Skip to main content
SpringerLink
Log in

Memory regulation in feeding habit transformation to dead prey fish of Chinese perch (Siniperca chuatsi)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Memory drove a critical process of feeding habit transformation in Chinese perch when they re-trained to eat dead prey fish. To investigate the regulatory mechanism of cAMP-response element-binding protein (CREB) signaling pathway on the memory of Chinese perch during feeding habit transformation, the phosphorylation levels of upstream signal proteins of CREB between the control group (trained once) and the experimental group (trained twice) were measured. The results illustrated that the re-training was correlated to phosphorylation of extracellular regulated protein kinase (ERK1/2) and calcium/calmodulin-dependent protein kinase II (CaMKII), and dephosphorylation of protein kinase A (PKA) of Chinese perch. Inhibition of ERK1/2-CREB pathway decreased the mRNA levels of memory-related genes ((fos-related antigen 2 (fra2), CCAAT enhancer-binding protein delta (c/ebpb), immediate-early gene zif268 (zif268), proto-oncogenes c-fos (c-fox) and synaptotagmin-IV (sytIV)) and mRNA levels of appetite-related genes (agouti-related peptide (agrp) and ghrelin), and activation of PP1-CREB pathway increased the phosphorylated levels of CREB, the mRNA levels of memory-related genes (fra2, c/ebpb, zif268, and c-fox), and the mRNA levels of appetite-related genes (pro-opiomelanocortin (pomc) and leptin) in primary brain cells of Chinese perch. The memory in Chinese perch feeding habit transformation was associated with the ERK1/2-CREB and PP1-CREB pathways, which could regulate the transcription of memory-related genes and appetite-related genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Availability of data and material

All data used to arrive at the conclusions of this paper are present in this manuscript. The raw data is available from the authors on request.

References

  • Ahima RS (2006) Adipose tissue as an endocrine organ. Obesity 14:242S-249S

    Article  CAS  PubMed  Google Scholar 

  • Ajemian M, Sohel S, Mattila J (2015) Effects of turbidity and habitat complexity on antipredator behavior of three-spined sticklebacks (Gasterosteus aculeatus). Environ Biol Fish 98:45–55

    Article  Google Scholar 

  • Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89:121–145

    Article  CAS  PubMed  Google Scholar 

  • Arias J, Alberts A, Brindle P, Claret F, Smeal T, Karin M et al (1994) Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature 370:226

    Article  CAS  PubMed  Google Scholar 

  • Asztalos Z, Von Wegerer J, Wustmann G, Dombradi V, Gausz J, Spatz HC et al (1993) Protein phosphatase 1-deficient mutant Drosophila is affected in habituation and associative learning. J Neurosci 13:924–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benito E, Barco A (2010) CREB’s control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33:230–240

    Article  CAS  PubMed  Google Scholar 

  • Bozon B, Kelly A, Josselyn SA, Silva AJ, Davis S, Laroche S (2003) MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos Trans R Soc B 358:805–814

    Article  CAS  Google Scholar 

  • Caine D (2005) Memory from A to Z: keywords, concepts and beyond. J Clin Neurosci 12:611–611

    Article  Google Scholar 

  • Chen L, Miyamoto Y, Furuya K, Mori N, Sokabe M (2007) PREGS induces LTP in the hippocampal dentate gyrus of adult rats via the tyrosine phosphorylation international cooperative research CREB signaling. J Neurophysiol 98:1538–1548

    Article  CAS  PubMed  Google Scholar 

  • Chen DY, Bambah-Mukku D, Pollonini G, Alberini CM (2012) Glucocorticoid receptors recruit the CaMKIIα-BDNF-CREB pathways to mediate memory consolidation. Nat Neurosci 15:1707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng XY, He S, Liang XF, Song Y, Yuan XC, Li L et al (2015) Molecular cloning, expression and single nucleotide polymorphisms of protein phosphatase 1 (PP1) in mandarin fish (Siniperca chuatsi). Comp Biochem Phys B 189:69–79

    Article  CAS  Google Scholar 

  • Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365:855

    Article  CAS  PubMed  Google Scholar 

  • Cole CJ, Josselyn SA (2008) Transcription regulation of memory: CREB, CaMKIV, Fos/Jun, CBP, and SRF. Learn Mem A Compr Ref 4:547–566

  • Colley PA, Routtenberg A (1993) Long-term potentiation as synaptic dialogue. Brain Res Rev 18:115–122

    Article  CAS  PubMed  Google Scholar 

  • Costa-Mattioli M, Gobert D, Harding H, Herdy B, Azzi M, Bruno M et al (2005) Translational control of hippocampal synaptic plasticity and memory by the eIF2α kinase GCN2. Nature 436:1166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Countryman RA, Kaban NL, Colombo PJ (2005) Hippocampal c-fos is necessary for long-term memory of a socially transmitted food preference. Neurobiol Learn Mem 84:175–183

    Article  CAS  PubMed  Google Scholar 

  • Cui R, Delclos PJ, Schumer M, Rosenthal GG (2017) Early social learning triggers neurogenomic expression changes in a swordtail fish. Proc R Soc Lond B Biol Sci 284:20170701

    Google Scholar 

  • Dailey MJ, Moran TH, Holland PC, Johnson AW (2016) The antagonism of ghrelin alters the appetitive response to learned cues associated with food. Behav Brain Res 303:191–200

    Article  CAS  PubMed  Google Scholar 

  • Diano S, Farr SA, Benoit SC, McNay EC, da Silva I, Horvath B et al (2006) Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci 9:381

    Article  CAS  PubMed  Google Scholar 

  • Diéguez C, Vazquez MJ, Romero A, López M, Nogueiras R (2011) Hypothalamic control of lipid metabolism: focus on leptin, ghrelin and melanocortins. Neuroendocrinology 94:1–11

    Article  PubMed  Google Scholar 

  • Dou Y, He S, Liang X-F, Cai W, Wang J, Shi L et al (2018) Memory function in feeding habit transformation of mandarin fish (Siniperca chuatsi). J Mol Sci 19:1254

    Article  Google Scholar 

  • During MJ, Cao L, Zuzga DS, Francis JS, Fitzsimons HL, Jiao X et al (2003) Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat Med 9:1173

    Article  CAS  PubMed  Google Scholar 

  • Elias CF, Aschkenasi C, Lee C, Kelly J, Ahima RS, Bjorbæk C et al (1999) Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron 23:775–786

    Article  CAS  PubMed  Google Scholar 

  • Everley KA, Radford AN, Simpson SD (2016) Pile-driving noise impairs antipredator behavior of the european sea bass Dicentrarchus labrax. Adv Exp Med Biol 875:273–279

  • Farr SA, Banks WA, Morley JE (2006) Effects of leptin on memory processing. Peptides 27:1420–1425

    Article  CAS  PubMed  Google Scholar 

  • Ferguson GD, Vician L, Herschman HR (2001) Synaptotagmin IV. Mol Neurobiol 23:173–185

    Article  CAS  PubMed  Google Scholar 

  • Ferguson GD, Wang H, Herschman HR, Storm DR (2004) Altered hippocampal short-term plasticity and associative memory in synaptotagmin IV (−/−) mice. Hippocampus 14:964–974

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Li N, Lai Y, Luo X, Wang Y, Shi C, Huang Z, Wu S, Su J (2015) A novel fish cell line derived from the brain of Chinese perch Siniperca chuatsi: development and characterization. J Fish Biol 86:32–45

    Article  CAS  PubMed  Google Scholar 

  • Genoux D, Haditsch U, Knobloch M, Michalon A, Storm D, Mansuy IM (2002) Protein phosphatase 1 is a molecular constraint on learning and memory. Nature 418:970

    Article  CAS  PubMed  Google Scholar 

  • Genoux D, Bezerra P, Montgomery JM (2011) Intra-spaced stimulation and protein phosphatase 1 dictate the direction of synaptic plasticity. Eur J Neurosci 33:1761–1770

    Article  PubMed  Google Scholar 

  • Giralt A, Saavedra A, Carretón O, Xifró X, Alberch J, Pérez-Navarro E (2011) Increased PKA signaling disrupts recognition memory and spatial memory: role in Huntington’s disease. Hum Mol Genet 20:4232–4247

    Article  CAS  PubMed  Google Scholar 

  • He J, Yamada K, Zou L-B, Nabeshima T (2001) Spatial memory deficit and neurodegeneration induced by the direct injection of okadaic acid into the hippocampus in rats. J Neural Transm 108:1435–1443

    Article  CAS  PubMed  Google Scholar 

  • He S, Liang X-F, Sun J, Li L, Yu Y, Huang W et al (2013) Insights into food preference in hybrid F1 of Siniperca chuatsi (♀)× Siniperca scherzeri (♂) mandarin fish through transcriptome analysis. BMC Genomics 14:601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henderson YO, Smith GP, Parent MB (2013) Hippocampal neurons inhibit meal onset. Hippocampus 23:100–107

    Article  CAS  PubMed  Google Scholar 

  • Higgs S (2002) Memory for recent eating and its influence on subsequent food intake. Appetite 39:159–166

    Article  PubMed  Google Scholar 

  • Higgs S (2008) Cognitive influences on food intake: the effects of manipulating memory for recent eating. Physiol Behav 94:734–739

    Article  CAS  PubMed  Google Scholar 

  • Horiuchi J, Yamazaki D, Naganos S, Aigaki T, Saitoe M (2008) Protein kinase A inhibits a consolidated form of memory in Drosophila. Proc Natl Acad Sci U S A 105:20976–20981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horwood JM, Dufour F, Laroche S, Davis S (2006) Signalling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur J Neurosci 23:3375–3384

    Article  PubMed  Google Scholar 

  • Hotte M, Thuault S, Dineley KT, Hemmings HC Jr, Nairn AC, Jay TM (2007) Phosphorylation of CREB and DARPP-32 during late LTP at hippocampal to prefrontal cortex synapses in vivo. Synapse 61:24–28

    Article  CAS  PubMed  Google Scholar 

  • Jarome TJ, Ferrara NC, Kwapis JL, Helmstetter FJ (2016) CaMKII regulates proteasome phosphorylation and activity and promotes memory destabilization following retrieval. Neurobiol Learn Mem 128:103–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038

    Article  CAS  PubMed  Google Scholar 

  • Kanoski SE, Fortin SM, Ricks KM, Grill HJ (2013) Ghrelin signaling in the ventral hippocampus stimulates learned and motivational aspects of feeding via PI3K-Akt signaling. Biol Psychiatry 73:915–923

    Article  CAS  PubMed  Google Scholar 

  • Katche C, Bekinschtein P, Slipczuk L, Goldin A, Izquierdo IA, Cammarota M et al (2010) Delayed wave of c-Fos expression in the dorsal hippocampus involved specifically in persistence of long-term memory storage. Proc Natl Acad Sci U S A 107:349–354

    Article  CAS  PubMed  Google Scholar 

  • Kelley JL, Magurran AE (2003) Effects of relaxed predation pressure on visual predator recognition in the guppy. Behav Ecol Sociobiol 54:225–232

    Article  Google Scholar 

  • Kelly MP, Cheung Y-F, Favilla C, Siegel SJ, Kanes SJ, Houslay MD et al (2008) Constitutive activation of the G-protein subunit Gαs within forebrain neurons causes PKA-dependent alterations in fear conditioning and cortical Arc mRNA expression. Learn Mem 15:75–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kida S, Josselyn SA, de Ortiz SP, Kogan JH, Chevere I, Masushige S et al (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348

    Article  CAS  PubMed  Google Scholar 

  • Kieffer JD, Colgan PW (1992) The role of learning in fish behaviour. Rev Fish Biol Fish 2:125–143

    Article  Google Scholar 

  • Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bächinger HP, Brennan RG et al (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370:223

    Article  CAS  PubMed  Google Scholar 

  • Lehnert SJ, Heath DD, Devlin RH, Pitcher TE (2016a) Post-spawning sexual selection in red and white Chinook salmon (Oncorhynchus tshawytscha). Behav Ecol 28:1–10

  • Lehnert SJ, Pitcher TE, Devlin RH, Heath DD (2016b) Red and white Chinook salmon: genetic divergence and mate choice. Mol Ecol 25:1259–1274

    Article  PubMed  Google Scholar 

  • Liang X, Kiu J, Huang B (1998) The role of sense organs in the feeding behaviour of Chinese perch. J Fish Biol 52:1058–1067

    Article  Google Scholar 

  • Liang X, Oku H, Ogata H, Liu J, He X (2001) Weaning Chinese perch Siniperca chuatsi (Basilewsky) onto artificial diets based upon its specific sensory modality in feeding. Aquac Res 32:76–82

    Article  Google Scholar 

  • Lieberman LA, Tsokos GC (2010) The IL-2 defect in systemic lupus erythematosus disease has an expansive effect on host immunity. J Biomed Biotechnol 2010(6):740619

  • Liu Y, Chen GD, Lerner MR, Brackett DJ, Matsumoto RR (2005) Cocaine up-regulates fra-2 and σ-1 receptor gene and protein expression in brain regions involved in addiction and reward. J Pharmacol Exp Ther 314:770–779

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605–623

    Article  CAS  PubMed  Google Scholar 

  • López M, Lelliott CJ, Vidal-Puig A (2007) Hypothalamic fatty acid metabolism: a housekeeping pathway that regulates food intake. BioEssays 29:248–261

    Article  PubMed  Google Scholar 

  • Lopez-Salon M, Alonso M, Vianna MR, Viola H, e Souza TM, Izquierdo I et al (2001) The ubiquitin–proteasome cascade is required for mammalian long-term memory formation. Eur J Neurosci 14:1820–1826

    Article  CAS  PubMed  Google Scholar 

  • Lucon-Xiccato T, Dadda M (2014) Assessing memory in zebrafish using the one-trial test. Behav Process 106:1–4

    Article  Google Scholar 

  • Luo F, Zheng J, Sun X, Deng WK, Li B, Liu F (2017) Prelimbic cortex extracellular signal-regulated kinase 1/2 activation is required for memory retrieval of long-term inhibitory avoidance. Brain Res 1661:88–99

    Article  CAS  PubMed  Google Scholar 

  • Mansuy IM, Shenolikar S (2006) Protein serine/threonine phosphatases in neuronal plasticity and disorders of learning and memory. Trends Neurosci 29:679–686

    Article  CAS  PubMed  Google Scholar 

  • Marie H, Morishita W, Yu X, Calakos N, Malenka RC (2005) Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45:741–752

    Article  CAS  PubMed  Google Scholar 

  • Milinski M (2014) Arms races, ornaments and fragrant genes: The dilemma of mate choice in fishes. Neuro Biobehav Rev 46:567–572

    Article  Google Scholar 

  • Murray RD, Kim K, Ren SG, Chelly M, Umehara Y, Melmed S (2004) Central and peripheral actions of somatostatin on the growth hormone-IGF-I axis. J Clin Investig 114:349–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Namura S, Iihara K, Takami S, Nagata I, Kikuchi H, Matsushita K et al (2001) Intravenous administration of MEK inhibitor U0126 affords brain protection against forebrain ischemia and focal cerebral ischemia. Proc Natl Acad Sci U S A 98:11569–11574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neale JH, Klinger P, Agranoff B (1973) Camptothecin blocks memory of conditioned avoidance in the goldfish. Science 179:1243–1246

    Article  CAS  PubMed  Google Scholar 

  • Nielsen SE, Shafer AB, Boyce MS, Stenhouse GB (2013) Does learning or instinct shape habitat selection? Plos One. 8:e53721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oomura Y, Hori N, Shiraishi T, Fukunaga K, Takeda H, Tsuji M et al (2006) Leptin facilitates learning and memory performance and enhances hippocampal CA1 long-term potentiation and CaMK II phosphorylation in rats. Peptides 27:2738–2749

    Article  CAS  PubMed  Google Scholar 

  • Provenza FD, Pfister JA, Cheney CD (1992) Mechanisms of learning in diet selection with reference to phytotoxicosis in herbivores. J Range Manage 45:36–45

    Article  Google Scholar 

  • Rahman A, Khan KM, Al-Khaledi G, Khan I, Al-Shemary T (2012) Over activation of hippocampal serine/threonine protein phosphatases PP1 and PP2A is involved in lead-induced deficits in learning and memory in young rats. Neurotoxicology 33:370–383

    Article  CAS  PubMed  Google Scholar 

  • Reese ES (1989) Orientation behavior of butterflyfishes (family Chaetodontidae) on coral reefs: spatial learning of route specific landmarks and cognitive maps. Environ Biol Fish 25:79–86

    Article  Google Scholar 

  • Shanley LJ, Irving AJ, Harvey J (2001) Leptin enhances NMDA receptor function and modulates hippocampal synaptic plasticity. J Neurosci. 21:RC186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi LJ, Liang XF, He S, Peng J (2020) Primary cell culture and identification of brain neurons in Chinese perch (Siniperca chuatsi). J Fish Chin 044(001):43–48

  • Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311–317

    Article  CAS  PubMed  Google Scholar 

  • Trompf L, Brown C (2014) Personality affects learning and trade-offs between private and social information in guppies, Poecilia Reticulata. Anim Behav 88:99–106

    Article  Google Scholar 

  • Vandesompele J, Preter KD, Pattyn F et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3(7):research 0034.1

    Article  Google Scholar 

  • Veyrac A, Besnard A, Caboche J, Davis S, Laroche S (2014) The transcription factor Zif268/Egr1, brain plasticity, and memory. Progr Mol Biol Transl Sci: Elsevier. 89–129

  • Vitolo OV, Sant’Angelo A, Costanzo V, Battaglia F, Arancio O, Shelanski M (2002) Amyloid β-peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc Natl Acad Sci U S A 99:13217–13221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wadzinski B, Wheat W, Jaspers S, Peruski L, Lickteig R, Johnson G et al (1993) Nuclear protein phosphatase 2A dephosphorylates protein kinase A-phosphorylated CREB and regulates CREB transcriptional stimulation. Mol Cell Biol 13:2822–2834

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walker AK, Ibia IE, Zigman JM (2012) Disruption of cue-potentiated feeding in mice with blocked ghrelin signaling. Physiol Behav 108:34–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warburton K (2003) Learning of foraging skills by fish. Fish Fish 4:203–215

  • Wayner M, Armstrong D, Phelix C, Oomura Y (2004) Orexin-A (Hypocretin-1) and leptin enhance LTP in the dentate gyrus of rats in vivo. Peptides 25:991–996

    Article  CAS  PubMed  Google Scholar 

  • Yamashita T, Inui S, Maeda K, Hua DR, Takagi K, Fukunaga K et al (2006) Regulation of CaMKII by α4/PP2Ac contributes to learning and memory. Brain Res 1082:1–10

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki D, Horiuchi J, Miyashita T, Saitoe M (2010) Acute inhibition of PKA activity at old ages ameliorates age-related memory impairment in Drosophila. J Neurosci 30:15573–15577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshihara M, Montana ES (2004) The synaptotagmins: calcium sensors for vesicular trafficking. Neuroscientist 10:566–574

    Article  CAS  PubMed  Google Scholar 

  • Zamorano C, Fernández-Albert J, Storm DR, Carné X, Sindreu C (2018) Memory retrieval re-activates Erk1/2 signaling in the same set of CA1 neurons recruited during conditioning. Neuroscience 370:101–111

    Article  CAS  PubMed  Google Scholar 

  • Zhu YP, Xi SH, Li MY, Ding TT, Liu N, Cao FY et al (2017) Fluoride and arsenic exposure affects spatial memory and activates the ERK/CREB signaling pathway in offspring rats. Neurotoxicology 59:56–64

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was financially supported by the National Key R & D Program of China (2018YFD0900400), China Agriculture Research System (CARS-46), and National Natural Science Foundation of China (31772822).

Author information

Authors and Affiliations

  1. College of Fisheries, Chinese Perch Research Center, Huazhong Agricultural University, Wuhan, 430070, China

    Linjie Shi, Jiao Li, Xu-Fang Liang, Shan He, Yaqi Dou, Jian Peng, Wenjing Cai & Hui Liang

  2. Engineering Research Center of Green Development for Conventional Aquatic Biological Industry in the Yangtze River Economic Belt, Ministry of Education, Wuhan, 430070, China

    Linjie Shi, Jiao Li, Xu-Fang Liang, Shan He, Yaqi Dou, Jian Peng, Wenjing Cai & Hui Liang

Authors
  1. Linjie Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xu-Fang Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shan He
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yaqi Dou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jian Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wenjing Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hui Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Xu-Fang Liang and Shan He conceived and designed the experiments; Linjie Shi, Jiao Li, Yaqi Dou, Jian Peng, Wenjing Cai, and Hui Liang performed the experiments; Yaqi Dou completed in feeding trial; Linjie Shi, Jiao Li, and Jian Peng completed in vitro and in vivo experiments; Linjie Shi, Jiao Li, Wenjing Cai, Shan He, and Hui Liang wrote and revised the manuscript.

Corresponding authors

Correspondence to Xu-Fang Liang or Shan He.

Ethics declarations

Ethics approval

Our research was approved by the ethics committee from Huazhong Agricultural University (Wuhan, Hubei, China) and performed in accordance with the relevant institutional and national guidelines, and the manuscript must conform to the ARRIVE Guidelines for Reporting Animal Research.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare that they have no competing interests. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Linjie Shi and Jiao Li contributed equally to this work.

Xu-Fang Liang and Shan He contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shi, L., Li, J., Liang, XF. et al. Memory regulation in feeding habit transformation to dead prey fish of Chinese perch (Siniperca chuatsi). Fish Physiol Biochem 47, 1893–1907 (2021). https://doi.org/10.1007/s10695-021-01001-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-021-01001-z

Keywords

Search

Navigation