Abstract
Olfactory receptor neurons of the nasal epithelium send their axons, via the olfactory nerve (ON), to the glomeruli of the olfactory bulb (OB), where the axon terminals form glutamatergic synapses with the apical dendrites of mitral and tufted cells, the output cells of the OB, and with juxtaglomerular (JG) interneurons. Many JG cells are GABAergic. Here we show that, despite the absence of conventional synapses, GABA released from JG cells activates GABABreceptors on ON terminals and inhibits glutamate release both tonically and in response to ON stimulation. Field potential recordings and current-source density analysis, as well as intracellular and whole cell recording techniques were used in rat OB slices. Baclofen (2–5 μM), a GABABagonist, completely suppressed ON-evoked synaptic responses of both mitral/tufted cells and JG cells, with no evidence for postsynaptic effects. Baclofen (0.5–1 μM) also reversed paired-pulse depression (PPD) of mitral/tufted cell responses to paired-pulse facilitation (PPF), and reduced depression of JG cell excitatory postsynaptic currents (EPSCs) during repetitive ON stimulation. These results suggest that baclofen reduced the probability of glutamate release from ON terminals. The GABABantagonists CGP35348 or CGP55845A increased mitral/tufted cell responses evoked by single-pulse ON stimulation, suggesting that glutamate release from ON terminals is tonically suppressed via GABABreceptors. The same antagonists reduced PPD of ON-evoked mitral/tufted cell responses at interstimulus intervals 50–400 ms. This finding suggests that a single ON impulse evokes sufficient GABA release, presumably from JG cells, to activate GABABreceptors on ON terminals. Thus GABABheteroreceptors on ON terminals are activated by ambient levels of extrasynaptic GABA, and by ON input to the OB. The time course of ON-evoked, GABABpresynaptic inhibition suggests that neurotransmission to M/T cells and JG cells will be significantly suppressed when ON impulses arrive in glomeruli at 2.5–20 Hz. GABABreceptor–mediated presynaptic inhibition of sensory input to the OB may play an important role in shaping the activation pattern of the OB glomeruli during olfactory coding.
References
74
Referenced
158
10.1016/S0306-4522(96)00706-3
10.1152/jn.1999.81.1.15
10.1152/jn.1999.82.1.489
{'issue': '11', 'key': 'B4', 'first-page': '129', 'volume': '55', 'author': 'Aroniadou-Anderjaska V', 'year': '1999', 'journal-title': 'Soc Neurosci Abstr'}
/ Soc Neurosci Abstr by Aroniadou-Anderjaska V (1999)10.1097/00001756-199607290-00033
10.1152/jn.1994.71.6.2557
10.1016/S0304-3940(99)00697-7
10.1016/0306-4522(87)90098-4
10.1016/0092-8674(91)90418-X
10.1146/annurev.ne.19.030196.002505
10.1002/(SICI)1096-9861(19971117)388:2<191::AID-CNE2>3.0.CO;2-X
10.1126/science.278.5337.463
10.1016/S0092-8674(94)90562-2
10.1016/0306-4522(90)90144-S
10.1074/jbc.273.41.26361
10.1113/jphysiol.1996.sp021204
10.1523/JNEUROSCI.16-05-01623.1996
10.1523/JNEUROSCI.17-23-09048.1997
10.1113/expphysiol.1995.sp003825
10.1016/0306-4522(95)00590-0
10.1097/00001756-199604100-00007
10.1152/jn.1975.38.2.369
10.1016/S0896-6273(00)80314-1
{'key': 'B26', 'first-page': '52', 'volume': '2', 'author': 'Frostl W', 'year': '1992', 'journal-title': 'Pharmacol Commun'}
/ Pharmacol Commun by Frostl W (1992)10.1002/cne.902660302
10.1073/pnas.90.8.3329
10.1016/0301-0082(79)90018-2
{'key': 'B30', 'first-page': '1268', 'volume': '500', 'author': 'Heyward PM', 'year': '1997', 'journal-title': 'Soc Neurosci Abstr'}
/ Soc Neurosci Abstr by Heyward PM (1997)10.1016/0006-8993(70)90263-5
10.1016/0896-6273(93)90308-E
10.1523/JNEUROSCI.17-03-01025.1997
10.1002/(SICI)1096-9861(19961223)376:4<557::AID-CNE5>3.0.CO;2-0
10.1002/(SICI)1096-9861(19980420)393:4<457::AID-CNE5>3.0.CO;2-#
10.1002/(SICI)1096-9861(19990503)407:2<261::AID-CNE7>3.0.CO;2-G
10.1038/25360
10.1523/JNEUROSCI.18-07-02602.1998
10.1016/0169-328X(94)90208-9
10.1152/jn.1996.76.2.1166
10.1037/h0028709
10.1016/S0306-4522(96)00308-9
10.1016/0006-8993(85)91172-2
10.1126/science.283.5398.74
10.1016/0006-8993(91)90985-5
10.1016/S0896-6273(00)80066-5
10.1126/science.175.4017.84
10.1152/jn.1993.70.4.1451
10.1002/(SICI)1096-9861(19990315)405:3<299::AID-CNE2>3.0.CO;2-6
10.1016/S0092-8674(00)81387-2
10.1016/S0074-7742(08)60304-9
10.1016/0304-3940(84)90517-2
10.1016/0361-9230(94)90091-4
10.1016/0014-2999(90)90337-6
10.1242/jcs.9.2.305
/ J Cell Sci by Pinching AJ (1971)10.1242/jcs.9.2.347
/ J Cell Sci by Pinching AJ (1971)10.1242/jcs.9.2.379
/ J Cell Sci by Pinching AJ (1971)10.1152/jn.1968.31.6.884
10.1016/0092-8674(94)90015-9
10.1016/0006-8993(77)90211-6
10.1016/0006-8993(77)90211-6
10.1016/0896-6273(92)90244-8
10.1016/0896-6273(94)90245-3
{'key': 'B65', 'first-page': '467', 'volume': '12', 'author': 'Shipley MT', 'year': '1996', 'journal-title': 'Handbook of Chemical Neuroanatomy. Integrated Systems of the CNS, Part III'}
/ Handbook of Chemical Neuroanatomy. Integrated Systems of the CNS, Part III by Shipley MT (1996)10.1523/JNEUROSCI.16-20-06374.1996
10.1002/cne.901850407
10.1523/JNEUROSCI.18-09-03138.1998
10.1152/jn.1993.70.6.2354
10.1016/0092-8674(94)90029-9
10.1523/JNEUROSCI.19-20-08808.1999
10.1163/156853964X00030
10.1038/25354
10.1016/S0166-2236(96)01015-6
10.1113/jphysiol.1995.sp020759
10.1113/jphysiol.1991.sp018798
10.1126/science.279.5348.237
Dates
Type | When |
---|---|
Created | 7 years, 8 months ago (Dec. 21, 2017, 9 a.m.) |
Deposited | 3 years ago (Aug. 10, 2022, 8:05 p.m.) |
Indexed | 3 weeks, 1 day ago (Aug. 7, 2025, 5:21 p.m.) |
Issued | 24 years, 11 months ago (Sept. 1, 2000) |
Published | 24 years, 11 months ago (Sept. 1, 2000) |
Published Print | 24 years, 11 months ago (Sept. 1, 2000) |
@article{Aroniadou_Anderjaska_2000, title={Tonic and Synaptically Evoked Presynaptic Inhibition of Sensory Input to the Rat Olfactory Bulb Via GABABHeteroreceptors}, volume={84}, ISSN={1522-1598}, url={http://dx.doi.org/10.1152/jn.2000.84.3.1194}, DOI={10.1152/jn.2000.84.3.1194}, number={3}, journal={Journal of Neurophysiology}, publisher={American Physiological Society}, author={Aroniadou-Anderjaska, Vassiliki and Zhou, Fu-Ming and Priest, Catherine A. and Ennis, Matthew and Shipley, Michael T.}, year={2000}, month=sep, pages={1194–1203} }