Avian hippocampal boundaries: an overview Tom V. Smulders

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Avian hippocampal boundaries: an overview

Tom V. Smulders
Disclaimer : This is in not a comprehensive review of the literature, but I do think it covers the essence. If I am missing crucial data or opinions, feel free to raise these issues on the list-serv or at the symposium. The recommendation at the end is my personal opinion, and people are free to disagree. For the sake of brevity, I have not cited extensively, nor described people’s results extensively. If any of my statements seem to be blatantly false, please let me know, and I will correct them.
I would also like to note that even in the mammalian brain, the term “hippocampus” is used with some slop. I have know people to refer to the hippocampus as the combination of Cornu Ammonis, Dentate Gyrus, and sometimes even Subiculum, while for other people, only the CA is the hippocampus “proper”. A similar sloppiness exists in the definition of the avian hippocampus.
Brief History
Rose (1914) considers the dorsal part of the medial wall of the ventricle as “clearly hippocampal” because of the 4-layered appearance. Everybody since has considered this part of the avian brain equivalent to the mammalian hippocampus to some degree or other (Huber and Crosby, 1929; Craigie, 1930, 1932, 1935, 1940; Durward, 1932), and agreement about this exists in the reptilian neuroanatomical field as well (starting with J.B. Johnston in 1913).
Källén (1962) followed the development of the medial pallium in mammals and birds as both developed into their respective “hippocampuses” and used it as a strong case example for the use of embryological evidence in homology arguments.
In their atlas, Karten and Hodos (1967) indicated a Hippocampus (Hp; including a cell-dense “V”-shaped area with one “leg” along the ventricle, and the other along the medial surface of the brain) and an Area Parahippocampalis (APH; dorsal and lateral of the Hp), without indicating clear boundaries between them or at their edges. Many authors refer to the combination of Hp and APH as the Hippocampal Formation (HF) or Hippocampal Complex (HC) (see also final recommendation). Most of the outside boundaries of the HF are obvious:

  • Lateral and Ventral boundary: the lateral ventricle

  • Dorsal and Caudal boundary: the surface of the brain

  • Medial boundary: the midline

  • the ventral-most boundary with the septum: a clear change in cell density, as well as usually a notch in the ventricular wall.

The boundaries that are less clear in the pigeon atlas, are:

  • the lateral/dorsal boundary between the ventricle and the surface of the brain

  • the rostral boundary

  • the division between HP and APH

Lateral/dorsal boundary

There is a fairly clear lateral boundary all the way through the caudal to rostral levels, based on a change in cell density (lower density in the HF). This lateral boundary also agrees with boundaries defined in AChE (Hampton et al 1995), as well as in 5-HT (Krebs et al 1991) and in CCK, VIP, L-Enk, and Somatostatin (Erichsen et al 1991). The boundary is also clear in in-situ hybridizations for several different Glutamate receptor subtypes (Jarvis Lab, unpublished data).

Some authors have put the boundaries of APH further lateral than the ones suggested by the cytoarchitecture. Shimizu and Karten (1990) called the entire HF “hippocampus”, and placed a dorsal and ventral APH lateral to that (in their study of the Wulst, many molecules also indicated the lateral boundary clearly, only they interpreted this as the boundary between Hp and APH). More recently, in the embryonic chick brain, Redies et al (2001) use the term APH for the medial pallium all the way from the Hp to the piriform cortex (this includes everything labeled CDL in Karten and Hodos), and they then subdivide it into 4 different parts. They base themselves on Puelles et al (2000)’s subdivision of the major developmental domains, which puts Hp, APH and CDL all in the medial pallium.

Rostral Boundary

Rostrally, the HF curves downward from the dorsal surface, into the brain (below the rostral Wulst) and ends in a narrow point. This can easily be seen again in Nissl stain in sagital sections, as well as followed in consecutive coronal sections. This boundary is also well defined by the presence of dense SS staining in the HA rostral and lateral to the boundary (Erichsen et al 1991). And again it is visible in sagital sections in in-situ hybridizations for several glutamate receptors.

Hp vs APH: Internal subdivisions of the HF

There are no clear lines one can draw between the Hp and APH in Nissl stain. At most, it could be defined as the imaginary line connecting the tops of the two arms of the “V” with each other, but this would be a tentative boundary at best. There are clear differences between different subregions of the HF in terms of neurochemistry, connectivity and cell morphology. Different studies have suggested different subdivision schemes of the avian HF based on these different techniques. Usually, there are more than just 2 subdivisions, which would fit in the classical Hp vs APH scheme. However, I do not see any evidence that different subdivisions in the “APH” are necessarily more related to each other than to “Hp” subdivisions.

Subdivisions of HF: homologies with mammals

Historically, there have been many proposals put forth about which subdivision of the avian hippocampal formation could be homologous to which subdivision of the mammalian hippocampal formation. Because of a clear lack of a Timm-staining mossy fiber tract, some authors suggest that there is no dentate gyrus in the avian hippocampus. Others have suggested that the entire “V” shaped structure is the DG. A recent theory (mostly from Bingman and colleagues) suggests that the dorsomedial HF is possibly homologous to the DG, based on connectivity and neurochemistry. They would suggest that the “V” corresponds to the CA fields, while the dorsolateral HF is subiculum and/or entorhinal cortex. This hypothesis is being actively tested in the adult pigeon at this time in the Bingman lab.

It does not seem as if there is much of a difference of opinion about neuro-anatomical boundaries in the medial pallium of the avian brain. Rather, there sometimes is an inconsistency of terminology. There is an area which is easily delineated in Nissl and many other markers in the adult brain (including the ones from Shimizu and Karten, 1990 and from Redies et al, 2001), as outlined above. I would recommend following the most common practice in the literature at this point, and referring to it as the hippocampal formation. The area lateral to this would then be referred to as the CDL (I do not know enough about the relationship between CDL and HA to say anything more about it). Subdivisions of the HF can then be referred to in a topographical manner (dorsolateral, ventromedial, etc). Since the word “hippocampus” has a rather specific meaning in the mammalian brain (either limited to the Cornu Ammonis, or CA + Dentate Gyrus), I recommend against naming any subpart of the HF “hippocampus” per se, in order to avoid suggesting direct homology with those mammalian structures. In mammals “hippocampal complex” (or “..formation”) can refer to the hippocampus and surrounding cortices (subiculum, EC, …). This vagueness is exactly what we need in the avian nomenclature as well at this point in time.

In a recent paper, Atoji et al (2002) suggest the existence of a ventral hippocampus: a cell-dense layer, located below the lateral ventricle in the ventral part of the hemisphere, and connected with the “dorsal” hippocampus (the one mentioned in the body of this letter) through a “fiber wall” rostral of A 4.0 (Karten and Hodos coordinates), and connecting directly to the dorsal hippocampus at A 4.0. They do not present any real evidence for its inclusion in the hippocampus, nor do they cite any other authors who support this idea.


Atoji, W., Wild, J. M., Yamamoto, Y., & Suzuki, Y. (2002). Intratelencephalic connections of the hippocampus in pigeons (Columba livia). Journal of Comparative Neurology, 447(2), 177-199.

Craigie, E. H. (1930). Studies on the brain of the kiwi (Apteryx australis). J Comp Neurol, 49(2), 223-357.

Craigie, E. H. (1932). The cell structure of the cerebral hemisphere of the humming bird. J Comp Neurol, 56, 135-168.

Craigie, E. H. (1935). The hippocampal and parahippocampal cortex of the emu (Dromiceius). J Comp Neurol, 61, 563-591.

Craigie, E. H. (1940). The cerebral cortex of palaeognathine and neognathine birds. J Comp Neurol, 73(2), 179-234.

Durward, A. (1932). Observations on the cell masses in the cerebral hemisphere of the New Zealand kiwi (Apteryx australis). J Anat, 66, 437-477.

Erichsen, J. T., Bingman, V. P., & Krebs, J. R. (1991). The distribution of neuropeptides in the dorsomedial telencephalon of the pigeon (Columba livia) : a basis for regional subdivisions. J.Comp.Neurol., 314, 478-492.

Hampton, R. R., Sherry, D. F., Shettleworth, S. J., Khurgel, M., & Ivy, G. (1995). Hippocampal volume and food-storing behavior are related in parids. Brain Behav Evol, 45(1), 54-61.

Huber, G. C., & Crosby, E. C. (1929). The nuclei and fiber paths of the avian diencephalon, with consideration of telencephalic and certain mesencephalic centers and connections. J Comp Neurol, 48(1), 1-225.

Johnston, J. B. (1913). The morphology of the septum, hippocampus, and pallial commissures in reptiles and mammals. J Comp Neurol, 23(5), 371-474.

Källén, B. (1962). Embryogenesis of brain nuclei in the chick telencephalon. Ergeb Anat Entwicklungsgesch, 36, 62-82.

Karten, H., & Hodos, W. (1967). A stereotaxic atlas of the brain of the pigeon (Columba livia). Baltimore: Johns Hopkins University Press.

Krebs, J. R., Erichsen, J. T., & Bingman, V. P. (1991). The distribution of neurotransmitters and neurotransmitter-related enzymes in the dorsomedial telencephalon of the pigeon (Columba livia). J.Comp.Neurol., 314, 467-477.

Redies, C., Medina, L., & Puelles, L. (2001). Cadherin expression by embryonic divisions and derived gray matter structures in the telencephalon of the chicken. J Comp Neurol, 438(3), 253-85.

Rose, M. (1914). Über die cytoarchitektonische Gliederung des Vorderhirns der Vögel. J Psychol Neurol, 21, 278-352.

Shimizu, T., & Karten, H. J. (1990). Immunohistochemical analysis of the visual wulst of the pigeon (Columba livia). J Comp Neurol, 300(3), 346-69.

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