mean value

MZMG

Marginal zone of MGB

Op

Optic nerve layer of the superior colliculus

opt

Optic tract

pc

Posterior commissure

PLi

Posterior limitans thalamic nucleus

Po

Posterior thalamic nuclear group

r

Rostral

RSD

Retrosplenial dysgranular cortex

Rt

Reticular thalamic nucleus

S1/2

Primary/secondary somatosensory cortex

SG

Suprageniculate nucleus

SNR

Substania nigra, reticular part

SuG

Superficial gray layer of the superior colliculus

TMRDA

Tetramethylrhodamine-labeled dextran amine

v

Ventral

V1/2

Primary/secondary visual cortex

VA

Ventral anterior thalamic nucleus

VL

Ventrolateral thalamic nucleus

VLG

Ventral lateral geniculate nucleus

VM

Venteromedial thalalamic nucleus

VPL

Ventral posterolateral thalamic nucleus

VPM

Ventral posteromedial thalamic nucleus

ZI

Zona incerta

Notes

Acknowledgments

We thank Anja Gürke and Janet Stallmann for their excellent histological assistance and Alexander Waite for editorial help. This work was supported by the State Sachsen-Anhalt, Bundesministerium für Bildung und Forschung, and Deutsche Forschungsgesellschaft (grants of Sonderforschungsbereich Transregio 31 to T.N., H.S., E.B.), Germany.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

We declare that all animal studies have been approved by the appropriate ethics committee (see “Materials and methods”) and have, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Supplementary material

429_2013_694_MOESM1_ESM.tif (19.5 mb)
Supplementary Figure 1 (Fig. 1 magenta/green). (A-C) Frontal sections showing the cytoarchitecture (blue-fluorescent Nissl-stain) of the primary auditory (A1), somatosensory (S1), and visual cortex (V1). (D-F) Frontal sections showing a representative injection site of tetramethylrhodamine-dextranamine (TMRDA) (magenta) into A1 (D), of fluorescein-dextran amine (FDA) (green) into S1/HL (E), and of FDA into V1 (F). (G) Horizontal section illustrating the anterograde and retrograde labeling in the medial geniculate body (MGV, MGM), brachium of the inferior colliculus (BIC), reticular thalamic (Rt), ventrolateral thalamic (VL), and ventral posterorlateral thalamic nucleus (VPL) following an injection of TMRDA into A1 and of FDA into S1. Note the TMRDA and FDA labeling in the MGM (arrows). (H) Frontal section illustrating the anterograde and retrograde labeling in the dorsal, ventral, and medial divisions of the medial geniculate body (MGD, MGV, MGM), marginal zone of medial geniculate body (MZMG), and suprageniculate thalamic nucleus (SG) following an injection of TMRDA into A1 and of FDA into S1. Note the retrograde TMRDA and FDA labeling in the MZMG (arrows). (I) Frontal section illustrating the anterograde and retrograde labeling in the MGD, SG, posterior limitans thalamic nucleus (PLi), and BIC following an injection of TMRDA into A1 and of FDA into S1. Within the SG, a double-labeled neuron (yellow fluorescent, enlarged in inset) can be seen. (K) Horizontal section illustrating the anterograde and retrograde labeling in the dorsal division of lateral geniculate body (DLG), lateral posterior (LP), posterior thalamic nucleus (Po), and Rt following an injection of TMRDA into V1 and of FDA into S1. Note the retrograde TMRDA and FDA labeling in Po (arrow). Scale bars 1 mm (D-G, K) and 500 μm (A-C, H, I). For other abbreviations see list. (TIFF 19973 kb)
429_2013_694_MOESM2_ESM.tif (16.3 mb)
Supplementary Figure 2 (Fig. 3 magenta/green). Serial reconstructions of sections through the thalamus showing retrograde labeling after injections of TMRDA into A1 and FDA into V1 (A, D), TMRDA into A1 and FDA into S1 (B, E), and TMRDA into V1 and FDA into S1 (C, F). Note the TMRDA and FDA labeling in the suprageniculate (SG), laterodorsal (LD), posterior thalamic nucleus (Po), and medial division of the medial geniculate body (MGM). Horizontal (A-C) and frontal sections (D-F), respectively. Scale bars 1 mm. For other abbreviations see list. (TIFF 16710 kb)
429_2013_694_MOESM3_ESM.tif (13.8 mb)
Supplementary Figure 3 (Fig. 5 magenta/green). Frontal sections showing retrogradely labeled somata (insets A, B, D, F and arrows in C, E) in the primary somatosensory (A, B), visual (C, D), and auditory cortex (E, F) following injections of FDA (green) and TMRDA (magenta) into A1 (B, D), S1 (C, F), and V1 (A, E). Scale bars 1 mm (A, B, D, F and insets C, E), 500 μm (C, E), 100 μm (inset A, B, D, F). For abbreviations see list. (TIFF 14166 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Julia U. Henschke
    • 1
  • Tömme Noesselt
    • 2
    • 3
  • Henning Scheich
    • 1
    • 3
  • Eike Budinger
    • 1
    • 3
    • 4
    Email author
  1. 1.Department Auditory Learning and SpeechLeibniz Institute for NeurobiologyMagdeburgGermany
  2. 2.Department of Biological Psychology, Institute of Psychology IIOtto-von-Guericke University MagdeburgMagdeburgGermany
  3. 3.Center for Behavioral Brain SciencesMagdeburgGermany
  4. 4.Clinic of NeurologyOtto-von-Guericke-University MagdeburgMagdeburgGermany

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