Parvalbumin interneurons constrain the size of the lateral amygdala engram

Neurobiology of Learning and Memory

Volumn 135, Issue , 2016, Pages 91-99

  Morrison, Dano J ^a,b   Rashid, Asim J ^a   Yiu, Adelaide P ^a,b   Yan, Chen ^a,b   Frankland, Paul W ^a,b,c   Josselyn, Sheena A ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Engram; Fear; Lateral amygdala; Memory; Parvalbumin; Sparse coding

Indexed keywords

PARVALBUMIN;

ADULT; ANIMAL EXPERIMENT; ARC GENE; ARTICLE; BRAIN SIZE; CELL COUNT; CONDITIONING; CONTROLLED STUDY; FEAR; FEMALE; GENE; GENE EXPRESSION; INTERNEURON; LATERAL AMYGDALA; MALE; MEMORY; MENTAL PERFORMANCE; MOUSE; NERVE CELL; NERVE EXCITABILITY; NONHUMAN; ANIMAL; ANIMAL BEHAVIOR; BASOLATERAL AMYGDALA; C57BL MOUSE; CONDITIONED REFLEX; CYTOLOGY; HEARING; METABOLISM; PHYSIOLOGY;

ANIMALS; AUDITORY PERCEPTION; BASOLATERAL NUCLEAR COMPLEX; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; FEAR; FEMALE; INTERNEURONS; MALE; MEMORY; MICE; MICE, INBRED C57BL; PARVALBUMINS;

EID: 84979515484     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2016.07.007     Document Type: Article

References (55)

1. Ahmad, S., & Hawkins, J. (2015). Properties of sparse distributed representations and their application to hierarchical temporal memory. ArXiv:150307469 Cs Q-Bio.
2. An, B., Hong, I., Choi, S., Long-term neural correlates of reversible fear learning in the lateral amygdala. Journal of Neuroscience 32 (2012), 16845–16856.
3. Armbruster, B.N., Li, X., Pausch, M.H., Herlitze, S., Roth, B.L., Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proceedings of the National Academy of Sciences USA 104 (2007), 5163–5168.
4. Barot, S.K., Kyono, Y., Clark, E.W., Bernstein, I.L., Visualizing stimulus convergence in amygdala neurons during associative learning. Proceedings of the National Academy of Sciences 105 (2008), 20959–20963.
5. Cowansage, K.K., Shuman, T., Dillingham, B.C., Chang, A., Golshani, P., Mayford, M., Direct reactivation of a coherent neocortical memory of context. Neuron 84 (2014), 432–441.
6. Druckmann, S., Chklovskii, D.B., Neuronal circuits underlying persistent representations despite time varying activity. Current Biology 22 (2012), 2095–2103.
7. Duan, W., Zhang, Y.-P., Hou, Z., Huang, C., Zhu, H., Zhang, C.-Q., Yin, Q., Novel insights into NeuN: From neuronal marker to splicing regulator. Molecular Neurobiology 53 (2016), 1637–1647.
8. Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., Lüthi, A., Amygdala inhibitory circuits and the control of fear memory. Neuron 62 (2009), 757–771.
9. Eichenbaum, H., Still searching for the engram. Learning & Behavior, 2016, 1–14, 10.3758/s13420-016-0218-1.
10. Fanselow, M.S., Bolles, R.C., Naloxone and shock-elicited freezing in the rat. Journal of Comparative and Physiological Psychology 93 (1979), 736–744.
11. Feng, F., Samarth, P., Paré D., Nair, S.S., Mechanisms underlying the formation of the amygdalar fear memory trace: A computational perspective. Neuroscience 322 (2016), 370–376.
12. Frankland, P.W., Josselyn, S.A., Anagnostaras, S.G., Kogan, J.H., Takahashi, E., Silva, A.J., Consolidation of CS and US representations in associative fear conditioning. Hippocampus 14 (2004), 557–569.
13. Freund, T.F., Katona, I., Perisomatic inhibition. Neuron 56 (2007), 33–42.
14. Ghosh, S., Chattarji, S., Neuronal encoding of the switch from specific to generalized fear. Nature Neuroscience 18 (2015), 112–120.
15. Gouty-Colomer, L.A., Hosseini, B., Marcelo, I.M., Schreiber, J., Slump, D.E., Yamaguchi, S., Kushner, S.A., Arc expression identifies the lateral amygdala fear memory trace. Molecular Psychiatry, 2015, 10.1038/mp.2015.18.
16. Gundersen, H.J., Jensen, E.B., The efficiency of systematic sampling in stereology and its prediction. Journal of Microscopy 147 (1987), 229–263.
17. Guzowski, J.F., Timlin, J.A., Roysam, B., McNaughton, B.L., Worley, P.F., Barnes, C.A., Mapping behaviorally relevant neural circuits with immediate-early gene expression. Current Opinion in Neurobiology 15 (2005), 599–606.
18. Han, J.-H., Kushner, S.A., Yiu, A.P., Cole, C.J., Matynia, A., Brown, R.A., Josselyn, S.A., Neuronal competition and selection during memory formation. Science 316 (2007), 457–460.
19. Han, J.-H., Kushner, S.A., Yiu, A.P., Hsiang, H.-L., Buch, T., Waisman, A., Josselyn, S.A., Selective erasure of a fear memory. Science 323 (2009), 1492–1496.
20. Herry, C., Ciocchi, S., Senn, V., Demmou, L., Müller, C., Lüthi, A., Switching on and off fear by distinct neuronal circuits. Nature 454 (2008), 600–606.
21. Hippenmeyer, S., Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D.R., Arber, S., A Developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biology, 3, 2005, e159.
22. Hromádka, T., DeWeese, M.R., Zador, A.M., Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biology, 6, 2008, e16.
23. Hsiang, H.-L., Epp, J.R., van den Oever, M.C., Yan, C., Rashid, A.J., Insel, N., Josselyn, S.A., Manipulating a “cocaine engram” in mice. The Journal of Neuroscience 34 (2014), 14115–14127.
24. Josselyn, S.A., Köhler, S., Frankland, P.W., Finding the engram. Nature Reviews Neuroscience 16 (2015), 521–534.
25. Kanerva, P., Sparse distributed memory. 1988, The MIT Press, Cambridge, Massachusetts.
26. Kim, J., Kwon, J.-T., Kim, H.-S., Josselyn, S.A., Han, J.-H., Memory recall and modifications by activating neurons with elevated CREB. Nature Neuroscience 17 (2013), 65–72.
27. Kim, D., Paré D., Nair, S.S., Assignment of model amygdala neurons to the fear memory trace depends on competitive synaptic interactions. Journal of Neuroscience 33 (2013), 14354–14358.
28. Kim, D., Samarth, P., Feng, F., Pare, D., Nair, S.S., Synaptic competition in the lateral amygdala and the stimulus specificity of conditioned fear: A biophysical modeling study. Brain Structure and Function 221:4 (2016), 2163–2182, 10.1007/s00429-015-1037-4.
29. Krashes, M.J., Koda, S., Ye, C., Rogan, S.C., Adams, A.C., Cusher, D.S., Lowell, B.B., Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. The Journal of Clinical Investigation 121 (2011), 1424–1428.
30. Krieg, D., Triesch, J., A unifying theory of synaptic long-term plasticity based on a sparse distribution of synaptic strength. Frontiers in Synaptic Neuroscience, 6, 2014, 3.
31. Lanuza, E., Moncho-Bogani, J., Ledoux, J.E., Unconditioned stimulus pathways to the amygdala: Effects of lesions of the posterior intralaminar thalamus on foot-shock-induced c-Fos expression in the subdivisions of the lateral amygdala. Neuroscience 155 (2008), 959–968.
32. Liu, X., Ramirez, S., Pang, P.T., Puryear, C.B., Govindarajan, A., Deisseroth, K., Tonegawa, S., Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484 (2012), 381–385.
33. Nichols, C.D., Roth, B., Engineered G-protein coupled receptors are powerful tools to investigate biological processes and behaviors. Frontiers in Molecular Neuroscience, 2, 2009, 16.
34. Paxinos, G., Franklin, K., The mouse brain in stereotaxic coordinates. 4th ed., 2012, Academic Press.
35. Quirk, G.J., Repa, J.C., LeDoux, J.E., Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: Parallel recordings in the freely behaving rat. Neuron 15 (1995), 1029–1039.
36. Reijmers, L.G., Perkins, B.L., Matsuo, N., Mayford, M., Localization of a stable neural correlate of associative memory. Science 317 (2007), 1230–1233.
37. Repa, J.C., Muller, J., Apergis, J., Desrochers, T.M., Zhou, Y., LeDoux, J.E., Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nature Neuroscience 4 (2001), 724–731.
38. Romanski, L.M., Clugnet, M.C., Bordi, F., LeDoux, J.E., Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behavioral Neuroscience 107 (1993), 444–450.
39. Rumpel, S., LeDoux, J., Zador, A., Malinow, R., Postsynaptic receptor trafficking underlying a form of associative learning. Science 308 (2005), 83–88.
40. Sah, P., Faber, E.S.L., Armentia, M.L.D., Power, J., The amygdaloid complex: anatomy and physiology. Physiological Reviews 83 (2003), 803–834.
41. Sanes, J.N., Donoghue, J.P., Plasticity and primary motor cortex. Annual Review of Neuroscience 23 (2000), 393–415.
42. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9 (2012), 671–675.
43. Silva, A.J., Kogan, J.H., Frankland, P.W., Kida, S., CREB and memory. Annual Review of Neuroscience 21 (1998), 127–148.
44. Spampanato, J., Polepalli, J., Sah, P., Interneurons in the basolateral amygdala. Neuropharmacology 60 (2011), 765–773.
45. Stefanelli, T., Bertollini, C., Lüscher, C., Muller, D., Mendez, P., Hippocampal Somatostatin Interneurons Control the Size of Neuronal Memory Ensembles. Neuron 89 (2016), 1074–1085.
46. Tanahira, C., Higo, S., Watanabe, K., Tomioka, R., Ebihara, S., Kaneko, T., Tamamaki, N., Parvalbumin neurons in the forebrain as revealed by parvalbumin-Cre transgenic mice. Neuroscience Research 63 (2009), 213–223.
47. Tayler, K.K., Tanaka, K.Z., Reijmers, L.G., Wiltgen, B.J., Reactivation of neural ensembles during the retrieval of recent and remote memory. Current Biology 23 (2013), 99–106.
48. Tonegawa, S., Liu, X., Ramirez, S., Redondo, R., Memory engram cells have come of age. Neuron 87 (2015), 918–931.
49. Tovote, P., Fadok, J.P., Lüthi, A., Neuronal circuits for fear and anxiety. Nature Reviews Neuroscience 16 (2015), 317–331.
50. Trouche, S., Sasaki, J.M., Tu, T., Reijmers, L.G., Fear extinction causes target-specific remodeling of perisomatic inhibitory synapses. Neuron 80 (2013), 1054–1065.
51. Weliky, M., Fiser, J., Hunt, R.H., Wagner, D.N., Coding of natural scenes in primary visual cortex. Neuron 37 (2003), 703–718.
52. Wixted, J.T., Squire, L.R., Jang, Y., Papesh, M.H., Goldinger, S.D., Kuhn, J.R., Steinmetz, P.N., Sparse and distributed coding of episodic memory in neurons of the human hippocampus. Proceedings of the National Academy of Sciences 111 (2014), 9621–9626.
53. Yiu, A.P., Mercaldo, V., Yan, C., Richards, B., Rashid, A.J., Hsiang, H.-L., Woodin, M.A., Neurons are recruited to a memory trace based on relative neuronal excitability immediately before training. Neuron 83 (2014), 722–735.
54. Zelikowsky, M., Hersman, S., Chawla, M.K., Barnes, C.A., Fanselow, M.S., Neuronal ensembles in amygdala, hippocampus, and prefrontal cortex track differential components of contextual fear. The Journal of Neuroscience 34 (2014), 8462–8466.
55. Zhou, Y., Won, J., Karlsson, M.G., Zhou, M., Rogerson, T., Balaji, J., Silva, A.J., CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nature Neuroscience 12 (2009), 1438–1443.