Literature DB >> 31544621

Early-life injury produces lifelong neural hyperexcitability, cognitive deficit and altered defensive behaviour in the squid Euprymna scolopes.

Ryan B Howard1, Lauren N Lopes1, Christina R Lardie1, Paul P Perez1, Robyn J Crook1.   

Abstract

Injury occurring in the neonatal period in mammals is known to induce plasticity in pain pathways that may lead to pain dysfunction in later life. Whether these effects are unique to the mammalian nervous system is not well understood. Here, we investigate whether similar effects of early-life injury are found in a large-brained comparative model, the cephalopod Euprymna scolopes. We show that the peripheral nervous system of E. scolopes undergoes profound and permanent plasticity after injury of peripheral tissue in the early post-hatching period, but not after the same injury given in the later juvenile period. Additionally, both innate defensive behaviour and learning are impaired by injury in early life. We suggest that these similar patterns of nervous system and behavioural remodelling that occur in squid and in mammals indicate an adaptive value for long-lasting plasticity arising from early-life injury, and suggest that injuries inflicted in very early life may signal to the nervous system that the environment is highly dangerous. Thus, neonatal pain plasticity may be a conserved pattern whose purpose is to set the developing nervous system's baseline responsiveness to threat. This article is part of the Theo Murphy meeting issue 'Evolution of mechanisms and behaviour important for pain'.

Entities:  

Keywords:  behaviour; cephalopod; early-life injury; nociceptive sensitization; pain

Mesh:

Year:  2019        PMID: 31544621      PMCID: PMC6790388          DOI: 10.1098/rstb.2019.0281

Source DB:  PubMed          Journal:  Philos Trans R Soc Lond B Biol Sci        ISSN: 0962-8436            Impact factor:   6.237


  25 in total

1.  Arm injury produces long-term behavioral and neural hypersensitivity in octopus.

Authors:  Jean S Alupay; Stavros P Hadjisolomou; Robyn J Crook
Journal:  Neurosci Lett       Date:  2013-11-15       Impact factor: 3.046

2.  Peripheral injury induces long-term sensitization of defensive responses to visual and tactile stimuli in the squid Loligo pealeii, Lesueur 1821.

Authors:  Robyn J Crook; Trevor Lewis; Roger T Hanlon; Edgar T Walters
Journal:  J Exp Biol       Date:  2011-10-01       Impact factor: 3.312

3.  Early Procedural Pain Is Associated with Regionally-Specific Alterations in Thalamic Development in Preterm Neonates.

Authors:  Emma G Duerden; Ruth E Grunau; Ting Guo; Justin Foong; Alexander Pearson; Stephanie Au-Young; Raphael Lavoie; M Mallar Chakravarty; Vann Chau; Anne Synnes; Steven P Miller
Journal:  J Neurosci       Date:  2017-12-18       Impact factor: 6.167

4.  Long-term behavioral effects of repetitive pain in neonatal rat pups.

Authors:  K J Anand; V Coskun; K V Thrivikraman; C B Nemeroff; P M Plotsky
Journal:  Physiol Behav       Date:  1999-06

5.  Early life inflammatory pain induces long-lasting deficits in hippocampal-dependent spatial memory in male and female rats.

Authors:  Yoko O Henderson; Nicole C Victoria; Kiyoshi Inoue; Anne Z Murphy; Marise B Parent
Journal:  Neurobiol Learn Mem       Date:  2014-11-13       Impact factor: 2.877

6.  Early neonatal inflammation affects adult pain reactivity and anxiety related traits in mice: genetic background counts.

Authors:  Cristina Benatti; Silvia Alboni; Giacomo Capone; Daniela Corsini; Federica Caggia; Nicoletta Brunello; Fabio Tascedda; Joan M C Blom
Journal:  Int J Dev Neurosci       Date:  2009-08-07       Impact factor: 2.457

Review 7.  Cognitive modulation of pain: how do attention and emotion influence pain processing?

Authors:  Chantal Villemure; Catherine M Bushnell
Journal:  Pain       Date:  2002-02       Impact factor: 6.961

8.  Rapid Associative Learning and Stable Long-Term Memory in the Squid Euprymna scolopes.

Authors:  Emily A Zepeda; Robert J Veline; Robyn J Crook
Journal:  Biol Bull       Date:  2017-09-05       Impact factor: 1.818

9.  Neonatal pain, parenting stress and interaction, in relation to cognitive and motor development at 8 and 18 months in preterm infants.

Authors:  Ruth E Grunau; Michael F Whitfield; Julianne Petrie-Thomas; Anne R Synnes; Ivan L Cepeda; Adi Keidar; Marilyn Rogers; Margot Mackay; Philippa Hubber-Richard; Debra Johannesen
Journal:  Pain       Date:  2009-05       Impact factor: 6.961

10.  Priming of Adult Incision Response by Early-Life Injury: Neonatal Microglial Inhibition Has Persistent But Sexually Dimorphic Effects in Adult Rats.

Authors:  Orla Moriarty; YuShan Tu; Ameet S Sengar; Michael W Salter; Simon Beggs; Suellen M Walker
Journal:  J Neurosci       Date:  2019-02-22       Impact factor: 6.167

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  4 in total

1.  Evolution of mechanisms and behaviour important for pain.

Authors:  Edgar T Walters; Amanda C de C Williams
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-09-23       Impact factor: 6.237

2.  Behavioral and neurophysiological evidence suggests affective pain experience in octopus.

Authors:  Robyn J Crook
Journal:  iScience       Date:  2021-02-23

3.  Painful Truth: The Need to Re-Center Chronic Pain on the Functional Role of Pain.

Authors:  Vivian Santiago
Journal:  J Pain Res       Date:  2022-02-16       Impact factor: 2.832

4.  Animal sentience.

Authors:  Heather Browning; Jonathan Birch
Journal:  Philos Compass       Date:  2022-03-17
  4 in total

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