Excitatory synapses on dendritic shafts of the caudal basal amygdala exhibit elevated levels of GABAA receptor α4 subunits following the induction of activity-based anorexia

Synapse

Volumn 68, Issue 1, 2014, Pages 1-15

  Wable, Gauri S ^a   Barbarich Marsteller, Nicole C ^b,c   Chowdhury, Tara G ^a   Sabaliauskas, Nicole A ^a   Farb, Claudia R ^a   Aoki, Chiye ^a  

^a NEW YORK UNIVERSITY   (United States)

^b College of Physicians and Surgeons of Columbia University ^*  (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Anorexia nervosa; Anxiety; Disinhibition; Exercise; Food restriction; Hyperactivity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA; ANOREXIA NERVOSA; ANXIETY; ARTICLE; BASAL AMYGDALA; BODY WEIGHT; BRAIN TISSUE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC SPINE; DIET RESTRICTION; EXCITATORY POSTSYNAPTIC POTENTIAL; EXCITATORY SYNAPSE; EXERCISE; FEMALE; FOOD INTAKE; GABAERGIC SYSTEM; HYPERACTIVITY; INTERNEURON; NERVE CELL EXCITABILITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STARVATION; SYNAPSE; WEIGHT REDUCTION;

ANOREXIA NERVOSA; ANXIETY; DISINHIBITION; EXERCISE; FOOD RESTRICTION; HYPERACTIVITY;

AMYGDALA; ANIMALS; ANOREXIA; DENDRITES; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GOLGI APPARATUS; MALE; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SYNAPSES;

EID: 84888051236     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.21690     Document Type: Article

References (71)

1. American Psychiatric Association. 2000. Diagnostic and statistical manual of mental disorders: DSM-IV-TR, American Psychiatric Publishing, Inc.
2. Adamec R, Hebert M, Blundell J, Mervis RF. 2012. Dendritic morphology of amygdala and hippocampal neurons in more and less predator stress responsive rats and more and less spontaneously anxious handled controls. Behav Brain Res 226:133-146.
3. Aigner M, Treasure J, Kaye W, Kasper S, Disorders WTF. 2011. World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for the pharmacological treatment of eating disorders. World J Biol Psychiatry 12:400-443.
4. Aoki C, Sabaliauskas N, Chowdhury T, Min JY, Colacino AR, Laurino K, Barbarich-Marsteller NC. 2012. Adolescent female rats exhibiting activity-based anorexia express elevated levels of GABA(A) receptor alpha4 and delta subunits at the plasma membrane of hippocampal CA1 spines. Synapse 66:391-407.
5. Bannai C, Kuzuya N, Koide Y, Fujita T, Itakura M, Kawai K, Yamashita K. 1988. Assessment of the relationship between serum thyroid hormone levels and peripheral metabolism in patients with anorexia nervosa. Endocrinol Jpn 35:455-462.
6. Bannerman D, Rawlins J, McHugh S, Deacon R, Yee B, Bast T, Zhang W-N, Pothuizen H, Feldon J. 2004. Regional dissociations within the hippocampus-Memory and anxiety. Neurosc Biobehav Rev 28:273-283.
7. Barbarich-Marsteller NC. 2012. Activity-based anorexia in the rat. In: Avena NM, editor. Animal models of eating disorders. New York: Humana Press. p 281-290.
8. Barbarich-Marsteller NC, Laurino K, Colacino AR. 2012. Pharmacological treatments for anorexia nervosa. In: Barbarich-Marsteller N, editor. Anorexia nervosa: Symptoms, treatment, and neurobiology. New York: Nova Science Publishers. p 97-117.
9. Barnard EA, Skolnick P, Olsen RW, Mohler H, Sieghart W, Biggio G, Braestrup C, Bateson AN, Langer SZ. 1998. International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: Classification on the basis of subunit structure and receptor function. Pharmacol Rev 50:291-313.
10. Benke D, Honer M, Michel C, Mohler H. 1996. GABAA receptor subtypes differentiated by their gamma-subunit variants: Prevalence, pharmacology and subunit architecture. Neuropharmacology 35:1413-1423.
11. Benke D, Michel C, Mohler H 1997. GABA(A) receptors containing the alpha4-subunit: Prevalence, distribution, pharmacology, and subunit architecture in situ. J Neurochem 69:806-814.
12. Birmingham CL, Su J, Hlynsky JA, Goldner EM, Gao M. 2005. The mortality rate from anorexia nervosa. Int J Eating Disord 38:143-146.
13. Brandys MK, Kas MJ, van Elburg AA, Campbell IC, Adan RA. 2011. A meta-analysis of circulating BDNF concentrations in anorexia nervosa. World J Biol Psychiatry 12:444-454.
14. Bulik CM, Slof-Op't Landt MC, van Furth EF, Sullivan PF. 2007. The genetics of anorexia nervosa. Annu Rev Nutr 27:263-275.
15. Carter AG, Soler-Llavina GJ, Sabatini BL. 2007. Timing and location of synaptic inputs determine modes of subthreshold integration in striatal medium spiny neurons. J Neurosci 27:8967-8977.
16. Epling WF, Pierce WD. 1996. Activity anorexia. Theory, research, and treatment. Mahwah: Lawrence Erlbaum Associates.
17. Epling WF, Pierce WD, Stefan L. 1983. A theory of activity-Based anorexia. Int J Eating Disord 3:27-46.
18. Farrant M, Nusser Z. 2005. Variations on an inhibitory theme: Phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6:215-229.
19. Franklin TB, Saab BJ, Mansuy IM. 2012. Neural mechanisms of stress resilience and vulnerability. Neuron 75:747-761.
20. Frick A, Magee JD. 2004. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7:126-135.
21. Fuller T, Russchen F, Price J. 1987. Sources of presumptive glutamergic/aspartergic afferents to the rat ventral striatopallidal region. J Comparative Neurol 258:317-338.
22. Gelegen C, van den Heuvel J, Collier DA, Campbell IC, Oppelaar H, Hessel E, Kas MJ. 2008. Dopaminergic and brain-derived neurotrophic factor signalling in inbred mice exposed to a restricted feeding schedule. Genes Brain Behav 7:552-559.
23. Golden NH, Shenker IR. 1992. Amenorrhrea in anorexia nervosa: Etiology and implications. Adolesc Med 3:503-518.
24. Golden NH, Shenker IR. 1994. Amenorrhea in anorexia nervosa. Neuroendocrine control of hypothalamic dysfunction. Int J Eating Disord 16:53-60.
25. Groenewegen HJ, Wright CI, Beijer AV, Voorn P. 1999. Convergence and segregation of ventral striatal inputs and outputs. Ann N Y Acad Sci 877:49-63.
26. Gulinello M, Orman R, Smith SS. 2003. Sex differences in anxiety, sensorimotor gating and expression of the alpha4 subunit of the GABAA receptor in the amygdala after progesterone withdrawal. Eur J Neurosci 17:641-648.
27. Hakansson ML, Brown H, Ghilardi N, Skoda RC, Meister B. 1998. Leptin receptor immunoreactivity in chemically defined target neurons of the hypothalamus. J Neurosci 18:559-572.
28. Hall JF, Hanford PV. 1954. Activity as a function of a restricted feeding schedule. J Comp Physiol Psychol 47:362-363.
29. Jiao Y, et al. 2011. A key mechanism underlying sensory experience-dependent maturation of neocortical GABAergic circuits in vivo. Proceedings of the National Academy of Sciences 108:12131-12136.
30. Jolkkonen E, Kemppainen S. 2000. Anatomic heterogeneity of the rat amygdaloid complex. Folia Morphol 59:1-0.
31. Joos AA, Saum B, van Elst LT, Perlov E, Glauche V, Hartmann A, Freyer T, Tuscher O, Zeeck A. 2011. Amygdala hyperreactivity in restrictive anorexia nervosa. Psychiatry Res 191:189-195.
32. Joshi S, Kapur J. 2009. Slow intracellular accumulation of GABA(A) receptor delta subunit is modulated by brain-derived neurotrophic factor. Neuroscience 164:507-519.
33. Kaye W. 2008 Neurobiology of anorexia and bulimia nervosa. Physiol Behav 94:121-135.
34. Kaye WH, Barbarich NC, Putnam K, Gendall KA, Fernstrom J, Fernstrom M, McConaha CW, Kishore A (2003) Anxiolytic effects of acute tryptophan depletion in anorexia nervosa. Int J Eating Disord 33:257-267; discussion 268-270.
35. Kaye WH, Bulik CM, Thornton L, Barbarich N, Masters K. 2004. Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am J Psychiatry 161:2215-2221.
36. Keating C, Tilbrook AJ, Rossell SL, Enticott PG, Fitzgerald PB. 2012. Reward processing in anorexia nervosa. Neuropsychologia 50:567-575.
37. Kelley AE, Swanson CJ. 1997. Feeding induced by blockade of AMPA and kainate receptors within the ventral striatum: A microinfusion mapping study. Behav Brain Res 89:107-113.
38. Kishi T, Tsumori T, Yokota S, Yasui Y. 2006. Topographical projection from the hippocampal formation to the amygdala: A combined anterograde and retrograde tracing study in the rat. J Comp Neurol 496:349-368.
39. Losonczy A, Makara JK, Magee JC. 2008. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452:436-441.
40. Maldonado-Irizarry CS, Swanson CJ, Kelley AE. 1995. Glutamate receptors in the nucleus accumbens shell control feeding behavior via the lateral hypothalamus. J Neurosci 15:6779-6788.
41. Mantzoros C, Flier JS, Lesem MD, Brewerton TD, Jimerson DC. 1997. Cerebrospinal fluid leptin in anorexia nervosa: Correlation with nutritional status and potential role in resistance to weight gain. J Clin Endocrinol Metab 82:1845-1851.
42. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
43. McDonald AJ. 1982. Neurons of the lateral and basolateral amygdaloid nuclei: A golgi study in the rat. J Comp Neurol 212:20.
44. McDonald AJ. 1996. Glutamate and aspartate immunoreactive neurons of the rat basolateral amygdala: Colocalization of excitatory amino acids and projections to the limbic circuit. J Comp Neurol 365:367-379.
45. McDonald AJ, Mascagni F, Mania I, Rainnie DG. 2005. Evidence for a perisomatic innervation of parvalbumin-containing interneurons by individual pyramidal cells in the basolateral amygdala. Brain Res 1035:32-40.
46. McDonald AJ, Muller JF, Mascagni F. 2002. GABAergic innervation of alpha type II calcium/calmodulin-dependent protein kinase immunoreactive pyramidal neurons in the rat basolateral amygdala. J Comp Neurol 446:199-218.
47. McHugh SB, Fillenz M, Lowry JP, Rawlins JN, Bannerman DM. 2011. Brain tissue oxygen amperometry in behaving rats demonstrates functional dissociation of dorsal and ventral hippocampus during spatial processing and anxiety. Eur J Neurosci 33:322-337.
48. Millhouse O, DeOlmos J. 1983. Neuronal configurations in lateral and basolateral amygdala. Neuroscience 10:1269-1300.
49. Mitra R, Sapolsky RM. 2008. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc Natl Acad Sci U S A 105:5573-5578.
50. Muller JF, Mascagni F, McDonald AJ. 2006. Pyramidal cells of the rat basolateral amygdala: Synaptology and innervation by parvalbumin-immunoreactive interneurons. J Comp Neurol 494:635-650.
51. Nakazato M, Hashimoto K, Shimizu E, Niitsu T, Iyo M. 2012. Possible involvement of brain-derived neurotrophic factor in eating disorders. IUBMB life 64:355-361.
52. Nedelescu H, Kelso CM, Lazaro-Munoz G, Purpura M, Cain CK, Ledoux JE, Aoki C. 2010. Endogenous GluR1-containing AMPA receptors translocate to asymmetric synapses in the lateral amygdala during the early phase of fear memory formation: an electron microscopic immunocytochemical study. J Comp Neurol 518:4723-4739.
53. O'Donnell JM, Shelton RC. 2010. Drug therapy of depression and anxiety disorders. In: Brunton LL, editors. Goodman and Gilman's the pharmacological basis of therapeutics. New York, USA: McGraw-Hill Professional. p 397-416.
54. Ono T, Luiten PG, Nishijo H, Fukuda M, Nishino H. 1985. Topographic organization of projections from the amygdala to the hypothalamus of the rat. Neurosci Res 2:221-238.
55. Paxinos G, Watson C. 2006. The rat brain in stereotaxic coordinates. San Diego, USA: Academic Press.
56. Powers PS, Bruty H. 2009. Pharmacotherapy for eating disorders and obesity. Child Adolesc Psychiatric Clin N Am 18:175-187.
57. Quirk GJ, Mueller D. 2008. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56-72.
58. Riddle MC, McKenna MC, Yoon YJ, Pattwell SS, Santos PM, Casey BJ, Glatt CE. 2013. Caloric restriction enhances fear extinction learning in mice. Neuropsychopharmacology 38:930-937.
59. Roberts DS, et al. 2006. Brain-derived neurotrophic factor (BDNF)-induced synthesis of early growth response factor 3 (Egr3) controls the levels of type A GABA receptor alpha 4 subunits in hippocampal neurons. J Biol Chem. 281:29431-29435.
60. Routtenberg A, Kuznesof AW. 1967. Self-starvation of rats living in activity wheels on a restricted feeding schedule. J Comp Physiol Psychol 64:414-421.
61. Sabaliauskas N, et al. 2012. Knockout of the γ-aminobutyric acid receptor subunit α4 reduces functional δ-containing extrasynaptic receptors in hippocampal pyramidal cells at the onset of puberty. Brain Res 1450:11-23.
62. Shen H, Gong QH, Aoki C, Yuan M, Ruderman Y, Dattilo M, Williams K, Smith SS. 2007. Reversal of neurosteroid effects at alpha4beta2delta GABAA receptors triggers anxiety at puberty. Nat Neurosci 10:469-477.
63. Shen H, Sabaliauskas N, Sherpa A, Fenton AA, Stelzer A, Aoki C, Smith SS. 2010. A critical role for alpha4betadelta GABAA receptors in shaping learning deficits at puberty in mice. Science 327:1515-1518.
64. Smith SS, Shen H, Gong QH, Zhou X. 2007. Neurosteroid regulation of GABA(A) receptors: Focus on the alpha4 and delta subunits. Pharmacol Ther 116:58-76.
65. Sullivan PF. 1995. Mortality in anorexia nervosa. Am J Psychiatry 152:1073-1074.
66. van der Plasse G, Schrama R, van Seters SP, Vanderschuren LJ, Westenberg HG. 2012. Deep brain stimulation reveals a dissociation of consummatory and motivated behaviour in the medial and lateral nucleus accumbens shell of the rat. PloS ONE 7:e33455.
67. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. 2002. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810-6818.
68. Vyas A, Pillai AG, Chattarji S. 2004. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128:667-673.
69. Woodson W, Farb CR, Ledoux JE. 2000. Afferents from the auditory thalamus synapse on inhibitory interneurons in the lateral nucleus of the amygdala. Synapse 38:124-137.
70. Wright CI, Beijer AV, Groenewegen HJ. 1996. Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J Neurosci 16:1877-1893.
71. Yuste R, Denk W. 1995. Dendritic spines as basic functional units of neuronal integration. Nature 375:682-684.