Long-term memory leads to synaptic reorganization in the mushroom bodies: a memory trace in the insect brain?
The insect mushroom bodies (MBs) are paired brain centers which, like the mammalian hippocampus, have a prominent function in learning and memory. Despite convergent evidence for their crucial role in the formation and storage of associative memories, little is known about the mechanisms underlying such storage. In mammals and other species, the consolidation of stable memories is accompanied by structural plasticity involving variations in synapse number and/or size. Here, we address the question of whether the formation of olfactory long-term memory (LTM) could be associated with changes in the synaptic architecture of the MB networks. For this, we took advantage of the modular architecture of the honeybee MB neuropil, where synaptic contacts between olfactory input and MB neurons are segregated into discrete units (microglomeruli) which can be easily visualized and counted. We show that the density in microglomeruli increases as a specific olfactory LTM is formed, while the volume of the neuropil remains constant. Such variation is reproducible and is clearly correlated with memory consolidation, as it requires gene transcription. Thus stable structural synaptic rearrangements, including the growth of new synapses, seem to be a common property of insect and mammalian brain networks involved in the storage of stable memory traces.
Hourcade
Benoît
B
Research Centre on Animal Cognition, Centre National de la Recherche Scientifique-Université Paul-Sabatier, Unité Mixte de Recherche 5169, 31062 Toulouse cedex 04, France.
Muenz
Thomas S
TS
Sandoz
Jean-Christophe
JC
Rössler
Wolfgang
W
Devaud
Jean-Marc
JM
D000818:Animals; D001516:Bees; D001921:Brain / Q000033:anatomy & histology* / Q000502:physiology; D003214:Conditioning, Classical / Q000502:physiology; D008568:Memory / Q000502:physiology*; D024521:Mushroom Bodies / Q000033:anatomy & histology / Q000502:physiology; D009473:Neuronal Plasticity / Q000502:physiology*; D019581:Neuropil / Q000502:physiology; D055696:Olfactory Perception / Q000502:physiology; D013569:Synapses / Q000502:physiology*
Learn Mem. 2001 Mar-Apr;8(2):53-62
11274250
Neuroscience. 2003;120(4):1137-48
12927218
Behav Neural Biol. 1994 Nov;62(3):259-63
7857249
Dev Neurobiol. 2009 May;69(6):350-64
19263416
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2007 Aug;193(8):801-24
17639413
Neuron. 2002 Sep 12;35(6):1019-27
12354393
J Comp Neurol. 1999 Feb 1;404(1):114-26
9886029
Nat Rev Neurosci. 2004 Jan;5(1):24-34
14708001
Nature. 1993 Nov 4;366:59-63
24308080
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2002 Jun;188(5):359-70
12073081
Eur J Neurosci. 2007 Dec;26(11):3193-206
18028113
Neuropharmacology. 2004 Oct;47(5):669-76
15458838
Neuron. 2007 Jan 4;53(1):103-15
17196534
Neuron. 2004 May 13;42(3):437-49
15134640
Dev Neurobiol. 2008 Jul;68(8):1007-17
18446779
Neurosci Lett. 2004 Feb 19;356(3):159-62
15036619
J Comp Psychol. 1983 Jun;97(2):107-19
6872507
Trends Neurosci. 2000 Apr;23(4):141-6
10717670
Proc Natl Acad Sci U S A. 2004 Mar 23;101(12):4268-73
15024125
Curr Opin Neurobiol. 2008 Oct;18(5):524-31
18834940
J Neurosci. 2005 Dec 14;25(50):11614-8
16354919
Cell Mol Life Sci. 2006 May;63(9):989-98
16596333
J Exp Biol. 1996;199(Pt 9):2011-9
9319922
Curr Opin Neurobiol. 2007 Oct;17(5):516-24
17950593
Nat Neurosci. 1999 Jan;2(1):74-8
10195183
Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19571-6
18073185
Nature. 1993 Jul 15;364(6434):238-40
8321320
Naturwissenschaften. 2001 Nov;88(11):472-6
11771476
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2009 Aug;195(8):733-40
19434412
J Neurosci. 2005 Feb 23;25(8):2062-9
15728846
Annu Rev Neurosci. 2005;28:275-302
16022597
J Comp Neurol. 2001 Jul 9;435(4):474-89
11406827
Brain Behav Evol. 2006;68(1):1-14
16557021
Prog Neurobiol. 2006 May;79(1):1-48
16781044
Learn Mem. 2009 Sep 30;16(10):607-15
19794186
J Neurosci. 2001 Aug 15;21(16):6395-404
11487663
Neurobiol Learn Mem. 2009 Nov;92(4):485-95
19539772
J Neurosci. 2009 Aug 19;29(33):10191-202
19692594
J Comp Neurol. 2004 Jul 26;475(3):303-14
15221947