β-adrenergic receptors are differentially expressed in distinct interneuron subtypes in the rat hippocampus

Journal of Comparative Neurology

Volumn 509, Issue 6, 2008, Pages 551-565

  Cox, David J ^a   Racca, Claudia ^a   LeBeau, Fiona E N ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

adrenergic receptors; Hippocampus; Interneurons

Indexed keywords

BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR; BIOLOGICAL MARKER; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; CHOLECYSTOKININ; NEUROPEPTIDE; NEUROPEPTIDE Y; NORADRENALIN; PARVALBUMIN; SOMATOSTATIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; INTERNEURON; MALE; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ANIMALS; ANTIBODY SPECIFICITY; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CHOLECYSTOKININ; HIPPOCAMPUS; INTERNEURONS; MALE; PARVALBUMINS; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA-1; RECEPTORS, ADRENERGIC, BETA-2; SOMATOSTATIN;

EID: 48249136262     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21758     Document Type: Article

References (76)

1. Abramoff MD, Magelhaes PJ, Ram SJ, 2004 Image processing with ImageJ. Biophotonics Int 11:36-42.
2. Amaral DG, Witter MP. 1995. The hippocampal region. In: Paxinos G, editor: The rat nervous system. San Diego: Academic Press. p 443-493
3. Axmacher N, Mormann F, Fernandez G, Elger CE, Fell J. 2006. Memory formation by neuronal synchronization. Brain Res Rev 52:170-182.
4. Bassant MH, Simon A, Poindessous-Jazat F, Csaba Z, Epelbaum J, Dournaud P. 2005. Medial septal GABAergic neurons express the somatostatin sst2A receptor: functional consequences on unit firing and hippocampal theta. J Neurosci 25:2032-2041.
5. Bergles DE, Doze VA, Madison DV, Smith SJ. 1996. Excitatory actions of norepinephrine on multiple classes of hippocampal CA1 interneurons. J Neurosci 16:572-585.
6. Berridge CW, Foote SL. 1996. Enhancement of behavioral and electroencephalographic indices of waking following stimulation of noradrenergic beta-receptors within the medial septal region of the basal forebrain. J Neurosci 16:6999-7009.
7. Berridge CW, Waterhouse BD. 2003. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42:33-84.
8. Booze RM, Crisostomo EA, Davis JN. 1993. Beta-adrenergic receptors in the hippocampal and retrohippocampal regions of rats and guinea pigs: autoradiographic and immunohistochemical studies. Synapse 13:206-214.
9. Brown RA, Walling SG, Milway JS, Harley CW. 2005. Locus ceruleus activation suppresses feedforward interneurons and reduces beta-gamma electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus. J Neurosci 25:1985-1991.
10. Buhl EH, Halasy K, Somogyi P. 1994. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
11. Buzsaki G. 2002. Theta oscillations in the hippocampus. Neuron 33:325-340.
12. Celio MR. 1990. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
13. Cope DW, Maccaferri G, Marton LF, Roberts JD, Cobden PM, Somogyi P. 2002. Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurones target different domains of pyramidal cells in the CA1 area of the rat hippocampus. Neuroscience 109:63-80.
14. Driver JE, Racca C, Cunningham MO, Towers SK, Davies CH, Whittington MA, LeBeau FEN. 2007. Impairments in hippocampal (γ) gamma frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP). Eur J Neurosci 26:1280-1288.
15. Fell J, Fernandez G, Klaver P, Elger CE, Fries P. 2003. Is synchronized neuronal gamma activity relevant for selective attention? Brain Res Brain Res Rev 42:265-272.
16. Freund TF. 2003. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-495.
17. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6:347-470.
18. Freund TF, Katona I. 2007 Perisomatic inhibition. Neuron 56:33-42.
19. Frotscher M, Leranth C. 1988. Catecholaminergic innervation of pyramidal and GABAergic nonpyramidal neurons in the rat hippocampus. Double label immunostaining with antibodies against tyrosine hydroxylase and glutamate decarboxylase. Histochemistry 88:313-319.
20. Fuentes-Santamaria V, Alvarado JC, Taylor AR, Brunso-Bechtold JK, Henkel CK. 2005 Quantitative changes in calretinin immunostaining in the cochlear nuclei after unilateral cochlear removal in young ferrets. J Comp Neurol 483:458-475.
21. Gelinas JN, Nguyen PV. 2005 β-Adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J Neurosci 25:3294-3303.
22. Gillies MJ, Traub RD, LeBeau FE, Davies CH, Gloveli T, Buhl EH, Whittington MA. 2002. A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol 543:779-793.
23. Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD, Whittington MA, Buhl EH. 2005. Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol 562:131-147.
24. Grillner S, Markram H, De Schutter E, Silberberg G, LeBeau FE. 2005. Microcircuits in action - from CPGs to neocortex. Trends Neurosci 28:525-533.
25. Gu Q. 2002. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815-835.
26. Gulyas AI, Hajos N, Freund TF. 1996. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16:3397-3411.
27. Gulyas AI, Hajos N, Katona I, Freund T. 2003. Interneurons are the local targets of hippocampal inhibitory cells which project to the medial septum. Eur J Neurosci 17:1861-1872.
28. Guo NN, Li BM. 2007. Cellular and subcellular distributions of beta1- and beta2-adrenoceptors in the CA1 and CA3 regions of the rat hippocampus. Neuroscience 146:298-305.
29. Hajos N, Palhalmi J, Mann EO, Nemeth B, Paulsen O, Freund TF. 2004. Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J Neurosci 24:9127-9137.
30. Harrington AM, Hutson JM, Southwell BR. 2007 Immunohistochemical localisation of cholinergic muscarinic receptor subtype 1 (M1r) in the guinea pig and human enteric nervous system. J Chem Neuroanat 33:193-201
31. Harris KM, Marshall PE, Landis DM. 1985. Ultrastructural study of cholecystokinin-immunoreactive cells and processes in area CA1 of the rat hippocampus. J Comp Neurol 233:147-158.
32. Hillman KL, Doze VA, Porter JE. 2005a. Functional characterization of the beta-adrenergic receptor subtypes expressed by CA1 pyramidal cells in the rat hippocampus. J Pharmacol Exp Ther 314:561-567.
33. Hillman KL, Knudson CA, Carr PA, Doze VA, Porter JE. 2005b. Adrenergic receptor characterization of CA1 hippocampal neurons using real time single cell RT-PCR. Brain Res Mol Brain Res 139:267-276.
34. Hoogland TM, Saggau P. 2004. Facilitation of L-type Ca2+ channels in dendritic spines by activation of beta2 adrenergic receptors. J Neurosci 24:8416-8427.
35. Huang YY, Kandel ER. 1996. Modulation of both the early and the late phase of mossy fiber LTP by the activation of beta-adrenergic receptors. Neuron 16:611-617.
36. Jane-wit D, Altuntas CZ, Johnson JM, Yong S, Wickley PJ, Clark P, Wang Q, Popoviæ ZB, Penn MS, Damron DS, Perez DM, Tuohy VK. 2007. Beta 1-adrenergic receptor autoantibodies mediate dilated cardiomyopathy by agonistically inducing cardiomyocyte apoptosis. Circulation 116:399-410.
37. Jinno S, Kosaka T. 2006. Cellular architecture of the mouse hippocampus: a quantitative aspect of chemically defined GABAergic neurons with stereology. J Comp Neurol 56:229-245.
38. Jurgens CW, Rau KE, Knudson CA, King JD, Carr PA, Porter JE, Doze VA. 2005. Beta1 adrenergic receptor-mediated enhancement of hippocampal CA3 network activity. J Pharmacol Exp Ther 314:552-560.
39. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, Freund TF. 1999. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544-4558.
40. Katsuki H, Izumi Y, Zorumski CF. 1997. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J Neurophysiol 77:3013-3020.
41. Katsumaru H, Kosaka T, Heizmann CW, Hama K. 1988. Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72:347-362.
42. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsaki G, Somogyi P. 2003. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-848.
43. Klausberger T, Marton LF, Baude A, Roberts JD, Magill PJ, Somogyi P. 2004. Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7:41-47.
44. Kosaka T, Katsumaru H, Hama K, Wu JY, Heizmann CW. 1987. GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119-130.
45. Lagace DC, Whitman MC, Noonan MA, Ables JL, DeCarolis NA, Arguello AA, Donovan MH, Fischer SJ, Farnbauch LA, Beech RD, DiLeone RJ,Greer CA, Mandyam CD, Eisch AJ. 2007. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J Neurosci 27:12623-12629.
46. Lin YW, Min MY, Chiu TH, Yang HW. 2003. Enhancement of associative long-term potentiation by activation of beta-adrenergic receptors at CA1 synapses in rat hippocampal slices. J Neurosci 23:4173-4181.
47. Loy R, Koziell DA, Lindsey JD, Moore RY. 1980. Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189:699-710.
48. Maccaferri G, McBain CJ. 1996. The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497:119-130.
49. Matyas F, Freund TF, Gulyas AI. 2004. Convergence of excitatory and inhibitory inputs onto CCK-containing basket cells in the CA1 area of the rat hippocampus. Eur J Neurosci 19:1243-1256.
50. McBain CJ, Fisahn A. 2001. Interneurons unbound. Nat Rev Neurosci 2:11-23.
51. McDonald AJ, Mascagni F. 2001 Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing interneurons. Neuroscience 107:641-652.
52. Milner TA, Bacon CE. 1989. GABAergic neurons in the rat hippocampal formation: ultrastructure and synaptic relationships with catecholaminergic terminals. J Neurosci 9:3410-3427.
53. Milner TA, Shah P, Pierce JP. 2000. Beta-adrenergic receptors primarily are located on the dendrites of granule cells and interneurons but also are found on astrocytes and a few presynaptic profiles in the rat dentate gyrus. Synapse 36:178-193.
54. Morales M, Bloom FE. 1997. The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17:3157-3167.
55. Murchison CF, Zhang XY, Zhang WP, Ouyang M, Lee A, Thomas SA. 2004. A distinct role for norepinephrine in memory retrieval. Cell 117:131-143.
56. Nicholas AP, Pieribone VA, Hokfelt T. 1993. Cellular localization of messenger RNA for beta-1 and beta-2 adrenergic receptors in rat brain: an in situ hybridization study. Neuroscience 56:1023-1039.
57. Nicholas AP, Hokfelt T, Pieribone VA. 1996. The distribution and significance of CNS adrenoceptors examined with in situ hybridization. Trends Pharmacol Sci 17:245-255.
58. Nunzi MG, Gorio A, Milan F, Freund TF, Somogyi P, Smith AD. 1985. Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus. J Comp Neurol 237:485-505.
59. Nyiri G, Freund TF, Somogyi P. 2001. Input-dependent synaptic targeting of alpha(2)-subunit-containing GABA(A) receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci 13:428-442.
60. Oleskevich S, Descarries L, Lacaille JC. 1989. Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat. J Neurosci 9:3803-3815.
61. Parra P, Gulyas AI, Miles R. 1998. How many subtypes of inhibitory cells in the hippocampus? Neuron 20:983-993.
62. Pawelzik H, Hughes DI, Thomson AM. 2002. Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin- positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol 443:346-367.
63. Paxinos G, Watson C. 2007. The rat brain in stereotaxic coordinates, 6th ed. London: Academic Press.
64. Pitler TA, Alger BE. 1992. Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci 12:4122-4132.
65. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M. 2005. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25:6775-6786.
66. Rainbow TC, Parsons B, Wolfe BB. 1984. Quantitative autoradiography of beta 1- and beta 2-adrenergic receptors in rat brain. Proc Natl Acad Sci U S A 81:1585-1589.
67. Schroeter S, Apparsundaram S, Wiley RG, Miner LH, Sesack SR, Blakely RD. 2000. Immunolocalization of the cocaine- and antidepressant-sensitive 1-norepinephrine transporter. J Comp Neurol 420:211-232.
68. Sederberg PB, Schulze-Bonhage A, Madsen JR, Bromfield EB, McCarthy DC, Brandt A, Tully MS, Kahana MJ. 2007. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb Cortex 17:1190-1196.
69. Somogyi P, Klausberger T. 2005. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol 562:9-26.
70. Summers RJ, Papaioannou M, Harris S, Evans BA. 1995. Expression of beta 3-adrenoceptor mRNA in rat brain. Br J Pharmacol 116:2547-2548.
71. Thomas MJ, Moody TD, Makhinson M, O'Dell TJ. 1996. Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17:475-482.
72. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH. 1998. Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol 506:755-773.
73. Whittington MA, Traub RD. 2003. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676-682.
74. Wilson RI, Nicoll RA. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.
75. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER. 1999. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24:715-726.
76. Zsiros V, Maccaferri G. 2008 Noradrenergic modulation of electrical coupling in GABAergic networks of the hippocampus. J Neurosci 28:1804-1815.