Muscarinic control of long-range GABAergic inhibition within the rhinal cortices
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The perirhinal cortex plays a critical role in memory formation, in part because it forms reciprocal connections with the neocortex and entorhinal cortex and is thus in a position to integrate and transfer higher-order information to and from the hippocampus. However, for reasons that remain unclear, perirhinal transfer of neocortical inputs to the entorhinal cortex occurs with a low probability. Using patch recordings in vitro and tract-tracing combined with GAD-67 immunohistochemistry, we show that the perirhinal cortex contains GABAergic neurons with long-range projections to superficial entorhinal cells. This finding challenges the traditional model of cortical inhibition in which all trans-areal inhibition is thought to be disynaptic because the axons of GABAergic interneurons are assumed to be confined within the area in which their somata are located. Moreover, consistent with recent studies indicating that the formation of perirhinal-dependent memories requires activation of muscarinic receptors, long-range IPSPs were presynaptically inhibited by M2 receptor activation. Overall, these results suggest that long-range feedforward inhibition regulates perirhinal transfer of neocortical inputs to the entorhinal cortex, but that cholinergic inputs can presynaptically adjust the impact of this control mechanism as a function of environmental contingencies.
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Projections from the perirhinal cortex to LEC and those from the postrhinal cortex to MEC are functionally different, with the former primarily sending inhibitory signals and the latter primarily sending excitatory ones.
“Projections from the perirhinal cortex to LEC and those from the postrhinal cortex to MEC are functionally different, with the former primarily sending inhibitory signals (Apergis-Schoute et al., 2007; Pinto et al., 2006; Willems et al., 2018) and the latter primarily sending excitatory ones (Koganezawa et al., 2015).”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Apergis-Schoute et al., 2007
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Short-Term Synaptic Plasticity
Zucker, R. S., & Regehr, W. G. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.092501.114547 · Cited by 5,068 · see citing works
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
The role of acetylcholine in learning and memory
Hasselmo, M. E. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.09.002 · Cited by 1,693 · see citing works
The role of calcium in neuromuscular facilitation
Katz, B., & Miledi, R. (1968) · The Journal of Physiology · doi:10.1113/jphysiol.1968.sp008469 · Cited by 1,347 · see citing works
Smith, Y., Bevan, M. D., Shink, É., & Bolam, J. P. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00004-9 · Cited by 948 · see citing works
Meunier, M., Bachevalier, J., Mishkin, M., & Murray, E. A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05418.1993 · Cited by 900 · see citing works
The entorhinal cortex of the monkey: II. Cortical afferents
Insausti, R., Amaral, D. G., & Cowan, W. M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902640306 · Cited by 835 · see citing works
Zola-Morgan, S. M., Squire, L., Amaral, D., & Suzuki, W. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04355.1989 · Cited by 766 · see citing works
Hoesen, G. W. V., Pandya, D. Ν., & Butters, N. (1975) · Brain Research · doi:10.1016/0006-8993(75)90205-x · Cited by 696 · see citing works
Presynaptic mechanism for long-term potentiation in the hippocampus
Bekkers, J. M., & Stevens, C. F. (1990) · Nature · doi:10.1038/346724a0 · Cited by 681 · see citing works
Manabe, T., Wyllie, D. J., Perkel, D. J., & Nicoll, R. A. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.4.1451 · Cited by 666 · see citing works
Suzuki, W., Zola-Morgan, S. M., Squire, L., & Amaral, D. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-06-02430.1993 · Cited by 543 · see citing works
The representation of stimulus familiarity in anterior inferior temporal cortex
Li, L., Miller, E. K., & Desimone, R. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.6.1918 · Cited by 539 · see citing works
Hoesen, G. W. V., & Pandya, D. Ν. (1975) · Brain Research · doi:10.1016/0006-8993(75)90204-8 · Cited by 499 · see citing works
The effects of hippocampal lesions upon spatial and non-spatial tests of working memory
Aggleton, J. P., Hunt, P. R., & Rawlins, J. N. P. (1986) · Behavioural Brain Research · doi:10.1016/0166-4328(86)90011-2 · Cited by 496 · see citing works
Wang, Y., Toledo‐Rodriguez, M., Gupta, A., Wu, C., Silberberg, G., Luo, J., & Markram, H. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.073353 · Cited by 491 · see citing works
Acetylcholine released from cerebral cortex in relation to state of activation
Celesia, G. G., & Jasper, H. H. (1966) · Neurology · doi:10.1212/wnl.16.11.1053 · Cited by 429 · see citing works
Acetylcholine Liberation from Cerebral Cortex during Paradoxical (REM) Sleep
Jasper, H. H., & Tessier, J. (1971) · Science · doi:10.1126/science.172.3983.601 · Cited by 427 · see citing works
Hersch, S. M., Gutekunst, C., Rees, H., Heilman, C. J., & Levey, A. I. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-03351.1994 · Cited by 404 · see citing works
Fahy, F. L., Riches, I. P., & Brown, M. W. (1993) · Experimental Brain Research · doi:10.1007/bf00234113 · Cited by 359 · see citing works
Paired‐pulse and frequency facilitation in the CA1 region of the in vitro rat hippocampus
Creager, R., Dunwiddie, T. V., & LYNCH, G. S. (1980) · The Journal of Physiology · doi:10.1113/jphysiol.1980.sp013133 · Cited by 345 · see citing works
Role of perirhinal cortex in object perception, memory, and associations
Murray, E. A., & Richmond, B. J. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00195-1 · Cited by 319 · see citing works
Dickson, C. T., Magistretti, J., Shalinsky, M. H., Fransén, E. A., Hasselmo, M. E., & Alonso, Á. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2562 · Cited by 317 · see citing works
Activity, modulation and role of basal forebrain cholinergic neurons innervating the cerebral cortex
Jones, B. E. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)45011-5 · Cited by 304 · see citing works
Miller, R. J. (1998) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.38.1.201 · Cited by 304 · see citing works
Gaffan, D., & Murray, E. A. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.30 · Cited by 265 · see citing works
Murray, E. A., & Mishkin, M. M. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-07-01991.1986 · Cited by 262 · see citing works
Any way you cut it: A new journal policy for the use of unbiased counting methods
Saper, C. B. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960101)364:1 · Cited by 226 · see citing works
Cholinergic Neurotransmission Is Essential for Perirhinal Cortical Plasticity and Recognition Memory
Warburton, E. C., Koder, T., Cho, K., Massey, P. V., Duguid, G., Barker, G. R. I., Aggleton, J. P., Bashir, Z. I., & Brown, M. W. (2003) · Neuron · doi:10.1016/s0896-6273(03)00358-1 · Cited by 226 · see citing works
Tamamaki, N., & Nojyo, Y. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903530306 · Cited by 225 · see citing works
Demonstration of long‐range GABAergic connections distributed throughout the mouse neocortex
Tomioka, R., Okamoto, K., Furuta, T., Fujiyama, F., Iwasato, T., Yanagawa, Y., Obata, K., Kaneko, T., & Tamamaki, N. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03989.x · Cited by 223 · see citing works
Gaffan, D., & Murray, E. A. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.1.30 · Cited by 217 · see citing works
Intracellular observations on the disinhibitory action of acetylcholine in the hippocampus
Ben‐Ari, Y., Krnjević, K., Reinhardt, W., & Ropert, N. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90093-2 · Cited by 215 · see citing works
Klink, R., & Alonso, A. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.1.144 · Cited by 211 · see citing works
Hájos, N., Papp, E., Acsády, L., Levey, A. I., & Freund, T. F. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00300-x · Cited by 210 · see citing works
Smith, Y., & Paré, D. (1994) · Journal of Comparative Neurology · doi:10.1002/cne.903420207 · Cited by 205 · see citing works
Self-citationInhibitory CA1-CA3-Hilar Region Feedback in the Hippocampus
Attila Gabor, S. I. K., Ylinen, A., Penttonen, M., & Buzsáki, G. (1994) · Science · doi:10.1126/science.8085161 · Cited by 197 · see citing works
Changes in Acetylcholine Extracellular Levels During Cognitive Processes: Table 1.Preprint
Pepeu, G., & Giovannini, M. G. (2004) · Learning & Memory · doi:10.1101/lm.68104 · Cited by 193 · see citing works
The rhinal cortices: a wall of inhibition between the neocortex and the hippocampus
DECURTIS, M., & Paré, D. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.08.005 · Cited by 185 · see citing works
Self-citationMurray, E. A., Baxter, M. G., & Gaffan, D. (1998) · Behavioral Neuroscience · doi:10.1037//0735-7044.112.6.1291 · Cited by 182 · see citing works
Meunier, M., Hadfield, W. S., Bachevalier, J., & Murray, E. A. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.3.1190 · Cited by 176 · see citing works
Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex
Leonard, B., Amaral, D., Squire, L., & Zola-Morgan, S. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05637.1995 · Cited by 174 · see citing works
Murray, E. A., Baxter, M. G., & Gaffan, D. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.6.1291 · Cited by 174 · see citing works
Ionic Mechanisms of Muscarinic Depolarization in Entorhinal Cortex Layer II Neurons
Klink, R., & Alonso, Á. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.4.1829 · Cited by 164 · see citing works
Paré, D., Smith, Y., & Paré, J.-F. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00272-k · Cited by 164 · see citing works
Self-citationFisher, R. S., Buchwald, N. A., Hull, C. D., & Levine, M. S. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902720404 · Cited by 161 · see citing works
Behrends, J. C., & ten Bruggencate, G. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.2.626 · Cited by 160 · see citing works
Winters, B. D., & Bussey, T. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04055.x · Cited by 141 · see citing works
Local synaptic connections of basal forebrain neurons
Záborszky, L., & Duque, A. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00255-2 · Cited by 135 · see citing works
Effects of muscarinic blockade in perirhinal cortex during visual recognition
Tang, Y., Mishkin, M., & Aigner, T. G. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12667 · Cited by 125 · see citing works
Nagahara, A. H., Otto, T., & Gallagher, M. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.1.3 · Cited by 118 · see citing works
Organization of long-range inhibitory connections with rat visual cortex
McDonald, C., & Burkhalter, A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-02-00768.1993 · Cited by 110 · see citing works
The effects of perirhinal cortical lesions on spatial reference memory in the rat
Wiig, K. A., & Bilkey, D. K. (1994) · Behavioural Brain Research · doi:10.1016/0166-4328(94)90055-8 · Cited by 110 · see citing works
Connections of the parahippocampal cortex in the cat. III. Cortical and thalamic efferents
Witter, M. P., & Groenewegen, H. J. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902520102 · Cited by 105 · see citing works
Sobótka, S., & Ringo, J. L. (1993) · Experimental Brain Research · doi:10.1007/bf00230436 · Cited by 104 · see citing works
McGaughy, J. A., Koene, R. A., Eichenbaum, H., & Hasselmo, M. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2386-05.2005 · Cited by 103 · see citing works
Kimura, F., & Baughman, R. W. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.2.709 · Cited by 102 · see citing works
Nagahara, A. H., Otto, T., & Gallagher, M. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.1.3 · Cited by 101 · see citing works
Ascending cholinergic pathways in the rat brain
Mesulam, B. H. W.-M. (1990) · doi:10.1093/oso/9780198542667.003.0002 · Cited by 98 · see citing works
Jones, R. S. G. (1994) · Hippocampus · doi:10.1002/hipo.450040317 · Cited by 97 · see citing works
Olfactory receptor neurons express D2 dopamine receptors
Koster, N. L., Norman, A. B., Richtand, N. M., Nickell, W. T., Puché, A. C., Pixley, S. K., & Shipley, M. T. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990906)411:4 · Cited by 95 · see citing works
Feedforward inhibition of the rat entorhinal cortex and subicular complex
Finch, D., Tan, A. M., & Isokawa-Akesson, M. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-07-02213.1988 · Cited by 95 · see citing works
Kajiwara, R., Takashima, I., Mimura, Y., Witter, M. P., & Iijima, T. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01033.2002 · Cited by 91 · see citing works
A Novel Type of GABAergic Interneuron Connecting the Input and the Output Regions of the Hippocampus
Ceranik, K., Bender, R., Geiger, J. R. P., Monyer, H., Jonas, P., Frotscher, M., & Lübke, J. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05380.1997 · Cited by 83 · see citing works
GABAergic Presubicular Projections to the Medial Entorhinal Cortex of the Rat
van Haeften, T., Wouterlood, F. G., Jorritsma‐Byham, B., & Witter, M. P. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-02-00862.1997 · Cited by 79 · see citing works
Effects of cholinergic deafferentation of the rhinal cortex on visual recognition memory in monkeys
Turchi, J. N., Saunders, R. C., & Mishkin, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409708102 · Cited by 70 · see citing works
Perirhinal N-methyl-d-aspartate and muscarinic systems participate in object recognition in rats
Abe, H., Ishida, Y., & Iwasaki, T. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2003.11.049 · Cited by 67 · see citing works
Shalinsky, M. H., Magistretti, J., Ma, L., & Alonso, A. A. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.3.1197 · Cited by 65 · see citing works
Muir, G. M., & Bilkey, D. K. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-04016.2001 · Cited by 64 · see citing works
Low-Probability Transmission of Neocortical and Entorhinal Impulses Through the Perirhinal Cortex
Pelletier, J. G., Apergis, J., & Paré, D. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01197.2003 · Cited by 62 · see citing works
Self-citationGABA-immunopositive neurons in rat neocortex with contralateral projections to S-I
Gonchar, Y., Johnson, P. B., & Weinberg, R. J. (1995) · Brain Research · doi:10.1016/0006-8993(95)00746-d · Cited by 59 · see citing works
Biella, G. R., Uva, L., & de Curtis, M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09972.2002 · Cited by 58 · see citing works
Pinto, A., Fuentes, C., & Paré, D. (2006) · Journal of Comparative Neurology · doi:10.1002/cne.20905 · Cited by 55 · see citing works
Self-citationBasic anatomy of the parahippocampal region in monkeys and rats
Burwell, R. D., & Witter, M. P. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198509172.003.0003 · Cited by 53 · see citing works
Propagation of Neocortical Inputs in the Perirhinal Cortex
Martina, M., Royer, S., & Paré, D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02878.2001 · Cited by 45 · see citing works
Self-citationFabri, M., & Manzoni, T. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00568-4 · Cited by 44 · see citing works
Murray, E. A., Graham, K. S., & Gaffan, D. (2005) · The Quarterly Journal of Experimental Psychology Section B · doi:10.1080/02724990544000077 · Cited by 41 · see citing works
Predominance of Late-Spiking Neurons in Layer VI of Rat Perirhinal Cortex
McGann, J. P., Moyer, J. R., & Brown, T. H. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-14-04969.2001 · Cited by 40 · see citing works
Funahashi, M., & Stewart, M. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01384-x · Cited by 37 · see citing works
Magistretti, J., Ma, L., Shalinsky, M. H., Lin, W., Klink, R., & Alonso, Á. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00036.2004 · Cited by 37 · see citing works
Symmetric synapses formed by callosal afferents in rat visual cortex
Hughes, C., & Peters, A. (1992) · Brain Research · doi:10.1016/s0006-8993(10)80033-2 · Cited by 34 · see citing works
Erişir, A., Levey, A. I., & Aoki, C. J. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1405 · Cited by 32 · see citing works
Perirhinal Cortex Muscarinic Receptor Blockade Impairs Taste Recognition Memory FormationPreprint
Gutiérrez, R., la Cruz, V. D., Rodríguez‐Ortiz, C. J., & Bermúdez‐Rattoni, F. (2004) · Learning & Memory · doi:10.1101/lm.69704 · Cited by 32 · see citing works
Cytoarchitectonic characterization of the parahippocampal region of the guinea pig
Uva, L., Grüschke, S., Biella, G. R., de Curtis, M., & Witter, M. P. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20121 · Cited by 27 · see citing works
Ino, T., Matsuzaki, S., Shinonaga, Y., Ohishi, H., Ogawa-Meguro, R., & Mizuno, N. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90448-i · Cited by 22 · see citing works
Differences in GABAergic transmission between two inputs into the perirhinal cortex
Garden, D. L. F., Kemp, N. M., & Bashir, Z. I. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02096.x · Cited by 16 · see citing works
Alonso, A. A. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198509172.003.0005 · Cited by 6 · see citing works
Fashena, D. (1999) · doi:10.1002/(sici)1096-9861(19990412)406:3
Flagged first, then by citations
Research works printed but not linked: 1
- Alonso A (2002) Electrophysiology of neurones in the perirhinal and ento- rhinal cortices and neuromodulatory changes in firing patterns. In: The parahippocampal region (Witter MP, Wouterlood F, eds), pp 89 -105. Oxford: Oxford UP.
Cited by
Sorted by citations
Neuronal Diversity in GABAergic Long-Range Projections from the Hippocampus
Jinno, S., Klausberger, T., Marton, L. F., Dalezios, Y., Roberts, J. D. B., Fuentealba, P., Bushong, E. A., Henze, D., Buzsáki, G., & Somogyi, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1847-07.2007 · Cited by 369 · see citing works
Long-range-projecting GABAergic neurons modulate inhibition in hippocampus and entorhinal cortex
Melzer, S., Michael, M., Caputi, A., Eliava, M., Fuchs, E. C., Whittington, M. A., & Monyer, H. (2012) · Science · doi:10.1126/science.1217139 · Cited by 333 · see citing works
McDonald, A. J., & Mott, D. D. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23709 · Cited by 172 · see citing works
The long and short of GABAergic neurons
Caputi, A., Melzer, S., Michael, M., & Monyer, H. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.021 · Cited by 167 · see citing works
Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.04.007 · Cited by 158 · see citing works
Long‐distance corticocortical GABAergic neurons in the adult monkey white and gray matter
Tomioka, R., & Rockland, K. S. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21504 · Cited by 144 · see citing works
Theta synchronizes the activity of medial prefrontal neurons during learningPreprint
Paz, R., Bauer, E. P., & Paré, D. (2008) · Learning & Memory · doi:10.1101/lm.932408 · Cited by 110 · see citing works
Self-citationBernice Porjesz, A., & Rangaswamy, M. (2007) · The Scientific World JOURNAL · doi:10.1100/tsw.2007.203 · Cited by 94 · see citing works
Specialized Cortical Subnetworks Differentially Connect Frontal Cortex to Parahippocampal Areas
Hirai, Y., Morishima, M., Karube, F., & Kawaguchi, Y. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2810-11.2012 · Cited by 73 · see citing works
Cortical Circuits of Callosal GABAergic Neurons
Rock, C., Zurita, H., Lebby, S., Wilson, C. J., & Apicella, A. J. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx025 · Cited by 70 · see citing works
Rangaswamy, M., & Bernice Porjesz, A. (2008) · Brain Research · doi:10.1016/j.brainres.2008.06.053 · Cited by 66 · see citing works
Effects of acetylcholine on neuronal properties in entorhinal cortex
Heys, J. G., Schultheiss, N. W., Shay, C. F., Tsuno, Y., & Hasselmo, M. E. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00032 · Cited by 56 · see citing works
GABAergic somatostatin-immunoreactive neurons in the amygdala project to the entorhinal cortex
McDonald, A. J., & Zaric, V. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.028 · Cited by 45 · see citing works
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Turesson, H., Rodríguez-Sierra, O. E., & Paré, D. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00004.2013 · Cited by 37 · see citing works
Self-citationDirect Interaction of GABABReceptors with M2Muscarinic Receptors Enhances Muscarinic Signaling
Boyer, S. B., Clancy, S. M., Terunuma, M., Revilla-Sanchez, R., Thomas, S. M., Moss, S. J., & Slesinger, P. A. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4103-09.2009 · Cited by 36 · see citing works
Popescu, A. T., & Paré, D. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00732.2010 · Cited by 35 · see citing works
Self-citationExcitatory Postrhinal Projections to Principal Cells in the Medial Entorhinal Cortex
Koganezawa, N., Gisetstad, R., Husby, E., Doan, T. P., & Witter, M. P. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0653-15.2015 · Cited by 34 · see citing works
Neuronal localization of M2 muscarinic receptor immunoreactivity in the rat amygdala
McDonald, A. J., & Mascagni, F. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.032 · Cited by 30 · see citing works
Perirhinal cortex and temporal lobe epilepsy
Biagini, G., D’Antuono, M., Benini, R., Guzman, P. D., Longo, D., & Avoli, M. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00130 · Cited by 27 · see citing works
Basu, K., Appukuttan, S., Manchanda, R., & Attila Gabor, S. I. K. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac329 · Cited by 28 · see citing works
Willems, J. G. P., Wadman, W. J., & Cappaert, N. L. M. (2018) · Hippocampus · doi:10.1002/hipo.22830 · Cited by 25 · see citing works
Muscarinic Receptors in Psychiatric Disorders – Can We Mimic ‘Health’?
Scarr, E. (2009) · Neurosignals · doi:10.1159/000231896 · Cited by 26 · see citing works
Kassab, R., & Alexandre, F. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00087 · Cited by 25 · see citing works
Extrinsic origins of the somatostatin and neuropeptide Y innervation of the rat basolateral amygdala
McDonald, A. J., & Zaric, V. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.03.004 · Cited by 23 · see citing works
Barinka, F., Salaj, M., Rybář, J., Krajčovičová, E., Kubová, H., & Druga, R. (2011) · Brain Research · doi:10.1016/j.brainres.2011.12.014 · Cited by 23 · see citing works
Ünal, G., Paré, J., Smith, Y., & Paré, D. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23297 · Cited by 18 · see citing works
Self-citationTanninen, S. E., Yu, X., Giritharan, T., Tran, L. M., Bakir, R., Volle, J., Morrissey, M. D., & Takehara‐Nishiuchi, K. (2015) · Hippocampus · doi:10.1002/hipo.22466 · Cited by 18 · see citing works
Maurer, A. P., Burke, S. N., Diba, K., & Barnes, C. A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0531-17.2017 · Cited by 17 · see citing works
Corticofugal VIP Gabaergic Projection Neurons in the Mouse Auditory and Motor Cortex
Bertero, A., Garcia, C., & Apicella, A. J. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.714780 · Cited by 15 · see citing works
Kajiwara, R., Tominaga, Y., & Tominaga, T. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00020 · Cited by 15 · see citing works
Neurophysiological maturation in adolescence – vulnerability and counteracting addiction to alcohol
Chwedorowicz, R., Skarżyńśki, H., Pucek, W., & Studziński, T. (2017) · Annals of Agricultural and Environmental Medicine · doi:10.5604/12321966.1234002 · Cited by 14 · see citing works
Biella, G. R., Spaiardi, P., Toselli, M., de Curtis, M., & Gnatkovsky, V. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00722.2009 · Cited by 14 · see citing works
Willems, J. G. P., Wadman, W. J., & Cappaert, N. L. M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00044 · Cited by 10 · see citing works
Fajardo‐Serrano, A., Liu, L., Mott, D. D., & McDonald, A. J. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.06.019 · Cited by 10 · see citing works
Calakos, K. C., Blackman, D. R., Schulz, A. M., & Bauer, E. P. (2016) · Synapse · doi:10.1002/syn.21953 · Cited by 9 · see citing works
Jhuang, Y.-C., & Chang, C. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac287 · Cited by 8 · see citing works
Kajiwara, R., & Tominaga, T. (2020) · BioEssays · doi:10.1002/bies.202000084 · Cited by 8 · see citing works
Dorman, R., Bos, J. J., Vinck, M. A., Marchesi, P., Fiorilli, J., Lorteije, J. A. M., Reiten, I., Bjaalie, J. G., Okun, M., & Pennartz, C. M. A. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad111 · Cited by 8 · see citing works
Molecular Genetic Strategies in the Study of Corticohippocampal CircuitsPreprint
Angelakos, C. C., & Abel, T. G. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021725 · Cited by 7 · see citing works
Endophenotypes in psychiatric genetics
Chen, A. C. H., Rangaswamy, M., & Porjesz, B. (2012) · Cambridge University Press eBooks · doi:10.1017/cbo9781139025997.030 · Cited by 4 · see citing works
Nilssen, E. S., Jacobsen, B., Doan, T. P., Girão, P. J., & Witter, M. P. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.29.518323 · Cited by 4 · see citing works
A computational model of perirhinal cortex: Gating and repair of input to the hippocampus
Lester, A. W., Howard, M. D., Fellous, J., & Bhattacharyya, R. (2013) · International Joint Conference on Neural Networks (IJCNN) · doi:10.1109/ijcnn.2013.6706901 · Cited by 1 · see citing works
NeuronalDiversityinGABAergicLong-RangeProjections fromtheHippocampus
DavidB, J. (2007) · Cited by 1 · see citing works
Encoding of Physical and Relational Information in the Lateral Entorhinal Cortex
Pilkiw, M. (2017) · TSpace (University of Toronto)
Tanninen, S. E. (2018) · TSpace (University of Toronto)
Nilssen, E. S., Jacobsen, B., Doan, T. P., Girão, P. J., & Witter, M. P. (2026) · eLife · doi:10.7554/elife.109082.2
- Authors
- Apergis-Schoute, J., Pinto, A., & Paré, D.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- ORCID
- Paré, Denis
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-04-11
- Volume
- 27
- Issue
- 15
- Pages
- 4061-4071
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6672538
- OpenAlex
- W2010288797
- Cited by
- 46
- References
- 86
- Citations by year
- 2026: 1 · 2023: 1 · 2022: 3 · 2021: 1 · 2020: 2 · 2019: 1 · 2018: 2 · 2017: 5 · 2016: 3 · 2015: 6 · 2013: 5 · 2012: 4
- FWCI
- 1.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0208712)
- National Institute of Mental Health (R01MH073610, MH073610)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- muscarinic receptors, M2 muscarinic receptor, perirhinal cortex, entorhinal cortex, GABAergic interneurons, long-range inhibition, feedforward inhibition, presynaptic inhibition, inhibitory postsynaptic potentials, cholinergic modulation, memory formation, hippocampus
- MeSH terms
- Animals, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Guinea Pigs, Isoenzymes, Nerve Net, Neural Inhibition, Entorhinal Cortex, 6-Cyano-7-nitroquinoxaline-2,3-dione, Excitatory Postsynaptic Potentials, Receptor, Muscarinic M2, Inhibitory Postsynaptic Potentials
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