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The hippocampal continuation (indusium griseum): its connectivity in the hedgehog tenrec and its status within the hippocampal formation of higher vertebrates

Abstract

The indusium griseum and its precallosal extension are usually considered poorly differentiated portions of the hippocampus. The connections of this so-called ‘hippocampal continuation’ (HCt) have only been analyzed so far in rodents, which show one of the least-developed HCt among mammals. In this study we have investigated the relatively well differentiated HCt of the small Madagascan hedgehog tenrec (Afrotheria) using histochemical and axonal transport techniques. The tenrec’s HCt shows associative and commissural connections. It receives laminar specific afferents from the entorhinal cortex (collaterals from neurons projecting to the dentate area), the anterior and posterior piriform cortices as well as the supramammillary region. A few fibers also originate in the olfactory bulb and the dentate hilus. Among these input areas only the dentate hilus receives a significant reciprocal projection from the HCt. Additional HCt efferents are directed to the subcallosal septum (presumed septohippocampal nucleus), the olfactory tubercle and the islands of Calleja. With the exception of the supramammillary afferents and possible efferents to the supraoptic nucleus we failed, however, to demonstrate distinct thalamic and hypothalamic connections. A comparison of the connections of the HCt with those of the hippocampal subdivisions reveal some similarity between the HCt and the dentate area, but the overall pattern of connectivity does not permit a correlation of the HCt with the dentate area, let alone the cornu ammonis and the subiculum. This view is supported by histochemical findings in the tenrec (immunoreactivity to calcium binding proteins) as well as the rat (data taken from the literature). The HCt is therefore considered a region in its own right within the hippocampal formation. It may be tentatively correlated with the medial cortex of reptiles, while the dentate area and the cornu ammonis may have evolved de novo in mammals.

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Notes

  1. 1.

    The nomenclature used here restricts the term taenia tecta to the region reciprocally connected with the olfactory bulb (Radtke-Schuller and Künzle 2000). Showing a less compact layer 2 and a layer 3 with mainly medium-sized, round neurons; this region is also referred to as the ventral taenia tecta, while the HCtA is called the dorsal taenia tecta (Haberly and Price 1978).

  2. 2.

    Among the candidate regions (subicular complex, entorhinal cortex) often cited in this respect, the entorhinal cortex is considered here as part of the caudolateral hemisphere which might have evolved in parallel to the Dt and CA. This assumption is made on the basis of: (1) the similarity between the entorhinal cortex and the primary olfactory cortex with regard to their three-layered organization in tenrec (Künzle 2002); (2) the presence of reciprocal connections between the mammalian entorhinal cortex and both the primary olfactory cortex and the olfactory bulb (Amaral and Witter 1995; Haberly 2001). The latter regions are poorly connected with the areas laterally adjacent to the reptilian MDM (Ulinski 1990; Hoogland and VanderZee 1995).

Abbreviations

Acb:

Nucleus accumbens

AChE:

Acetylcholinesterase

Ay:

Amygdala

AyCo:

Cortical amygdala

BDA:

Biotinylated dextran amine

CA:

Cornu ammonis

Cab:

Calbindin

Car:

Calretinin

cc:

Corpus callosum

CCK:

Cholecystokinin

CjC:

Islands of Calleja

CjM:

Insula magna

DgC:

Nuclear complex of diagonal band

Dt:

Dentate area

DtGr/Hi/Mo:

Granule cell layer/hilus/molecular layer of Dt

EnkM:

Met-enkephalin

Et:

Echinops telfairi

ERh:

Entorhinal cortex

ERhD/V:

Dorsal/ventral portion of ERh

gmf:

Granule mossy fiber system

HbM:

Medial habenula

HCt:

Hippocampal continuation

HCtA/D/P:

Anterior/dorsal/posterior portion of HCt

HCtMo(1)/2/3:

First/second/third layer of HCt

Hy:

Hypothalamus

HyA/L:

Anterior/lateral Hy

MCx:

Cortex of medial hemisphere with infralimbic, prelimbic and/or cingulate areas

MDM:

Medial and dorsomedial cortex of reptiles

Mm:

Mammillary region

MmM:

Medial Mm

MmP:

Perimammillary region

NCx:

Neocortex

NPY:

Neuropeptide Y

OfA:

Anterior olfactory nuclear complex

OfB:

Olfactory bulb

Pav:

Parvalbumin

PCx:

Subrhinal paleocortex (numbers refer to zones involved)

PCxD/V:

Dorsal/ventral portion of PCx

ppc:

Proportional prosencephalic coordinates

PRh:

Perirhinal cortex

PSbE:

Presubiculum

rao:

Retrograde and subsequent anterograde transport of BDA in collateral fibers

RCx:

Rhinal cortex (additional numbers refer to zones)

Re:

Reuniens complex

RL:

Rostrolateral thalamus (including presumed equivalents of anterior thalamic nuclei)

RM:

Rostromedial thalamus (including presumed ncl. medialis dorsalis)

Sbi:

Subiculum

Se:

Septum

SeDc:

Subcallosal portion of dorsal Se

SeDm:

Dorsal Se without SeDc

SOp:

Supraoptic nucleus

StP:

Striopallidum

SuP:

Substance P

TrMH:

Transition zone between HCt2 and deep layers of MCx

TT:

Taenia tecta (also referred to as ventral TT)

Tu:

Olfactory tubercle

WGA-HRP:

Wheat germ agglutinin conjugated to horseradish peroxidase

XCx:

Poorly defined area caudally adjacent to RCx

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Acknowledgements

The excellent technical assistance of Angelika Antonius, Antonija Nekic and Sigi Schaller is gratefully acknowledged. The author has also appreciated the help of S. Kerling, A. Klaus and B. Reyermann. The work was supported by the Deutsche Forschungsgemeinschaft, grant Ku 624/3–1.

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Correspondence to H. Künzle.

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Künzle, H. The hippocampal continuation (indusium griseum): its connectivity in the hedgehog tenrec and its status within the hippocampal formation of higher vertebrates. Anat Embryol 208, 183–213 (2004). https://doi.org/10.1007/s00429-004-0384-3

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Keywords

  • Medial cortex
  • Taenia tecta
  • Septohippocampal nucleus
  • Islands of Calleja
  • Brain evolution