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Axon Terminals of Gabaergic Chandelier Cells Are Lost at Epileptic Foci

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Axon Terminals of Gabaergic Chandelier Cells Are Lost at Epileptic Foci Brae Re.search. 32(~ ( 1985 ) 251 260 25 1 Elsevier BRE lll-ltJt) Axon Terminals of GABAergic Chandelier Cells Are Lost At Epileptic Foci CHARLES E. RIBAK l)epartment ~{['Anatomy. University o,t CaliJornia. lrvine, ( A 92717 ( U. S.,4. ) (Accepted May 8th, 1984) K<'r words': chandelier cells ecrct~ral cortex GABA ncurons -- epilcps 3 Axon terminals of chandelier cells were analvzed in monkcvs with cortical local epilepsy produced hy alumina gel to determine il this type of GABAergic terminal is lost at epileptic loci. These tcrminals form a dcnse plexus with the axon initial scgments of pyrami- dal neurons, especially those in layers II and II1. Axon initial segments of pyramidal neurons were traccd for at lea';l 4(i um in serial thin sections and hewed this point were observed to become mvelinated. In single sections, 10- 15 axon terminals were lound to form symmetric synapses throughout the entire length of the axon initial segments irom noncpileptic preparations and were observed to synapsc with only these structures and not adjacent dendritcs or spines. In epileptic cortex, the axon initial scgmenls el pyramidal neu- rons ~crc apposcd by glial profiles that contamcd cluslers of filaments typical of reactivc astrocytes. Only a few, small axon termimtls were observed to form symmetric synapses with these axon initial segments. Thus, thc chandelier cell axons appeared to degenerate in epileptic cortex. The highly strategic site of GABAergic inhibitory synapses on axon initial segments suggests that they cxcrt a strong influence on the output of pyramidal cells. The near absence of thcsc chandclicr cell axons in epileptic foci most likely conlributcs to the hyperexcitability of neurons. INTRODt r('TI()N were classified as aspinous and sparsely spinous stel- late cells, subsequent Golgi studies have revealed It is now apparent that in some varieties of epilep- major subclasses of this category based on cell body sy, a severe deficit occurs in the cortical GABAergic shape, dendritic orientation and axonal distribu- system. Numerous studies of experimental models tion 13,2°,2<*,>. One cell type, the basket cell, was sug- that resemble post-traumatic epilepsy have shown a gested to be GABAergic because its axonal plexus loss of GABAergic terminals in epileptic foei e-' ca. A that forms pericellular nests around pyramidal cells quantitative assessment at the electron microscopic in laver V was GAD-positive in immunocytochemi- level has indicated that this loss is preferential for cal preparationsS,le,-'t,2L This identification was given GABAergic, symmetric synapses2e. Biochemical further support from recent studies that utilized col- studies also support this finding in that indices for chicine-treated immtinocytochemical preparations other neurotransmitters were not reduced as se- that displayed the cell bodies of this neuronal verely as those for GABA I,e,.<. These findings in ani- type li,iz. Since the terminals of this plexus form sym- mal models have received corroboration from bio- metric axosomatic synapses, they are readily quanti- chemical results of human epileptic loci >. Therefore, fied and were shown to be reduced by S()c~ al epilep- a loss of GABAergic terminals appears to be a hall- tic foci e-~. These data indicated that a basket cell defi- mark of epileptic loci. cit occurs at epileptic foci and as a result the laver V The initial inmmnocytochemical study on the mor- pyramidal cells at such sites arc probably more hy- phology of cortical GABAcrgic neurons revealed an percxcitable than normal. abundant variety of stained cell types distributed The present stud,,,' was undertaken to determine if throughout all layers of cortex -q. This study localized another cortical GABAergic cell lype was reduced in the synthesizing enzyme of GABA, glutamate decar- function at epileptic foci. The cell type chosen for this boxvlase (GAD). Although most of these neurons analysis was the chandelicr cell. Szcntfigothai and ('orrevl?omh'nce. Charles E. Ribak, Department of Anatomy, University of California, hvine, ('A 92717, U .S. ,,k. Ilil06-S993i85 $03.31i ~ IriS5 El~cxicr Science Publishers B.V 252 /\rbib :~ first described this neuron in Golgi prepara-. from the embedded specimens and stained with tions. This neuron is characterized by a small soma (I.05cf toluidine blue. Specimens were oriented in with aspinous dendrites in layers I1 and 111. The chan- the ultramicrotome to obtain SeCtions thai yielded delier cell's axon forms numerous vertical chains tha! the longest segments of apical dendrites. The ~dja- appear to be apposed to pyramidal cell apical den- cent thin sections from these specimens usually had drites in light microscopic preparations Is,~3. Howe~- the most number of identified axon initial segments cr, Somogyi > subsequently demonstrated in eleclron These sections were then stained with uranyl acetate microscopic preparations that these axons form swn- and lead citrate and examined ot~ ~ × 2 mm formvar, metric synapses with the axon initial segment,~ of p~- coated slot grids with the electron microscopc, ramidal cells in layers 11 and 111. Further studies have confirmed these electron microscopic obserw~tions in RESUI:I-S numerous species anti cortical regions +'`>.> including the hippocampus ~1. The morphology of these lermi- All observations were obtained from electron mi- nals and the localization of GAD-positive reaction croscopic preparations of monkey sensorimotor cor- product within these terminals s,>.et,~: have indicated tex. The analysis in the present study was limited to that they are GABAergic. These data suggest that the axon initial segments of pyramidal cells in layers chandelier cell axon terminals exert a strong inhibito- 11, IlI and V. Since the findings from the nonepiteptic ry influence on the output of pyramidal cells. A loss hemisphere were similar to those described in a pre- of such a plexus of axons might also contribute to ~hc vious study of normal primate sensorimotor cortex>, hyperexcitability of neurons in an epileptic focus. they will be presented first. Then, the data obtained from epileptic cortex will be compared with the data MATERIALS AND METHODS from the nonepileptic cortex. The present study utilized specimens obtained Nonepileptic cortex from 3 of the 5 experimental monkeys from a prc- A previous study 22 from this laboratory described vious study-'~. All of the monkeys had received alumi- the features of nonepileptic monkey sensorimotor na gel applications to the left cerebral hemispheres to cortex in electron microscopic preparanons. De- produce seizure foci. Two of these monkeys (animals scnptions of layer V pyramidal neurons and adjacenl 3 and 5 from Ribak et al.>) received intracortical in- neuropil regions were provided. Briefly, layer V py- jections directly into both pre- and postcentral gyri. ramidal neurons have multiangular-shaped somata The remaining experimental monkey (animal 2 from formed by an array of basal dendrites, a single apical Ribak et al. ~3) had an injection of alumina gel limited dendrite and a single axon usually located between to the subarachnoid space in the area of the central the basal dendrites. Much of the soma is occupied by sulcus. Electrocorticography of all experimental ani- a large, rounded nucleus wh~se nucleoplasm con- mals verified epileptic foci > and subsequently, the tains a relatively homogeneous sprinkling of electron- monkeys were fixed by intracardiac perfusions of a opaque chromatin and a centrally located nucleo- mixture of two aldehydes. The fixative solution con- lus ]~.22. Pyramidal neurons contain numerous orga- tained 4% paraformaldehyde, 0.1% glutaraldehyde. nelles in the perikaryal cytoplasm including both free and 0.002% CaCI~ in a 0.12 M phosphate buffer. ribosomes and cisternae of granular endoptasmic re- Blocks of cortical tissue were obtained from the uculum. Terminals thai form axosomatic s}napses epileptic focus and the homologous area in the con- with these neurons make only ,~ymmetnc synapses. tralateral nonepileptic cortex. All blocks were sec- Pyramidal neurons in layers II and III are somewhat tioned on a Sorvall TC-2 tissue sectioner at a thick- smaller than those in layer V. bul they share the same ness of 150 urn. Specimens that contained the entire ultrastructural characteristics, Since our prewous ul- cortical thickness were cut from these sections. trastructural studv 22 provided details on the somata These specimens were postfixed in 2% OsOa for I h. and dendrites of pyramidal neurons and the axon ter- dehydrated in ethanol and embedded in Epon. For minals thai formed synapses with these structures, light microscopy, semithin 1 um sections were cut the present study will involve primarily an analysis 253 of the synaptic contacts \`` itll aXOil initial Scglnenls of cells have somewhat fewer terminals that synapse pyranlidal netlrons. with their initial segments. These findings are consis- The axon initial segmeill {irises from the axon hill- tenl with a previous quantitative description of axon ock region of the neuronal cell hod\'. Peters ct ill. > initial segments of pyramidal ncclions ill prmlate seN- provide a COlllplctc description of the feattll-es of soIimotor cortex 2s. In lhat sttldv, Sloper and Powell > ~lxon initial segments. Such features will bl-icfh' bc reported that the total length of all axon initial seg- describcd lind attention will bc given to those slttlC- nlenl of a pyralllidal cell in ]avers I1 or I11 received ttlres and rehiiionships th{it appe:,lr differcnt in tilL' 13.4
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