Stuttering Interneurons Generate Fast and Robust Inhibition onto Projection Neurons with Low Capacity of Short Term Modulation in Mouse Lateral Amygdala

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Song, Chen ^a   Xu, Xiao Bin ^a   He, Ye ^a   Liu, Zhi Peng ^a   Wang, Min ^a   Zhang, Xin ^a   Li, Bao Ming ^a   Pan, Bing Xing ^a  

^a NANCHANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACCOMMODATING INTERNEURON; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FAST SPIKING INTERNEURON; GABAERGIC TRANSMISSION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LATE SPIKING INTERNEURON; LATENT PERIOD; LATERAL AMYGDALA; MALE; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NERVE PROJECTION; NEUROMODULATION; NONHUMAN; PRESYNAPTIC INHIBITION; STUTTERING INTERNEURON; SYNAPSE VESICLE; UNITARY INHIBITORY POSTSYNAPTIC CURRENT;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; FLUORESCENCE; HISTOLOGICAL TECHNIQUES; INTERNEURONS; MALE; MICE; PATCH-CLAMP TECHNIQUES; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 84875100364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060154     Document Type: Article

References (45)

1. LeDoux J, Cicchetti P, Xagoraris A, Romanski L, (1990) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10: 1062-1069.
2. Schafe GE, Doyere V, LeDoux JE, (2005) Tracking the Fear Engram: The Lateral Amygdala Is an Essential Locus of Fear Memory Storage. J Neurosci 25: 10010-10014.
3. Davis M, Whalen P, (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6: 13-34.
4. Rumpel S, LeDoux J, Zador A, Malinow R, (2005) Postsynaptic Receptor Trafficking Underlying a Form of Associative Learning. Science 308: 83-88.
5. Tsvetkov E, Carlezon W, Benes F, Kandel E, Bolshakov V, (2002) Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron 34: 289-300.
6. Sah P, Westbrook R, Luthi A, (2008) Fear conditioning and long-term potentiation in the amygdala: what really is the connection? Ann N Y Acad Sci 1129: 88-95.
7. Heldt SA, Ressler KJ, (2010) Amygdala-Specific Reduction of {alpha}1-GABAA Receptors Disrupts the Anticonvulsant, Locomotor, and Sedative, But Not Anxiolytic, Effects of Benzodiazepines in Mice. J Neurosci 30: 7139-7151.
8. Pare D, Royer S, Smith Y, Lang E, (2003) Contextual inhibitory gating of impulse traffic in the intra-amygdaloid network. Ann N Y Acad Sci 985: 78-91.
9. Mahan A, Ressler K, (2012) Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci 35: 24-35.
10. Quirk G, Gehlert D, (2003) Inhibition of the amygdala: key to pathological states? Ann N Y Acad Sci 985: 263-272.
11. Spampanato J, Polepalli J, Sah P, (2011) Interneurons in the basolateral amygdala. Neuropharmacology 60: 765-773.
12. Davila J, Olmos L, Legaz I, Medina L, Guirado S, et al. (2008) Dynamic patterns of colocalization of calbindin, parvalbumin and GABA in subpopulations of mouse basolateral amygdalar cells during development. J Chem Neuroanat 35: 67-76.
13. McDonald A, Mascagni F, (2001) Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105: 681-693.
14. Mascagni F, McDonald A, (2003) Immunohistochemical characterization of cholecystokinin containing neurons in the rat basolateral amygdala. Brain Res 976: 171-184.
15. Woodruff AR, Sah P, (2007) Networks of Parvalbumin-Positive Interneurons in the Basolateral Amygdala. J Neurosci 27: 553-563.
16. Sosulina L, Graebenitz S, Pape H-C, (2010) GABAergic Interneurons in the Mouse Lateral Amygdala: A Classification Study. J Neurophysiol 104: 617-626.
17. Rainnie D, Mania I, Mascagni F, McDonald A, (2006) Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala. J Comp Neurol 498: 142-161.
18. Karube F, Kubota Y, Kawaguchi Y, (2004) Axon Branching and Synaptic Bouton Phenotypes in GABAergic Nonpyramidal Cell Subtypes. J Neurosci 24: 2853-2865.
19. Ma Y, Hu H, Agmon A, (2012) Short-Term Plasticity of Unitary Inhibitory-to-Inhibitory Synapses Depends on the Presynaptic Interneuron Subtype. J Neurosci 32: 983-988.
20. Gupta A, Wang Y, Markram H, (2000) Organizing Principles for a Diversity of GABAergic Interneurons and Synapses in the Neocortex. Science 287: 273-278.
21. Tamas G, Lorincz A, Simon A, Szabadics J, (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299: 1902-1905.
22. Tepper J, Tecuapetla F, Koos T, Ibanez-Sandoval O, (2010) Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4: 150.
23. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A, (2006) Distinct Subtypes of Somatostatin-Containing Neocortical Interneurons Revealed in Transgenic Mice. J Neurosci 26: 5069-5082.
24. Pan B, Dong Y, Ito W, Yanagawa Y, Shigemoto R, et al. (2009) Selective gating of glutamatergic inputs to excitatory neurons of amygdala by presynaptic GABAb receptor. Neuron 61: 917-929.
25. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, et al. (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467: 60-79.
26. Jasnow AM, Ressler KJ, Hammack SE, Chhatwal JP, Rainnie DG, (2009) Distinct Subtypes of Cholecystokinin (CCK)-Containing Interneurons of the Basolateral Amygdala Identified Using a CCK Promoter-Specific Lentivirus. J Neurophysiol 101: 1494-1506.
27. Paz R, Pelletier J, Bauer E, Pare D, (2006) Emotional enhancement of memory via amygdala-driven facilitation of rhinal interactions. Nat Neurosci 9: 1321-1329.
28. Soltesz I, Smetters DK, Mody I, (1995) Tonic inhibition originates from synapses close to the soma. Neuron 14: 1273-1283.
29. Staley KJ, Mody I, (1991) Integrity of perforant path fibers and the frequency of action potential independent excitatory and inhibitory synaptic events in dentate gyrus granule cells. Synapse 9: 219-224.
30. Hefft S, Jonas P, (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8: 1319-1328.
31. Connelly WM, Schulz JM, Lees G, Reynolds JN, (2010) Differential short-term plasticity at convergent inhibitory synapses to the substantia nigra pars reticulata. J Neurosci 30: 14854-14861.
32. Xiang Z, Huguenard JR, Prince DA, (2002) Synaptic inhibition of pyramidal cells evoked by different interneuronal subtypes in layer v of rat visual cortex. J Neurophysiol 88: 740-750.
33. Gupta A, Wang Y, Markram H, (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273-278.
34. Muller JF, Mascagni F, McDonald AJ, (2007) Postsynaptic targets of somatostatin-containing interneurons in the rat basolateral amygdala. J Comp Neurol 500: 513-529.
35. Defelipe J, Gonzalez-Albo M, Del Rio M, Elston G, (1999) Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J Comp Neurol 412: 515-526.
36. Yoshida T, Uchigashima M, Yamasaki M, Katona I, Yamazaki M, et al. (2011) Unique inhibitory synapse with particularly rich endocannabinoid signaling machinery on pyramidal neurons in basal amygdaloid nucleus. PNAS 108: 3059-3064.
37. Marowsky A, Rudolph U, Fritschy J-M, Arand M, (2012) Tonic Inhibition in Principal Cells of the Amygdala: A Central Role for {alpha}3 Subunit-Containing GABAA Receptors. J Neurosci 32: 8611-8619.
38. Fioravante D, Regehr WG, (2011) Short-term forms of presynaptic plasticity. Curr Opin Neurobiol 21: 269-274.
39. Zucker RS, Regehr WG, (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.
40. Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, et al. (2001) Distribution of CB1 Cannabinoid Receptors in the Amygdala and their Role in the Control of GABAergic Transmission. J Neurosci 21: 9506-9518.
41. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, et al. (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19: 4544-4558.
42. Marsicano G, Lutz B, (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11: 4213-4225.
43. Narushima M, Uchigashima M, Hashimoto K, Watanabe M, Kano M, (2006) Depolarization-induced suppression of inhibition mediated by endocannabinoids at synapses from fast-spiking interneurons to medium spiny neurons in the striatum. Eur J Neurosci 24: 2246-2252.
44. Koos T, Tepper JM, (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2: 467-472.
45. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, et al. (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279-285.