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Proechimys Guyannensis: an Animal Model of Resistance to Epilepsy

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Proechimys Guyannensis: an Animal Model of Resistance to Epilepsy Epilepsia, 46(Suppl. 5):189–197, 2005 Blackwell Publishing, Inc. C International League Against Epilepsy Proechimys guyannensis:AnAnimal Model of Resistance to Epilepsy ∗ ∗ ∗ †Ricardo Mario Arida, †Fulvio Alexandre Scorza, ‡Reinaldo de Amorim Carvalho, ∗ and Esper A. Cavalheiro ∗ Disciplina de Neurologia Experimental, Universidade Federal de Sao˜ Paulo–UNIFESP, and †Laboratorio´ de Neurociencias,ˆ Nucleo´ de Pesquisas Tecnologicas´ (NPT)–Universidade de Mogi das Cruzes-UMC, Sao˜ Paulo, and ‡Centro Nacional de Primatas, Para,´ Brazil Summary: Purpose: The potential interest of Proechimys Wistar rats were able to induce status epilepticus (SE) in PG guyannensis (PG), a spiny rat species living in the Amazo- animals. Pilocarpine-induced SE in PG had a shorter duration, nian region, as an animal model of anticonvulsant mechanisms, rarely exceeding 2 h, in contrast to the 8- to 12- h long SE in prompted the investigation of the susceptibility of this animal the Wistar rat. Of the 61 PG animals injected with pilocarpine, species to different epileptogenic treatments. 48 presented with SE and only two presented with some sponta- Methods: Adult male Wistar and PG animals were submitted neous seizures after silent periods of 60 and 66 days. KA elicited to amygdala kindling, the pilocarpine model and the intrahip- self-sustained electrographic SE in PG animals, which lasted for pocampal kainic acid (KA) model. Electrographic, behavioral, 72 h. None of the surviving animals presented with spontaneous and neuropathological changes were compared between Wistar seizures in the long-term observation period (up to 120 days). and PG animals. Conclusions: These findings indicate that the PG animal Results: PG animals demonstrated a striking resistance to may have natural endogenous anticonvulsant mechanisms and reaching stage 5 of kindling. Of the 43 PG rats submitted to also may be an animal model that is resistant to epilepto- the kindling process, only three animals reached stage 5. In the genic treatments. KeyWords: Epilepsy—Proechimys guyan- pilocarpine and KA models, doses lower than those used in nensis—Kindling—Pilocarpine—Kainic acid. Proechimys guyannensis (PG), a rodent that lives in the to the epileptogenic treatment of the muscarinic choliner- Amazonian region, belongs to the Echimydae family, Hys- gic agonist pilocarpine (6). A previous study (7) showed tricomorpha suborder, Proechimys genus (1). PG, known that, in PG, behavioral and electrographic characteristics as Casiragua in Brazil, inhabits forests often near coasts of pilocarpine-induced status epilepticus (SE) are less in- and waterways. They are nocturnal, leaving their dens in tense than those observed in other laboratory animals (8) the evening to forage on the forest floor. The main char- and, in contrast to rats and mice, they do not develop spon- acteristic of this species is the high degree of maturity taneous seizures in the long run. shown by the newborn animal, which contrasts with the The reliability of PG as a natural animal model with majority of conventional animal species used in laborato- endogenous antiepileptic mechanisms prompted the in- ries. This animal species has received some attention as a vestigation of the susceptibility of this animal specie to natural host to infectious parasites (2), and has been ex- different experimental epilepsy paradigms. Accordingly, tensively studied in relation to their ecology and evolution the aim of the present study was to observe electrographic, (3–5). However, the organization of the PG brain has been behavioral, and neuropathological changes in PG using poorly studied. three models of temporal lobe epilepsy, i.e., the amygdala Animal studies have significantly contributed to the un- kindling, the pilocarpine model, and the intrahippocam- derstanding of the epileptogenesis and the mechanism of pal kainic acid (KA) model, and compare these findings action of several antiepileptic drugs. During a comparative with those widely reported in Wistar rats using the same investigation of the response of different rodent species to experimental protocols. proconvulsant agents, the PG was found to be resistant MATERIAL AND METHODS Address correspondence and reprint requests to Dr. R. M. Arida at Animals Disciplina de Neurologia Experimental, Universidade Federal de S˜ao Paulo–UNIFESP,Rua Botucat´u 862, Vila Clementino, CEP 04023-9000, Adult male Wistar and PG animals (2–3 months old, S˜ao Paulo, SP. Brazil. E-mail: [email protected] weighing 210–250 g) were used in these experiments. PG 189 190 R. M. ARIDA ET AL. animals, originally from the Brazilian Amazon basin, were EEG recordings bred in a colony established at the Universidade Federal For EEG recordings (pilocarpine- and KA-injected an- de S˜ao Paulo/Escola Paulista de Medicina and housed in imals), bipolar twisted wire electrodes were implanted a standard light-dark cycle with free access to food and stereotaxically in the right hippocampus and fixed to the water. Wistar rats of the same age and sex were obtained skull with dental acrylic cement. Notice that in KA experi- from the laboratory colony. ments, intrahippocampal injections were also made in the right hippocampus. Surface records were led from jew- Experimental procedures eler screws positioned bilaterally over the sensorimotor cortex. Following pilocarpine (Merck, Darmstadt, Ger- Amygdala kindling many) or KA injections, EEG activity was continuously Under deep anesthesia (Thionembutal, 50 mg/kg, i.p.), recorded for periods from 6 to 72 h. Animals that survived 43 PGs were stereotaxically implanted with twisted bipo- pilocarpine- or KA-induced SE were continuously moni- µ lar electrodes of nichrome wires (100 m), aimed at the tored during 24 h for the next 120 days for the detection right amygdala. To determine the appropriate stereotaxic of spontaneous seizures using a video-EEG system (Stel- coordinates for the amygdala in this animal species, some late System). Infrared-emitting lights were used during animals were submitted to stereotaxic surgery and histo- the dark periods to allow for video recording of the ani- logical examinations were performed to find out the ap- mals’ activity. Two independent observers were recruited propriate electrode placements. The following coordinates for EEG and behavioral analysis. were established for the PG: 2.3 mm posterior to bregma, 5.0 lateral to midline, and 8.5 deep. The same surgical Histology procedures were used for Wistar animals (n = 14) and At the end of the experiments, histological analyses stereotaxic coordinates were determined (2.5 mm poste- were performed for the three models of temporal lobe rior to bregma, 4.5 lateral to midline, and 8.5 deep) ac- epilepsy. Following variable survival times, ranging from cording to the atlas of Pellegrino and Cushman (9). The 1to120 days, animals were perfused and their brains pro- parameters of surgical techniques and stimulation were cessed for neo-Timm and Nissl methods following pro- performed following protocols similar to those described tocols described in previous studies (13,15). Naive Wis- in previous studies (10,11). tar and PG animals (n = 2) were perfused at times that matched those of experimental animals and served as Pilocarpine controls. Fourteen Wistar and 61 PG animals were used for the Statistical analysis pilocarpine procedure. Pilocarpine or vehicle injections Statistical analysis for the kindling procedure was done were performed following protocols similar to those de- using the t test and Fisher’s Exact test to analyze the after scribed in previous studies (12,13). To minimize the pe- discharge (AD) duration, number of stimuli to reach stage ripheral effects of pilocarpine, the cholinergic antagonist 5, and after discharge threshold (ADT) on PG and Wis- methyl-scopolamine (1 mg/kg, i.p.; Sigma, St. Louis, MO, tar animals. Significance was established at the p < 0.05 U.S.A.) was administered to all Wistar and PG animals. level. Intrahippocampal KA RESULTS Under deep anesthesia, PG animals were placed in Behavioral and EEG observations a stereotaxic apparatus. KA injections were made with a1µl Hamilton syringe in the CA1 subregion of the Kindling hippocampus. The appropriate hippocampal coordinates All Wistar rats (n = 14) submitted to kindling process (3.5 mm posterior to bregma, 4.0 lateral to midline, and reached stage 5. The mean number of stimulations and 4.0 from the cortex surface) were determined from pre- the AD duration required for the first generalized seizure vious experiments (6). The same surgical procedure was (stage 5) and for each stage of kindling for Wistar rats used for Wistar rats and stereotaxic coordinates were de- is similar to those observed in previous studies (16,17). termined according to the atlas of Pellegrino and Cush- From 43 PG animals submitted to the kindling process, man (9). KA (Sigma, St. Louis, MO, U.S.A.) was dis- only three animals reached stage 5. Of the 40 animals solved in artificial serum, pH = 7.4, and infused in a vol- that did not reach stage 5, 16 did not get beyond stage ume of 0.2 µl overaperiod of 2 min. Different doses 1, 14 did not get beyond stage 2, 7 did not get beyond of KA were tested in PG animals: 1.0 µg(n= 3), stage 3, and 3 did not get beyond stage 4. During kindling 0.5 µg(n= 3), 0.25 µg(n= 3), 0.1 µg(n= 10), (stages 1–3), all animals presented behavioral alterations and 0.06 µg(n= 5). Wistar rats (n = 6) received the similar to those observed in Wistar rats and other species, same KA dose (1 ug/0.2 ul) as described by Cavalheiro
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