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Ammon's Horn Sclerosis : Its Pathogenesis and Clinical Significance Tohoku J. Exp. Med., 1990, 161, Suppl., 273-295 Ammon's Horn Sclerosis : Its Pathogenesis and Clinical Significance KEIJI SANOand TAKAAKIKIRINO Department of Neurosurgery, Teikyo University, Tokyo 173 SANO, K. and KIRINO, T. Ammon's Horn Sclerosis : Its Pathogenesis and Clinical Significance. Tohoku J. Exp. Med., 1990, 161, Suppl., 273-295•\ Sclerosis of the cornu Ammonis or Ammon's horn sclerosis (AHS) is an "often- described, yet hitherto enigmatic phenomen" as Spielmyer put it in 1927. It has been found in cases with ischemia, anoxia or hypoglycemia and in more than half of the epileptic brains examined at autopsy. Various theories about its path- ogenesis have been propunded. Among them, the "Pathoklise" theory of the Vogts and the vascular theory of Spielmeyer and his associates were prevailing until recently. In 1953, two articles were published to contribute to the path- ogenesis of ictal automatism (a type of complex partial or temporal lobe seizures). One is the incisural sclerosis theory by Penfield and his associates and the other is the Ammon's horn sclerosis theory by Sano and Malamud. The former authors described a diffuse sclerosis of the infero-mesial temporal structures without, however, specifically relating it to AHS. They considered it was the result of localized anoxia of that portion of the brain caused by incisural herniation occurring during parturition. Sano and Malamud maintained that AHS is a result of convulsions, a distinct scar adjacent to which epileptogenic foci may develop in the course of time to cause ictal antomatism. The latter theory was corroborated by Sano, Falconer and others. Falconer expanded the theory to the assertion that not only ictal automatism but other types of intractable epilepsy may be due to "mesial temporal (Ammon's horn) sclerosis" . The most recent development in the pathogenesis of AHS is the excitotoxicity theory. Namely, AHS is caused by excessive excitation of neurons, probably by putative excitatory neurotransmitters, especially, glutamate. For this theory, there is a significant body of evidence. The problem of AHS, an old research subject and a matter of long-lasting contro- versy, has now been updated and become one of the newest topics in the field of experimental neurobiology.•\Ammon's horn sclerosis; historical view; temporal lobe epilepsy; ischemic neuronal damage Historical account of the term "Hippocumpus" or "Cornu Ammonis" In a book titled "De Humano Foetu" published in 1587, Julius Caesar Arantius (Italian Aranzi) (1530-1589), a pupil of Andreas Vesalius, described a structure in the inferior horn of the lateral ventricle which recalled the image of a "Hippocampus", that is, "Marinus Equulus" (a little horse of the sea) or rather of a "Bombycinus Vermis Candidus" (a white silk worm) (Lewis 1922-1923; Tilney 1938). The term bombycinus vermis, which was more becoming of the two, has never gained popularity and has been forgotten in the literature. The 273 274 K. Sano and T. Kirino other term hippocampus has left the readers in doubt whether the anatomical structure was being compared with fish or mythodological horse. The mythodological hippocampus, the horse of Poseidon (Neptunus) or Triton, has the shape of a horse in its fore part and that of a fish in its hind portion. Its forelegs are shown sometimes with horse's hoofs, sometimes with flippers. It was about 100 years later that Diemerbroek (1672, cited from Lewis 1922-1923) named this structure Pes hippocampi because of the similarity of this and the flippers of the imaginary hipocampus. This nomenclature was again adopted in INA (1936) and in PNA (1955). If, however, one is frank enough, he may say the hippocumpus of the brain is more like a paw of a hippopotamus. Thus, Johan C.A. Mayer (1779, cited from Lewis 1922-1923) proposed the term •gPes hippopotami major•h for this structure. By the way, Pes hippopotami minor corresponded to Calcar avis which was described by Morand (1744, cited from Lewis 1922-1923). The designation of Mayer may be regarded as a modification of that of Haller (1762, cited from Lewis 1922-1923) who proposed Pes hippicampi major for the hippocampus and pes hippocampi minor for the calcar avis. BNA (1895) adopted Hippocampus and at the same time Digitationses hippocampi, therefore evidently thinking of the mythodological horse under the name of Hippocampus. This view has been fixed among anatomists since then. PNA adopted Pes hippocampi, and at the same time, Hippocampus which includes Pes hippocampi, Alveus hippocampi, and Fimbria hippocampi. Among neurophysiologists, however, Hippocampus as the sea-horse fish has been prevailing, probably since MacLean (1949). The sea-horse fish, the mythodological horse or the hippopotamus, all these are related with water and are pertinent to that structure which lies in the cerebrospinal fluid. If one takes the structure out of the ventricle, one may notice that it may look like a horn of some animal. Winslow (1732, cited from Lewis 1922-1923) regarded it a ram's horn and named it Corn arietis (ram's horn). It was de Garengoet (1742, cited from Lewis 1922-1923) who prefered a more mystical name and called it Cornu Ammonis (Ammon's horn). Ammon (Amon, Amun, Amen, Amoun), the Hidden , was the first god of Thebes in Ancient Egypt. When the rulers of Thebes found the 12th Dynasty, Ammon became the chief diety of Egypt. In the early picture, Ammon was expressed as having the head of a ram with ram's horn. As Amon-Re (Ra, Phra), he was represented in the form of a man wearing on his head a disk surmounted by two tall ostrich plumes. Therefore Cornu Ammonis is identical with cornus arietis. This Cornu Ammonis or Ammon's horn or its German equivalent Ammonshorn has found its favorite place in the German bibliography. The term hippocampal formation which includes hippocampus, fascia dentata (gyrus dentatus) and subiculum may probably originate from Formatio Ammonis of Rose (1927). Ammon's Horn Sclerosis 275 Historical account of Ammon 's horn sclerosis (Sclerosis of the Cornu Ammonis) The first gross description of this lesion is generally credited to Bouchet and Cazauvielh 1825, cited from Spielmeyer 1927) who observed changes of sclerosis or sofening in the hippocampus of epileptic as well as of nonepileptic psychopathic patients. The first microscopic examination was done in 1880 by Sommer who found the change to be restricted to the band of pyramidal cells of the hippocampus which has since been called •gSommer's sector•h. In 1889, Chaslin described a marginal gliosis in cases of epilepsy and regarded Ammon's horn sclerosis as representing merely a site of predilection for such gliosis. In 1899, Bratz (1889a, b) confirmed Sommer's findings but noted that the end-plate was as often affected as Sommer's sector and that a portion of the dorsal cell band was resistant in many cases. He found that Ammon's horn sclerosis existed in 25 out of 50 cases of idiopathic epilepsy, and he also noted the same lesion in other diseases associated with convulsive disorders. He regarded Ammon's horn sclero- sis as a congenital lesion. Stauder (1935) found Ammon's horn sclerosis in 36 of 53 patients with long-standing epileptic seizures and he could notice, in most of these 36, clinical pictures related to temporal lobe lesions. In 1953, Sano and Malamud discovered Ammon's horn sclerosis in 29 (58%) of the brain of 50 institutionalized epileptic patients. This Ammon's horn sclerosis was found unilaterally in cases of "idiopathic epilepsy" and bilaterally in cases with malformed brains as was previously noted by Bratz (1920). Sano Fig. 1. Nomenclature of various divisions of the hippocampal formation accord- ing to Rose, Lorente de No or the Spielmeyer's school. Subiculum includes subiculum and prosubiculum of Lorente de NO. 276 K. Sano and T. Kirino and Malamud (1953) plotted sclerotic changes of the hipocampus according to Rose's cell divisions (1927) and found the severest changes in H1 and H5 (CA1 and CA4 of Lorente de NO (1933, 1934) which correspond to the so-called Sommer's sector and the end-plate (Bratz's sector) respectively. Figure 1 shows diagram- matically the correlation between the cell divisions of Rose (1927) and Lorente de NO (1933, 1934) and traditional terms used by Spielmeyer's school (Bodechtel 1930). In contrast to Stauder (1935) who correlated Ammon's horn sclerosis with neurological deficits of the temporal lobe, Sano and Malamud (1953) propounded a theory that psychomotor epilepsy or ictal automatism may be due to firing of foci adjacent to the sclerosed area (e.g. Sommer's sector), especially in cases that developed automatism in the course of repeated convulsive seizures. This will be discussed below. As for the pathogenesis of Ammon's horn sclerosis, there have been keen active discussions between two German schools. The Vogts (Vogt and Vogt 1922; Vogt 1925) regarded it as strong evidence for their theory of Pathoklise, arguing that the sharp differences in cell morphology in Sommer's sector, the end-plate, the portion between them, and the subiculum represented differences in physico- chemical structure. Accoding to Spielmeyer and his associates (Spielmeyer 1925, 1927, 1929, 1930a, b, 1933; Uchimura 1928a, b), the change was explained on a vascular basis. They demonstrated ischemic changes in Sommer's sector and in the end-plate in acute cases of epilepsy and assumed that in chronic cases the degenerated ganglion cells were ultimately replaced by glia, to produce the final picture of sclerosis. Moreover, they observed similar changes in primary vascular or circulatory disorders. In the absence of vascular disease in "idiopathic" epilepsy, they advanced the theory of angiospasm. It is well known that the anteroinferior portion of the hippocampal formation is supplied by the anterior choroidal artery, while its major part is supplied by the posterior cerebral artery.
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