The hippocampo-amygdala control of contextual fear expression is affected in a model of intellectual disability

Brain Structure and Function

Volumn 220, Issue 6, 2015, Pages 3673-3682

  Zhang, Chun Lei ^a   Houbaert, Xander ^a   Lepleux, Marilyn ^a   Deshors, Melissa ^a   Normand, Elisabeth ^a   Gambino, Frédéric ^a   Herzog, Etienne ^a   Humeau, Yann ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b Bordeaux Functional Genomic Center   (France)

Author keywords

Contextual fear expression; Hippocampal projections; Intellectual disability; Optogenetic

Indexed keywords

OPSIN; INTERLEUKIN 1 RECEPTOR ACCESSORY PROTEIN; INTERLEUKIN-1 RECEPTOR ACCESSORY PROTEIN-LIKE 1, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASOLATERAL AMYGDALA; BRAIN FUNCTION; CONDITIONED REFLEX; CONTEXTUAL FEAR; CONTROLLED STUDY; FEAR; HIPPOCAMPUS; IN VIVO STUDY; INTELLECTUAL IMPAIRMENT; MOUSE; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC EFFICACY; SYNAPTIC TRANSMISSION; AMYGDALA; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPSE; SYNAPTIC POTENTIAL;

AMYGDALA; ANIMALS; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; FEAR; HIPPOCAMPUS; INTELLECTUAL DISABILITY; INTERLEUKIN-1 RECEPTOR ACCESSORY PROTEIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SYNAPSES; SYNAPTIC POTENTIALS;

EID: 84942322924     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0882-x     Document Type: Article

References (33)

1. Anagnostaras SG, Gale GD, Fanselow MS (2001) Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11:8–17 doi:10.1002/1098-1063(2001) 11:1<8:AID-HIPO1015>3.0.CO;2-7
2. Baroncelli L, Braschi C, Spolidoro M et al (2011) Brain plasticity and disease: a matter of inhibition. Neural Plast 2011:1–11. doi:10.1155/2011/286073
3. Bienvenu TCM, Busti D, Magill PJ et al (2012) Cell-type-specific recruitment of amygdala interneurons to hippocampal theta rhythm and noxious stimuli in vivo. Neuron 74:1059–1074. doi:10.1016/j.neuron.2012.04.022
4. Carrié A, Jun L, Bienvenu T et al (1999) A new member of the IL-1 receptor family highly expressed in hippocampus and involved in X-linked mental retardation. Nat Genet 23:25–31. doi:10.1038/12623
5. Felix-Ortiz AC, Tye KM (2014) Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J Neurosci 34:586–595. doi:10.1523/JNEUROSCI.4257-13.2014
6. Felix-Ortiz AC, Beyeler A, Seo C et al (2013) BLA to vHPC inputs modulate anxiety-related behaviors. Neuron 79:658–664. doi:10.1016/j.neuron.2013.06.016
7. Gambino F, Pavlowsky A, Begle A et al (2007) IL1-receptor accessory protein-like 1 (IL1RAPL1), a protein involved in cognitive functions, regulates N-type Ca2+-channel and neurite elongation. Proc Natl Acad Sci 104:9063–9068. doi:10.1073/pnas.0701133104
8. Gatto CL, Broadie K (2010) Genetic controls balancing excitatory and inhibitory synaptogenesis in neurodevelopmental disorder models. Front Synaptic Neurosci 2:4. doi:10.3389/fnsyn.2010.00004
9. Goosens KA (2011) Hippocampal regulation of aversive memories. Curr Opin Neurobiol 21:460–466. doi:10.1016/j.conb.2011.04.003
10. Goshen I, Brodsky M, Prakash R et al (2011) Dynamics of retrieval strategies for remote memories. Cell 147:678–689. doi:10.1016/j.cell.2011.09.033
11. Hayashi T, Yoshida T, Ra M et al (2013) IL1RAPL1 associated with mental retardation and autism regulates the formation and stabilization of glutamatergic synapses of cortical neurons through RhoA signaling pathway. PLoS One 8:e66254. doi:10.1371/journal.pone.0066254.s002
12. Herry C, Mons N (2004) Resistance to extinction is associated with impaired immediate early gene induction in medial prefrontal cortex and amygdala. Eur J Neurosci 20:781–790. doi:10.1111/j.1460-9568.2004.03542.x
13. Houbaert X, Zhang CL, Gambino F et al (2013) Target-specific vulnerability of excitatory synapses leads to deficits in associative memory in a model of intellectual disorder. J Neurosci 33:13805–13819. doi:10.1523/JNEUROSCI.1457-13.2013
14. Hübner C, Bosch D, Gall A et al (2014) Ex vivo dissection of optogenetically activated mPFC and hippocampal inputs to neurons in the basolateral amygdala: implications for fear and emotional memory. Front Behav Neurosci 8:64. doi:10.3389/fnbeh.2014.00064
15. Knapska E, Macias M, Mikosz M et al (2012) Functional anatomy of neural circuits regulating fear and extinction. Proc Natl Acad Sci 109:17093–17098. doi:10.1073/pnas.1202087109
16. Kullmann DM, Moreau AW, Bakiri Y, Nicholson E (2012) Plasticity of inhibition. Neuron 75:951–962. doi:10.1016/j.neuron.2012.07.030
17. Ledoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184. doi:10.1146/annurev.neuro.23.1.155
18. Lisman JE, Coyle JT, Green RW et al (2008) Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 31:234–242. doi:10.1016/j.tins.2008.02.005
19. Liu X, Ramirez S, Pang PT et al (2012) Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484:381–385. doi:10.1038/nature11028
20. Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci. doi:10.1038/nrn3492
21. Morozov A, Sukato D, Ito W (2011) Selective suppression of plasticity in amygdala inputs from temporal association cortex by the external capsule. J Neurosci 31:339–345
22. Muller J, Corodimas KP, Fridel Z, Ledoux JE (1997) Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behav Neurosci 111:683–691
23. Orsini CA, Kim JH, Knapska E, Maren S (2011) Hippocampal and prefrontal projections to the basal amygdala mediate contextual regulation of fear after extinction. J Neurosci 31:17269–17277. doi:10.1523/JNEUROSCI.4095-11.2011
24. Pavlowsky A, Gianfelice A, Pallotto M et al (2010) A postsynaptic signaling pathway that may account for the cognitive defect due to IL1RAPL1 mutation. Curr Biol 20:103–115. doi:10.1016/j.cub.2009.12.030
25. Pavlowsky A, Chelly J, Billuart P (2011) Emerging major synaptic signaling pathways involved in intellectual disability. Mol Psychiatry. doi:10.1038/mp.2011.139
26. Pentkowski NS, Blanchard DC, Lever C et al (2006) Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur J Neurosci 23:2185–2196. doi:10.1111/j.1460-9568.2006.04754.x
27. Petreanu L, Huber D, Sobczyk A, Svoboda K (2007) Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci 10:663–668. doi:10.1038/nn1891
28. Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369–391
29. Piton A, Michaud JL, Peng H et al (2008) Mutations in the calcium-related gene IL1RAPL1 are associated with autism. Hum Mol Genet 17:3965–3974. doi:10.1093/hmg/ddn300
30. Rudy JW, Huff NC, Matus-Amat P (2004) Understanding contextual fear conditioning: insights from a two-process model. Neurosci Biobehav Rev 28:675–685. doi:10.1016/j.neubiorev.2004.09.004
31. Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83–88. doi:10.1126/science.1103944
32. Valnegri P, Montrasio C, Brambilla D et al (2011) The X-linked intellectual disability protein IL1RAPL1 regulates excitatory synapse formation by binding PTP and RhoGAP2. Hum Mol Genet 20:4797–4809. doi:10.1093/hmg/ddr418
33. Yoshida T, Yasumura M, Uemura T et al (2011) IL-1 receptor accessory protein-like 1 associated with mental retardation and autism mediates synapse formation by trans-synaptic interaction with protein tyrosine phosphatase. J Neurosci 31:13485–13499. doi:10.1523/JNEUROSCI.2136-11.2011