Divergent Routing of Positive and Negative Information from the Amygdala during Memory Retrieval

Neuron

Volumn 90, Issue 2, 2016, Pages 348-361

  Beyeler, Anna ^a   Namburi, Praneeth ^a   Glober, Gordon F ^a   Simonnet, Clémence ^a   Calhoon, Gwendolyn G ^a   Conyers, Garrett F ^a   Luck, Robert ^a   Wildes, Craig P ^a   Tye, Kay M ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATIVE MEMORY; AVERSION; BASOLATERAL AMYGDALA; BRAIN NERVE CELL; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; MALE; MEMORY; MEMORY RETRIEVAL; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PREDICTION; PRIORITY JOURNAL; REWARD; SYNAPSE; VENTRAL HIPPOCAMPUS; ANIMAL; ASSOCIATION; HIPPOCAMPUS; NERVE TRACT; PHYSIOLOGY; RECALL;

ANIMALS; BASOLATERAL NUCLEAR COMPLEX; CENTRAL AMYGDALOID NUCLEUS; CUES; HIPPOCAMPUS; MALE; MENTAL RECALL; MICE; NEURAL PATHWAYS; NUCLEUS ACCUMBENS;

EID: 84962086924     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.03.004     Document Type: Article

References (44)

1. Adhikari A. Distributed circuits underlying anxiety. Front. Behav. Neurosci. 2014, 8:112.
2. Allsop S.A., Vander Weele C.M., Wichmann R., Tye K.M. Optogenetic insights on the relationship between anxiety-related behaviors and social deficits. Front. Behav. Neurosci. 2014, 8:241.
3. Ambroggi F., Ishikawa A., Fields H.L., Nicola S.M. Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons. Neuron 2008, 59:648-661.
4. Amorapanth P., Nader K., LeDoux J.E. Lesions of periaqueductal gray dissociate-conditioned freezing from conditioned suppression behavior in rats. Learn. Mem. 1999, 6:491-499.
5. Ben-Ari Y., Tremblay E., Ottersen O.P. Injections of kainic acid into the amygdaloid complex of the rat: an electrographic, clinical and histological study in relation to the pathology of epilepsy. Neuroscience 1980, 5:515-528.
6. Berridge K.C., Robinson T.E. Parsing reward. Trends Neurosci. 2003, 26:507-513.
7. Bordi F., LeDoux J. Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum. J. Neurosci. 1992, 12:2493-2503.
8. Britt J.P., Benaliouad F., McDevitt R.A., Stuber G.D., Wise R.A., Bonci A. Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 2012, 76:790-803.
9. Calhoun M.E., Jucker M., Martin L.J., Thinakaran G., Price D.L., Mouton P.R. Comparative evaluation of synaptophysin-based methods for quantification of synapses. J. Neurocytol. 1996, 25:821-828.
10. Ciocchi S., Herry C., Grenier F., Wolff S.B.E., Letzkus J.J., Vlachos I., Ehrlich I., Sprengel R., Deisseroth K., Stadler M.B., et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 2010, 468:277-282.
11. Ciocchi S., Passecker J., Malagon-Vina H., Mikus N., Klausberger T. Brain computation. Selective information routing by ventral hippocampal CA1 projection neurons. Science 2015, 348:560-563.
12. Cohen J.Y., Haesler S., Vong L., Lowell B.B., Uchida N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 2012, 482:85-88.
13. Etkin A., Wager T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 2007, 164:1476-1488.
14. Etkin A., Prater K.E., Schatzberg A.F., Menon V., Greicius M.D. Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Arch. Gen. Psychiatry 2009, 66:1361-1372.
15. Felix-Ortiz A.C., Tye K.M. Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J. Neurosci. 2014, 34:586-595.
16. Felix-Ortiz A.C., Beyeler A., Seo C., Leppla C.A., Wildes C.P., Tye K.M. BLA to vHPC inputs modulate anxiety-related behaviors. Neuron 2013, 79:658-664.
17. Fontanini A., Grossman S.E., Figueroa J.A., Katz D.B. Distinct subtypes of basolateral amygdala taste neurons reflect palatability and reward. J. Neurosci. 2009, 29:2486-2495.
18. Fuster J.M., Uyeda A.A. Reactivity of limbic neurons of the monkey to appetitive and aversive signals. Electroencephalogr. Clin. Neurophysiol. 1971, 30:281-293.
19. Goosens K.A., Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn. Mem. 2001, 8:148-155.
20. Gore F., Schwartz E.C., Brangers B.C., Aladi S., Stujenske J.M., Likhtik E., Russo M.J., Gordon J.A., Salzman C.D., Axel R. Neural Representations of Unconditioned Stimuli in Basolateral Amygdala Mediate Innate and Learned Responses. Cell 2015, 162:134-145.
21. Janak P.H., Tye K.M. From circuits to behaviour in the amygdala. Nature 2015, 517:284-292.
22. Jennings J.H., Sparta D.R., Stamatakis A.M., Ung R.L., Pleil K.E., Kash T.L., Stuber G.D. Distinct extended amygdala circuits for divergent motivational states. Nature 2013, 496:224-228.
23. Jimenez S.A., Maren S. Nuclear disconnection within the amygdala reveals a direct pathway to fear. Learn. Mem. 2009, 16:766-768.
24. Lammel S., Tye K.M., Warden M.R. Progress in understanding mood disorders: optogenetic dissection of neural circuits. Genes Brain Behav. 2014, 13:38-51.
25. McDonald A.J. Neuronal organization of the lateral and basolateral amygdaloid nuclei in the rat. J. Comp. Neurol. 1984, 222:589-606.
26. McDonald A.J. Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 1998, 55:257-332.
27. Mervaala E., Föhr J., Könönen M., Valkonen-Korhonen M., Vainio P., Partanen K., Partanen J., Tiihonen J., Viinamäki H., Karjalainen A.K., Lehtonen J. Quantitative MRI of the hippocampus and amygdala in severe depression. Psychol. Med. 2000, 30:117-125.
28. Namburi P., Al-Hasani R., Calhoon G.G., Bruchas M.R., Tye K.M. Architectural representation of valence in the limbic system. Neuropsychopharmacology 2015, Published online December 9, 2015. 10.1038/npp.2015.358.
29. Namburi P., Beyeler A., Yorozu S., Calhoon G.G., Halbert S.A., Wichmann R., Holden S.S., Mertens K.L., Anahtar M., Felix-Ortiz A.C., et al. A circuit mechanism for differentiating positive and negative associations. Nature 2015, 520:675-678.
30. Nieh E.H., Kim S.-Y., Namburi P., Tye K.M. Optogenetic dissection of neural circuits underlying emotional valence and motivated behaviors. Brain Res. 2013, 1511:73-92.
31. Nieh E.H., Matthews G.A., Allsop S.A., Presbrey K.N., Leppla C.A., Wichmann R., Neve R., Wildes C.P., Tye K.M. Decoding neural circuits that control compulsive sucrose seeking. Cell 2015, 160:528-541.
32. Oh S.W., Harris J.A., Ng L., Winslow B., Cain N., Mihalas S., Wang Q., Lau C., Kuan L., Henry A.M., et al. A mesoscale connectome of the mouse brain. Nature 2014, 508:207-214.
33. Paton J.J., Belova M.A., Morrison S.E., Salzman C.D. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 2006, 439:865-870.
34. Pitkänen A. The Amygdala: A Functional Analysis 2000, Oxford University Press.
35. Senn V., Wolff S.B.E., Herry C., Grenier F., Ehrlich I., Gründemann J., Fadok J.P., Müller C., Letzkus J.J., Lüthi A. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 2014, 81:428-437.
36. Shabel S.J., Janak P.H. Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal. Proc. Natl. Acad. Sci. USA 2009, 106:15031-15036.
37. Shinonaga Y., Takada M., Mizuno N. Topographic organization of collateral projections from the basolateral amygdaloid nucleus to both the prefrontal cortex and nucleus accumbens in the rat. Neuroscience 1994, 58:389-397.
38. Somerville L.H., Kim H., Johnstone T., Alexander A.L., Whalen P.J. Human amygdala responses during presentation of happy and neutral faces: correlations with state anxiety. Biol. Psychiatry 2004, 55:897-903.
39. Stuber G.D., Sparta D.R., Stamatakis A.M., van Leeuwen W.A., Hardjoprajitno J.E., Cho S., Tye K.M., Kempadoo K.A., Zhang F., Deisseroth K., Bonci A. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 2011, 475:377-380.
40. Tye K.M., Stuber G.D., de Ridder B., Bonci A., Janak P.H. Rapid strengthening of thalamo-amygdala synapses mediates cue-reward learning. Nature 2008, 453:1253-1257.
41. Tye K.M., Prakash R., Kim S.-Y., Fenno L.E., Grosenick L., Zarabi H., Thompson K.R., Gradinaru V., Ramakrishnan C., Deisseroth K. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 2011, 471:358-362.
42. Tye K.M., Mirzabekov J.J., Warden M.R., Ferenczi E.A., Tsai H.-C., Finkelstein J., Kim S.-Y., Adhikari A., Thompson K.R., Andalman A.S., et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 2013, 493:537-541.
43. Zhang S.-J., Ye J., Miao C., Tsao A., Cerniauskas I., Ledergerber D., Moser M.-B., Moser E.I. Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 2013, 340:1232627.
44. Zhang W., Schneider D.M., Belova M.A., Morrison S.E., Paton J.J., Salzman C.D. Functional circuits and anatomical distribution of response properties in the primate amygdala. J. Neurosci. 2013, 33:722-733.