Literature DB >> 27856766

Context-dependent memory traces in the crab's mushroom bodies: Functional support for a common origin of high-order memory centers.

Francisco Javier Maza1, Julieta Sztarker1, Avishag Shkedy1, Valeria Natacha Peszano1, Fernando Federico Locatelli1, Alejandro Delorenzi2.   

Abstract

The hypothesis of a common origin for the high-order memory centers in bilateral animals is based on the evidence that several key features, including gene expression and neuronal network patterns, are shared across several phyla. Central to this hypothesis is the assumption that the arthropods' higher order neuropils of the forebrain [the mushroom bodies (MBs) of insects and the hemiellipsoid bodies (HBs) of crustaceans] are homologous structures. However, even though involvement in memory processes has been repeatedly demonstrated for the MBs, direct proof of such a role in HBs is lacking. Here, through neuroanatomical and immunohistochemical analysis, we identified, in the crab Neohelice granulata, HBs that resemble the calyxless MBs found in several insects. Using in vivo calcium imaging, we revealed training-dependent changes in neuronal responses of vertical and medial lobes of the HBs. These changes were stimulus-specific, and, like in the hippocampus and MBs, the changes reflected the context attribute of the memory trace, which has been envisioned as an essential feature for the HBs. The present study constitutes functional evidence in favor of a role for the HBs in memory processes, and provides key physiological evidence supporting a common origin of the arthropods' high-order memory centers.

Entities:  

Keywords:  Arthropoda; evolution; homology; in vivo Ca2+ imaging; memory centers

Mesh:

Year:  2016        PMID: 27856766      PMCID: PMC5150377          DOI: 10.1073/pnas.1612418113

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  59 in total

1.  Pattern and process in the evolution of learning.

Authors:  Mauricio R Papini
Journal:  Psychol Rev       Date:  2002-01       Impact factor: 8.934

2.  Behaviorally related neural plasticity in the arthropod optic lobes.

Authors:  Martín Berón de Astrada; Mercedes Bengochea; Julieta Sztarker; Alejandro Delorenzi; Daniel Tomsic
Journal:  Curr Biol       Date:  2013-07-03       Impact factor: 10.834

3.  Mushroom bodies of the cockroach: their participation in place memory.

Authors:  M Mizunami; J M Weibrecht; N J Strausfeld
Journal:  J Comp Neurol       Date:  1998-12-28       Impact factor: 3.215

4.  Mapping membrane potential transients in crayfish (Procambarus clarkii) optic lobe neuropils with voltage-sensitive dyes.

Authors:  S Yagodin; C Collin; D L Alkon; N F Sheppard; D B Sattelle
Journal:  J Neurophysiol       Date:  1999-01       Impact factor: 2.714

5.  Contextual Pavlovian conditioning in the crab Chasmagnathus.

Authors:  María Sol Fustiñana; Martín Carbó Tano; Arturo Romano; María Eugenia Pedreira
Journal:  Anim Cogn       Date:  2012-11-01       Impact factor: 3.084

6.  Comparative brain architecture of the European shore crab Carcinus maenas (Brachyura) and the common hermit crab Pagurus bernhardus (Anomura) with notes on other marine hermit crabs.

Authors:  Jakob Krieger; Andy Sombke; Florian Seefluth; Matthes Kenning; Bill S Hansson; Steffen Harzsch
Journal:  Cell Tissue Res       Date:  2012-02-29       Impact factor: 5.249

7.  Drosophila mushroom body Kenyon cells generate spontaneous calcium transients mediated by PLTX-sensitive calcium channels.

Authors:  Shaojuan Amy Jiang; Jorge M Campusano; Hailing Su; Diane K O'Dowd
Journal:  J Neurophysiol       Date:  2005-03-16       Impact factor: 2.714

8.  Mushroom body extrinsic neurons in the honeybee brain encode cues and contexts differently.

Authors:  Syed Abid Hussaini; Randolf Menzel
Journal:  J Neurosci       Date:  2013-04-24       Impact factor: 6.167

9.  Identification of individual neurons reflecting short- and long-term visual memory in an arthropodo.

Authors:  Daniel Tomsic; Martén Berón de Astrada; Julieta Sztarker
Journal:  J Neurosci       Date:  2003-09-17       Impact factor: 6.167

Review 10.  Memorable trends.

Authors:  Yadin Dudai; Richard G M Morris
Journal:  Neuron       Date:  2013-10-30       Impact factor: 17.173

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  11 in total

Review 1.  The role of the hippocampus in navigation is memory.

Authors:  Howard Eichenbaum
Journal:  J Neurophysiol       Date:  2017-02-01       Impact factor: 2.714

2.  Mushroom body evolution demonstrates homology and divergence across Pancrustacea.

Authors:  Nicholas James Strausfeld; Gabriella Hanna Wolff; Marcel Ethan Sayre
Journal:  Elife       Date:  2020-03-03       Impact factor: 8.140

3.  Contextual memory reactivation modulates Ca2+-activity network state in a mushroom body-like center of the crab N. granulata.

Authors:  Francisco Javier Maza; Francisco José Urbano; Alejandro Delorenzi
Journal:  Sci Rep       Date:  2022-07-06       Impact factor: 4.996

4.  The velvet worm brain unveils homologies and evolutionary novelties across panarthropods.

Authors:  Christine Martin; Henry Jahn; Mercedes Klein; Jörg U Hammel; Paul A Stevenson; Uwe Homberg; Georg Mayer
Journal:  BMC Biol       Date:  2022-01-25       Impact factor: 7.364

5.  Shore crabs reveal novel evolutionary attributes of the mushroom body.

Authors:  Nicholas Strausfeld; Marcel E Sayre
Journal:  Elife       Date:  2021-02-09       Impact factor: 8.140

6.  Immunocytochemical Localization of Enzymes Involved in Dopamine, Serotonin, and Acetylcholine Synthesis in the Optic Neuropils and Neuroendocrine System of Eyestalks of Paralithodes camtschaticus.

Authors:  Elena Kotsyuba; Vyacheslav Dyachuk
Journal:  Front Neuroanat       Date:  2022-04-08       Impact factor: 3.543

7.  An insect-like mushroom body in a crustacean brain.

Authors:  Gabriella Hannah Wolff; Hanne Halkinrud Thoen; Justin Marshall; Marcel E Sayre; Nicholas James Strausfeld
Journal:  Elife       Date:  2017-09-26       Impact factor: 8.140

8.  Adaptations to extreme conditions.

Authors:  Barbara S Beltz
Journal:  Elife       Date:  2019-08-30       Impact factor: 8.140

9.  Neuroanatomy of a hydrothermal vent shrimp provides insights into the evolution of crustacean integrative brain centers.

Authors:  Julia Machon; Jakob Krieger; Rebecca Meth; Magali Zbinden; Juliette Ravaux; Nicolas Montagné; Thomas Chertemps; Steffen Harzsch
Journal:  Elife       Date:  2019-08-06       Impact factor: 8.140

10.  Shells as 'extended architecture': to escape isolation, social hermit crabs choose shells with the right external architecture.

Authors:  Jakob Krieger; Marie K Hörnig; Mark E Laidre
Journal:  Anim Cogn       Date:  2020-08-08       Impact factor: 3.084

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