Pilocarpine Induced Behavioral and Biochemical Alterations in Chronic Seizure-Like Condition in Adult Zebrafish
Abstract
:1. Introduction
2. Results
2.1. Pilocarpine-Induced Seizure-Like Behavior
2.2. Mean Seizure Score
2.3. Total Distance Travelled, Time Spent in Upper and Lower Half of the Tank
2.4. Comparison of Locomotor Pattern and Behavior
2.5. Modulation of Inflammatory Markers (HMGB1, TLR4, NF-κB, TNF-α, and IL-1), BDNF, CREB-1 and NPY upon Pilocarpine Exposure
2.5.1. HMGB1
2.5.2. TLR4
2.5.3. NF-κB
2.5.4. TNF-α
2.5.5. IL-1
2.5.6. BDNF
2.5.7. CREB-1
2.5.8. NPY
2.6. Modulation of Neurotransmitters Levels in Zebrafish Brain
2.7. Proteomic Analysis
3. Discussion
4. Material and Methods
4.1. Experimental Equipment and Chemicals
4.2. Zebrafish (Danio rerio) Care and Maintenance
4.3. Pilocarpine-Induced Seizure Behavior
Experimental Design
4.4. Epilepsy Behavior and Seizure Score Recording
4.5. Gene Expression Studies
4.5.1. Brain Harvesting
4.5.2. Isolation of RNA and First-Strand cDNA Synthesis
4.5.3. StepOne®® Real-time PCR
4.6. Brain Neurotransmitter Analysis
4.7. Zebrafish Brain Protein Estimation
4.7.1. In-Solution Tryptic Digestion
4.7.2. Sample Desalting/Cleanup Using Spin Columns
4.7.3. Nanoflow-Ultra High-Performance Liquid Chromatography-Tandem Mass Spectrometry (LC-MS/MS)
4.7.4. Protein Identification and Differential Expression Using PEAKS Bioinformatics Software
4.8. Software and Instrumentation
4.9. Statistical Analysis:
Author Contributions
Funding
Conflicts of Interest
References
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Score 0 | Normal Swimming |
Score 1 | Jittery movement at the top of the tank |
Score 2 | Ataxia/Hyperactivity |
Score 3 | Circular movement, Circling around small area |
Score 4 | Erratic burst movement with loss of posture/Corkscrew swimming |
S.N. | Accession | −10lgP | Coverage (%) | #Peptides | #Unique | Avg. Mass | Protein Description | Biological Process (GO) from Uniprot and Protein Analysis Through Evolutionary Relationships (PANTHER) |
---|---|---|---|---|---|---|---|---|
1 | P17561|EPD_DANRE | 89.06 | 15 | 2 | 2 | 24,472 | Ependymin | cell-matrix adhesion (GO:0007160) |
2 | tr|Q6DHB6|Q6DHB6_DANRE | 71.15 | 6 | 4 | 3 | 49,994 | Keratin 91 | NA |
3 | tr|A0A2R8Q6V3|A0A2R8Q6V3_DANRE | 38.54 | 4 | 2 | 2 | 57,453 | Keratin type II cytoskeletal 8 | NA |
4 | tr|A8WGN0|A8WGN0_DANRE | 38.54 | 4 | 2 | 2 | 57,660 | Keratin 8 | NA |
5 | tr|Q6P3K5|Q6P3K5_DANRE | 44.56 | 4 | 2 | 2 | 57,828 | Krt5 protein | NA |
6 | tr|Q9PUB5|Q9PUB5_DANRE | 44.56 | 4 | 2 | 2 | 58,587 | Type II cytokeratin | fin regeneration (GO:0031101) |
7 | tr|F1R5A5|F1R5A5_DANRE | 44.56 | 4 | 2 | 2 | 58,715 | Keratin 5 | |
8 | tr|A9JRN9|A9JRN9_DANRE | 61.41 | 3 | 2 | 2 | 95,635 | LOC794362 protein | axon development (GO:0061564) |
9 | tr|F1QCR7|F1QCR7_DANRE | 61.41 | 3 | 2 | 2 | 95,577 | Neurofilament medium polypeptide a | |
10 | tr|Q32PU7|Q32PU7_DANRE | 83.35 | 8 | 3 | 1 | 49,717 | Tubulin beta chain | microtubule-based process (GO:0007017) |
11 | tr|B8A516|B8A516_DANRE | 68.72 | 6 | 2 | 2 | 49,969 | Tubulin alpha chain | microtubule-based process (GO:0007017), microtubule cytoskeleton organization (GO:0000226), mitotic cell cycle (GO:0000278) |
12 | tr|Q502J6|Q502J6_DANRE | 79.92 | 25 | 2 | 2 | 11,412 | Gamma1a-synuclein | dopaminergic neuron differentiation (GO:0071542), larval locomotory behavior (GO:0008345) |
13 | tr|A0A2R8RP85|A0A2R8RP85_DANRE | 79.92 | 25 | 2 | 2 | 11,442 | Synuclein gamma b (breast cancer-specific protein 1) |
S.N. | Accession | −10lgP | Coverage (%) | #Peptides | #Unique | Avg. Mass | Protein Description | Biological Process (GO) From Uniprot and Protein Analysis Through Evolutionary Relationships (PANTHER) |
---|---|---|---|---|---|---|---|---|
1 | tr|Q6P5M9|Q6P5M9_DANRE | 153.04 | 50 | 16 | 2 | 49,787 | Tubulin beta chain | Cellular comp. organization or biogenesis (GO:0071840) |
2 | Q90486|HBB1_DANRE | 123.66 | 64 | 7 | 7 | 16,389 | Hemoglobin subunit beta-1 | Cellular comp. organization or biogenesis (GO:0071840), localization (GO: 0051179), Metabolic process (GO:0008152), response to stimulus (GO:0050896) |
3 | tr|Q6ZM12|Q6ZM12_DANRE | 40.06 | 16 | 2 | 2 | 16,295 | Hemoglobin beta adult 2 | |
4 | tr|Q6ZM13|Q6ZM13_DANRE | 80.62 | 29 | 3 | 2 | 15,413 | Hemoglobin alpha adult 2 | |
5 | tr|B3DG37|B3DG37_DANRE | 123.66 | 64 | 7 | 7 | 16,389 | Ba1 protein | |
6 | tr|Q803Z5|Q803Z5_DANRE | 83.91 | 43 | 5 | 1 | 15,508 | Hbaa1 protein | |
7 | tr|Q6DGK4|Q6DGK4_DANRE | 40.06 | 16 | 2 | 2 | 16,279 | Zgc:92880 protein | |
8 | tr|Q9DEU2|Q9DEU2_DANRE | 112.71 | 10 | 8 | 2 | 112,703 | Sodium/potassium-transporting ATPase subunit alpha | Biological regulation (GO:0065007), localization (GO: 0051179), |
9 | Q7ZVF9|ACTB2_DANRE | 105.86 | 28 | 6 | 6 | 41,753 | Actin cytoplasmic 2 | Cellular process (GO:0009987), localization (GO: 0051179) |
10 | Q7ZVI7|ACTB1_DANRE | 116.98 | 27 | 7 | 1 | 41,767 | Actin cytoplasmic 1 | |
11 | tr|A8WG05|A8WG05_DANRE | 105.86 | 28 | 6 | 6 | 41,753 | Bactin2 protein | |
12 | tr|B2GS08|B2GS08_DANRE | 116.98 | 27 | 7 | 1 | 41,710 | Bactin1 protein | |
13 | tr|R4GE02|R4GE02_DANRE | 96.97 | 23 | 4 | 3 | 27,149 | Si:ch211-113a14.11 | Cellular comp. organization or biogenesis (GO:0071840) |
14 | tr|Q7ZU04|Q7ZU04_DANRE | 90.53 | 20 | 5 | 5 | 42,916 | Creatine kinase brain b | NA |
15 | tr|Q9I8N9|Q9I8N9_DANRE | 81.04 | 29 | 3 | 3 | 14,918 | Brain-type fatty acid-binding protein | NA |
16 | tr|A0A2R8Q1X2|A0A2R8Q1X2_DANRE | 78.78 | 12 | 3 | 3 | 47,246 | Enolase 1a (alpha) | Glycolytic process (GO:0006096) |
17 | tr|Q08BA1|Q08BA1_DANRE | 77.71 | 7 | 3 | 3 | 59,744 | ATP synthase subunit alpha | Metabolic process (GO:0008152), response to stimulus (GO:0050896) |
18 | tr|A8WGC6|A8WGC6_DANRE | 53.73 | 6 | 2 | 2 | 55,130 | ATP synthase subunit beta | |
19 | tr|Q6PC77|Q6PC77_DANRE | 61.34 | 29 | 3 | 3 | 18,258 | ATP synthase subunit d mitochondrial | |
20 | Q5MJ86|G3P2_DANRE | 76.85 | 8 | 2 | 2 | 36,107 | Glyceraldehyde-3-phosphate dehydrogenase 2 | Metabolic process (GO:0008152) |
21 | tr|Q8JHI0|Q8JHI0_DANRE | 67.61 | 12 | 3 | 3 | 32,763 | Solute carrier family 25 (mitochondrial carrier; adenine nucleotide translocator) member 5 | Transporter activity (GO:0005215) |
22 | tr|F1R5A5|F1R5A5_DANRE | 67.55 | 5 | 4 | 2 | 58,715 | Keratin 5 | Fin regeneration (GO:0031101) |
23 | tr|I3IRY2|I3IRY2_DANRE | 46.87 | 10 | 2 | 2 | 15,746 | Keratin type 1 c19e (Fragment) | NA |
24 | tr|F1R8U0|F1R8U0_DANRE | 46.87 | 4 | 2 | 2 | 47,785 | Keratin 94 | NA |
25 | tr|Q1RLR3|Q1RLR3_DANRE | 46.87 | 3 | 2 | 2 | 50,931 | Keratin 93 | NA |
26 | tr|Q1LXJ9|Q1LXJ9_DANRE | 46.87 | 3 | 2 | 2 | 49,934 | Keratin type 1 c19e | NA |
27 | tr|Q24JW4|Q24JW4_DANRE | 66.4 | 14 | 3 | 3 | 35,677 | Flj13639 | NA |
28 | Q90XG0|TPISB_DANRE | 65.52 | 11 | 2 | 2 | 26,828 | Triosephosphate isomerase B | Metabolic process (GO:0008152) |
29 | P17561|EPD_DANRE | 55.6 | 12 | 2 | 2 | 24,472 | Ependymin | Cell-matrix adhesion (GO:0007160) |
30 | Q7T356|143BB_DANRE | 44.88 | 10 | 2 | 2 | 27,393 | 14-3-3 protein beta/alpha-B | Cell cycle (GO:0007049), Signal transduction (GO:0007165) |
31 | tr|A4FVM3|A4FVM3_DANRE | 44.86 | 7 | 2 | 2 | 36,022 | LOC557717 protein (Fragment) | Exocytosis (GO:0006887), Intracellular protein transport (GO:0006886), lysosomal transport (GO:0007041) |
32 | tr|A9JRN9|A9JRN9_DANRE | 92.47 | 8 | 5 | 4 | 95,635 | LOC794362 protein | ND |
33 | tr|A0A2R8QP59|A0A2R8QP59_DANRE | 44.86 | 4 | 2 | 2 | 66,189 | Syntaxin binding protein 1b | Localization (GO: 0051179), multicellular organismal process (GO: 0032501), signaling (GO:0023052). |
34 | tr|F1QM13|F1QM13_DANRE | 44.86 | 4 | 2 | 2 | 67,075 | Syntaxin-binding protein 1a | |
35 | tr|A2BGE0|A2BGE0_DANRE | 44.86 | 3 | 2 | 2 | 68,575 | Si:rp71-10d23.3 | Localization (GO:0051179), multicellular organismal process (GO:0032501), |
36 | tr|F1QYN7|F1QYN7_DANRE | 33.39 | 9 | 2 | 2 | 21,828 | Myelin protein zero | Cellular process (GO:0009987) |
37 | tr|F8W3W8|F8W3W8_DANRE | 111.06 | 60 | 9 | 9 | 10,776 | Myelin basic protein a | |
38 | tr|A0A2R8QC30|A0A2R8QC30_DANRE | 33.39 | 9 | 2 | 2 | 22,667 | Uncharacterized protein | NA |
39 | tr|A0A2R8Q6P3|A0A2R8Q6P3_DANRE | 33.39 | 8 | 2 | 2 | 25,013 | Uncharacterized protein | NA |
40 | tr|Q0D294|Q0D294_DANRE | 111.32 | 42 | 5 | 5 | 11,351 | Histone H4 | Nucleosome assemble (GO:0006334) |
41 | tr|Q6GQM9|Q6GQM9_DANRE | 98.45 | 15 | 4 | 2 | 46,841 | Eno2 protein | Metabolic process (GO:0008152) |
42 | Q6PI52|CALM_DANRE | 98.01 | 52 | 6 | 6 | 16,838 | Calmodulin | Biological regulation (GO:0065007), Cellular component organization or biogenesis (GO:0071840), cellular process (GO:0009987) |
43 | tr|Q7SZP4|Q7SZP4_DANRE | 94.54 | 15 | 6 | 5 | 64,751 | Zgc:65851 | Nervous system development (GO:0007399) |
44 | tr|F1QCR7|F1QCR7_DANRE | 92.47 | 8 | 5 | 4 | 95,577 | Neurofilament medium polypeptide a | Axon development (GO:0061564) |
45 | tr|A0A2R8RRA6|A0A2R8RRA6_DANRE | 92.13 | 8 | 4 | 4 | 74,958 | Serotransferrin | Hemoglobin biosynthetic process (GO:0042541) |
46 | tr|F1Q8F1|F1Q8F1_DANRE | 87.46 | 9 | 4 | 3 | 54,195 | Internexin neuronal intermediate filament protein alpha b | Neuron projection morphogenesis (GO:0048812) |
47 | tr|Q58EH1|Q58EH1_DANRE | 87.46 | 9 | 4 | 3 | 54,223 | Gefiltin | Neuron projection morphogenesis (GO:0048812) |
48 | tr|Q5BJC7|Q5BJC7_DANRE | 80.62 | 29 | 3 | 2 | 15,403 | Si:xx-by187g17.5 protein | hydrogen peroxide catabolic process (GO:0042744), protein heterooligomerization (GO:0051291) |
49 | tr|A0A0B5JW41|A0A0B5JW41_DANRE | 79.76 | 34 | 3 | 3 | 10,145 | Cd59 (Fragment) | defense response to Gram-positive bacterium (GO:0050830) |
50 | tr|B3DFP9|B3DFP9_DANRE | 78.8 | 50 | 4 | 4 | 15,537 | Apolipoprotein A-II | chordate embryonic development (GO:0043009), nuclear division (GO:0000280) |
51 | tr|A0A0R4IKF0|A0A0R4IKF0_DANRE | 65.95 | 18 | 4 | 4 | 30,140 | Apolipoprotein A-Ib | biological regulation (GO:0065007), Cellular component organization or biogenesis (GO:0071840), localization (GO:0051179), metabolic process (GO:0008152), multicellular organismal process (GO:0032501) |
52 | Q804W2|PRV7_DANRE | 78.02 | 33 | 3 | 3 | 12,029 | Parvalbumin-7 | biological regulation (GO:0065007) |
53 | tr|Q6TH32|Q6TH32_DANRE | 72.15 | 21 | 2 | 2 | 18,771 | Cofilin 1 | developmental process (GO:0032502), metabolic process (GO:0008152) |
54 | Q9PVK4|LDHBA_DANRE | 71.3 | 11 | 3 | 3 | 36,247 | L-lactate dehydrogenase B-A chain | metabolic process (GO:0008152) |
55 | tr|Q7T334|Q7T334_DANRE | 69.4 | 10 | 2 | 2 | 35,420 | Malate dehydrogenase | |
56 | tr|U3JAS0|U3JAS0_DANRE | 68.21 | 25 | 3 | 3 | 15,001 | Synaptosomal-associated protein | cellular protein-containing complex assembly (GO:0034622), synaptic vesicle exocytosis (GO:0016079), vesicle fusion to plasma membrane (GO:0099500) |
57 | tr|Q7SX92|Q7SX92_DANRE | 63.05 | 21 | 2 | 2 | 13,341 | Beta-synuclein | dopaminergic neuron differentiation (GO:0071542), larval locomotory behavior (GO:0008345) |
58 | tr|E7F9E8|E7F9E8_DANRE | 61.67 | 7 | 3 | 2 | 44,183 | Neurofilament light polypeptide a | axon development (GO:0061564) |
59 | tr|A0A0N4STS4|A0A0N4STS4_DANRE | 60.07 | 11 | 2 | 2 | 26,174 | Ubiquitin B | modification-dependent protein catabolic process (GO:0019941), protein ubiquitination (GO:0016567) |
60 | tr|B3DLH2|B3DLH2_DANRE | 60.07 | 5 | 2 | 2 | 51,501 | Zgc:172187 protein | |
61 | tr|A0JPF1|A0JPF1_DANRE | 60.07 | 5 | 2 | 2 | 59,921 | Zgc:153686 | |
62 | tr|Q7SXA3|Q7SXA3_DANRE | 60.07 | 16 | 2 | 2 | 17,999 | Ribosomal protein S27a | metabolic process (GO:0008152) |
63 | tr|B8JKN6|B8JKN6_DANRE | 59.82 | 12 | 2 | 2 | 17,404 | Peptidyl-prolyl cis-trans isomerase | protein refolding (GO:0042026) |
64 | tr|A0A2R8Q9S7|A0A2R8Q9S7_DANRE | 58.58 | 60 | 2 | 2 | 6468 | Si:dkey-46i9.1 | NA |
65 | tr|Q0ZBR7|Q0ZBR7_DANRE | 58.26 | 31 | 3 | 3 | 12,412 | Macrophage migration inhibitory factor | auditory receptor cell development (GO:0060117), cell proliferation (GO:0008283), embryonic morphogenesis (GO:0048598), inner ear development (GO:0048839), negative regulation of apoptotic process (GO:0043066) |
66 | tr|Q502C8|Q502C8_DANRE | 53.39 | 26 | 3 | 3 | 17,109 | Peroxiredoxin 5 | cell redox homeostasis (GO:0045454), cellular response to oxidative stress (GO:0034599), fin regeneration (GO:0031101), hydrogen peroxide catabolic process (GO:0042744) |
67 | tr|A0A0R4IG45|A0A0R4IG45_DANRE | 52.38 | 2 | 2 | 2 | 94,588 | Dynamin 1a | biological regulation (GO:0065007), cellular component organization or biogenesis (GO:0071840), cellular process (GO:0009987), localization (GO:0051179), metabolic process (GO:0008152) |
68 | tr|E9QF63|E9QF63_DANRE | 52.38 | 2 | 2 | 2 | 95,446 | Dynamin 1b | |
69 | tr|Q6TNV0|Q6TNV0_DANRE | 51.28 | 11 | 2 | 2 | 19,385 | Cytochrome c oxidase subunit 4I1 | metabolic process (GO:0008152) |
70 | tr|Q4VBT9|Q4VBT9_DANRE | 51.28 | 11 | 2 | 2 | 19,443 | Cox4i1 protein | metabolic process (GO:0008152), mitochondrial electron transport, cytochrome c to oxygen (GO:0006123) |
71 | tr|Q5TZ35|Q5TZ35_DANRE | 50.73 | 13 | 2 | 2 | 22,261 | Visinin-like 1b | NA |
72 | tr|A0A2R8RID5|A0A2R8RID5_DANRE | 50.34 | 5 | 2 | 2 | 84,805 | Aconitate hydratase mitochondrial | tricarboxylic acid cycle (GO:0006099) |
Q6IQM2|CYC_DANRE | 49.91 | 18 | 2 | 2 | 11,456 | Cytochrome c | mitochondrial electron transport, cytochrome c to oxygen (GO:0006123) | |
73 | Q8JH70|ALDCB_DANRE | 48.6 | 9 | 2 | 2 | 39,259 | Fructose-bisphosphate aldolase C-B | glycolytic process (GO:0006096) |
74 | tr|Q05AL9|Q05AL9_DANRE | 46.87 | 4 | 2 | 2 | 47,758 | Zgc:153629 protein | NA |
75 | tr|Q1JQ08|Q1JQ08_DANRE | 46.87 | 3 | 2 | 2 | 51,584 | Si:dkeyp-113d7.4 protein (Fragment) | NA |
76 | tr|F1R9V3|F1R9V3_DANRE | 42.3 | 4 | 2 | 2 | 71,094 | Si:dkey-4p15.3 | cellular process (GO:0009987), localization (GO:0051179), response to stimulus (GO:0050896) |
77 | tr|A0A0R4IMF8|A0A0R4IMF8_DANRE | 42.3 | 4 | 2 | 2 | 70,145 | Heat shock cognate 71 kDa protein | cellular process (GO:0009987), localization (GO:0051179), response to stimulus (GO:0050896) |
S.N. | Accession | Group Profile (Ratio, Control: Epileptic) | Description | PANTHER GO-Slim Biological Process (Danio rerio) |
---|---|---|---|---|
1 | tr|F8W3W8|F8W3W8_DANRE | 1.00:0.09 | Myelin basic protein a | No Match |
2 | tr|Q8AY63|Q8AY63_DANRE | 1.00:0 | Brain-subtype creatine kinase | No Match |
3 | tr|F1R3D3|F1R3D3_DANRE | 1.00:0.02 | Glyceraldehyde-3-phosphate dehydrogenase | No Match |
4 | tr|R4GE02|R4GE02_DANRE | 1.00:0.03 | Si:ch211-113a14.11 | Cellular component organization or biogenesis (GO:0071840 |
5 | tr|Q9I8N9|Q9I8N9_DANRE | 1.00:0.04 | Brain-type fatty acid-binding protein | No Match |
6 | tr|Q6IQP5|Q6IQP5_DANRE | 1.00:0 | Enolase 1 (Alpha) | No Match |
7 | tr|Q1LWD7|Q1LWD7_DANRE | 1.00:0.02 | Parvalbumin | No Match |
8 | tr|A0A0R4IS04|A0A0R4IS04_DANRE | 1.00:0 | Myelin protein zero | No Match |
9 | tr|B3DG37|B3DG37_DANRE | 1.00:0.03 | Ba1 protein | No Match |
10 | tr|E9QJ96|E9QJ96_DANRE | 1.00:0.03 | 14-3-3 protein beta/alpha-A (Fragment) | No Match |
11 | tr|Q08BA1|Q08BA1_DANRE | 1.00:0.08 | ATP synthase subunit alpha | Metabolic process (GO:0008152), Response to stimulus (GO:0050896) |
12 | tr|Q6PC77|Q6PC77_DANRE | 1.00:0 | ATP synthase subunit d mitochondrial | Metabolic process (GO:0008152) |
13 | tr|A8WGC6|A8WGC6_DANRE | 1.00:0.04 | ATP synthase subunit | Metabolic process (GO:0008152) |
14 | tr|Q24JW4|Q24JW4_DANRE | 1.00:0 | Flj13639 | Multicellular organismal process (GO:0032501) |
15 | tr|A3KPR4|A3KPR4_DANRE | 1.00:0.00 | Histone H4 | No Match |
16 | tr|Q7T334|Q7T334_DANRE | 1.00:0 | Malate dehydrogenase | Metabolic process (GO:0008152) |
17 | tr|Q6ZM12|Q6ZM12_DANRE | 1.00:0 | Hemoglobin beta adult 2 | localization (GO:0051179), Metabolic process (GO:0008152), Response to stimulus (GO:0050896) |
18 | tr|A0A0B5JW41|A0A0B5JW41_DANRE | 1.00:0.01 | Cd59 (Fragment) | No Match |
19 | tr|A0A0R4IKF0|A0A0R4IKF0_DANRE | 1.00:0 | Apolipoprotein A-Ib | Cellular component organization or biogenesis (GO:0071840), Biological regulation (GO:0065007), localization (GO:0051179), Metabolic process (GO:0008152), Multicellular organismal process (GO:0032501) |
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Paudel, Y.N.; Kumari, Y.; Abidin, S.A.Z.; Othman, I.; Shaikh, M.F. Pilocarpine Induced Behavioral and Biochemical Alterations in Chronic Seizure-Like Condition in Adult Zebrafish. Int. J. Mol. Sci. 2020, 21, 2492. https://doi.org/10.3390/ijms21072492
Paudel YN, Kumari Y, Abidin SAZ, Othman I, Shaikh MF. Pilocarpine Induced Behavioral and Biochemical Alterations in Chronic Seizure-Like Condition in Adult Zebrafish. International Journal of Molecular Sciences. 2020; 21(7):2492. https://doi.org/10.3390/ijms21072492
Chicago/Turabian StylePaudel, Yam Nath, Yatinesh Kumari, Syafiq Asnawi Zainal Abidin, Iekhsan Othman, and Mohd. Farooq Shaikh. 2020. "Pilocarpine Induced Behavioral and Biochemical Alterations in Chronic Seizure-Like Condition in Adult Zebrafish" International Journal of Molecular Sciences 21, no. 7: 2492. https://doi.org/10.3390/ijms21072492