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

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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.

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Notes

  1. As reviewed by Driver and Noesselt (2008), multisensory interplay reveals crossmodal influences on sensory-specific brain areas, in particular of the cortex. The authors suggest, that there are at least three possible neuronal pathways mediating this multisensory interplay, which are not mutually exclusive: Account A (for "All multisensory): Direct feedforward influences between A1, V1, and S1, which might either arise subcortically at thalamic levels (account A.I) and/or via corticocortical connections directly between the primary sensory cortices (account A.II). Account B (for new Bimodal brain areas): Some multisensory regions may exist near classic unisensory regions. Account C (for "Critical role of feedback circuitry"): Feedback connections may exist from higher-level multisensory regions back to lower-level areas that are (predominantly) sensory-specific apart from these feedback influences. This feedback can also be mediated by thalamo-cortico-thalamic loops (see also Sherman and Guillery 2011). In the present study, we will largely provide evidence for the first possibility (account A).

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

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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.

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Authors and Affiliations

  1. Department Auditory Learning and Speech, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39118, Magdeburg, Germany

    Julia U. Henschke, Henning Scheich & Eike Budinger

  2. Department of Biological Psychology, Institute of Psychology II, Otto-von-Guericke University Magdeburg, Universitätsplatz 2, 39106, Magdeburg, Germany

    Tömme Noesselt

  3. Center for Behavioral Brain Sciences, Magdeburg, Germany

    Tömme Noesselt, Henning Scheich & Eike Budinger

  4. Clinic of Neurology, Otto-von-Guericke-University Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany

    Eike Budinger

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  1. Julia U. Henschke
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Correspondence to Eike Budinger.

Electronic supplementary material

Supplementary material

For those who are red-green color blind, Figures 1, 3 and 5 are provided in magenta-green (Suppl. Figures 1–3).

Below is the link to the electronic supplementary material.

429_2013_694_MOESM1_ESM.tif

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

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

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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Henschke, J.U., Noesselt, T., Scheich, H. et al. Possible anatomical pathways for short-latency multisensory integration processes in primary sensory cortices. Brain Struct Funct 220, 955–977 (2015). https://doi.org/10.1007/s00429-013-0694-4

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