@article{MTMT:109314,
	title = {Interneuron diversity series: Rhythm and mood in perisomatic inhibition},
	url = {https://m2.mtmt.hu/api/publication/109314},
	author = {Freund, Tamás},
	doi = {10.1016/S0166-2236(03)00227-3},
	journal-iso = {TRENDS NEUROSCI},
	journal = {TRENDS IN NEUROSCIENCES},
	volume = {26},
	unique-id = {109314},
	issn = {0166-2236},
	year = {2003},
	eissn = {1878-108X},
	pages = {489-495}
}

@article{MTMT:109325,
	title = {Interneurons are the local targets of hippocampal inhibitory cells which project to the medial septum},
	url = {https://m2.mtmt.hu/api/publication/109325},
	author = {Gulyás, Attila and Hájos, Norbert and Katona, István and Freund, Tamás},
	doi = {10.1046/j.1460-9568.2003.02630.x},
	journal-iso = {EUR J NEUROSCI},
	journal = {EUROPEAN JOURNAL OF NEUROSCIENCE},
	volume = {17},
	unique-id = {109325},
	issn = {0953-816X},
	year = {2003},
	eissn = {1460-9568},
	pages = {1861-1872},
	orcid-numbers = {Gulyás, Attila/0000-0003-4961-636X}
}

@article{MTMT:2138091,
	title = {Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo.},
	url = {https://m2.mtmt.hu/api/publication/2138091},
	author = {Klausberger, T and Magill, PJ and Marton, LF and Roberts, JD and Cobden, PM and Buzsáki, György and Somogyi, Péter Pál},
	doi = {10.1038/nature01374},
	journal-iso = {NATURE},
	journal = {NATURE},
	volume = {421},
	unique-id = {2138091},
	issn = {0028-0836},
	abstract = {Neural-network oscillations at distinct frequencies have been implicated in the encoding, consolidation and retrieval of information in the hippocampus. Some GABA (gamma-aminobutyric acid)-containing interneurons fire phase-locked to theta oscillations (4-8 Hz) or to sharp-wave-associated ripple oscillations (120-200 Hz), which represent different behavioural states. Interneurons also entrain pyramidal cells in vitro. The large diversity of interneurons poses the question of whether they have specific roles in shaping distinct network activities in vivo. Here we report that three distinct interneuron types--basket, axo-axonic and oriens-lacunosum-moleculare cells--visualized and defined by synaptic connectivity as well as by neurochemical markers, contribute differentially to theta and ripple oscillations in anaesthetized rats. The firing patterns of individual cells of the same class are remarkably stereotyped and provide unique signatures for each class. We conclude that the diversity of interneurons, innervating distinct domains of pyramidal cells, emerged to coordinate the activity of pyramidal cells in a temporally distinct and brain-state-dependent manner.},
	keywords = {Animals; Male; RATS; Rats, Sprague-Dawley; Electrophysiology; Organ Specificity; Theta Rhythm/drug effects; gamma-Aminobutyric Acid/metabolism; *Anesthesia; Atropine/pharmacology; Pyramidal Cells/cytology/drug effects/physiology; Interneurons/*cytology/drug effects/*physiology; Hippocampus/*cytology/drug effects/*physiology; Consciousness/drug effects/physiology; Axons/drug effects/physiology; *Action Potentials/drug effects},
	year = {2003},
	eissn = {1476-4687},
	pages = {844-848}
}

@article{MTMT:109324,
	title = {Large variability in synaptic N-methyl-D-aspartate receptor density on interneurons and a comparison with pyramidal-cell spines in the rat hippocampus},
	url = {https://m2.mtmt.hu/api/publication/109324},
	author = {Nyíri, Gábor and Stephenson, FA and Freund, Tamás and Somogyi, Péter Pál},
	doi = {10.1016/S0306-4522(03)00157-X},
	journal-iso = {NEUROSCIENCE},
	journal = {NEUROSCIENCE},
	volume = {119},
	unique-id = {109324},
	issn = {0306-4522},
	year = {2003},
	eissn = {1873-7544},
	pages = {347-363}
}

@article{MTMT:2941543,
	title = {Postsynaptic effects of GABAergic synaptic diversity: regulation of neuronal excitability by changes in IPSC variance},
	url = {https://m2.mtmt.hu/api/publication/2941543},
	author = {Aradi, I and Santhakumar, V and Chen, K and Soltesz, Ivan},
	doi = {10.1016/S0028-3908(02)00167-3},
	journal-iso = {NEUROPHARMACOLOGY},
	journal = {NEUROPHARMACOLOGY},
	volume = {43},
	unique-id = {2941543},
	issn = {0028-3908},
	abstract = {GABAergic synaptic inputs to principal cells are heterogeneous in terms of their anatomical, molecular and physiological properties. Whether diversity in GABAergic synaptic inputs affects the efficacy of GABAergic inhibition is not understood. Here we show that alterations in the heterogeneity of IPSC populations arriving at single cells can significantly modify the effects of GABAergic inputs on neuronal excitability. The effects of IPSC diversity were examined in a computational model that incorporated experimentally measured values for spontaneous IPSCs and CA1 pyramidal cell electrophysiological properties. The simulations showed that increased variance in the conductance or decay of IPSCs could potently modulate the firing rate of the postsynaptic cells. The actual direction of the IPSC variance-induced modulation in postsynaptic cell discharges depended on the mean IPSC conductance and mean decay time constant around which the variance was introduced, as well as on the degree of depolarization and firing of the postsynaptic cell. Further analysis of the underlying mechanisms determined that these effects of IPSC variance on neuronal excitability were entirely predicted from the non-linear actions of IPSCs on action potential generation. The variance effects on neuronal excitability could be strong enough to overcome even large chances in mean IPSC conductance, demonstrating that increased mean synaptic conductance (or increased mean IPSC or IPSP) alone does not necessarily imply a more effective inhibition, a finding which has important implications for epilepsy research. These data show that the degree of heterogeneity of the GABAergic synaptic inputs to principal cells can powerfully modulate the efficacy of GABAergic inhibition. The results indicate the functional importance of the diversity of interneurons in cortical and hippocampal circuits, and suggest that plastic changes in GABAergic synaptic diversity may modulate neuronal excitability under both normal and pathological conditions. (C) 2002 Elsevier Science Ltd. All rights reserved.},
	keywords = {EPILEPSY; DIVERSITY; SYNAPSES; PLASTICITY; PYRAMIDAL CELLS; OSCILLATIONS; THETA-RHYTHM; RAT HIPPOCAMPUS; INHIBITORY INTERNEURONS; dentate gyrus; interneuron; FEBRILE SEIZURES; GRANULE CELLS; GABA(A); IPSC},
	year = {2002},
	eissn = {1873-7064},
	pages = {511-522}
}

@article{MTMT:109138,
	title = {Cell type dependence and variability in the short-term plasticity of EPSCs in identified mouse hippocampal interneurones},
	url = {https://m2.mtmt.hu/api/publication/109138},
	author = {Losonczy, Attila and Zhang, L and Shigemoto, R and Somogyi, Péter Pál and Nusser, Zoltán},
	doi = {10.1113/jphysiol.2002.020024},
	journal-iso = {J PHYSIOL-LONDON},
	journal = {JOURNAL OF PHYSIOLOGY-LONDON},
	volume = {542},
	unique-id = {109138},
	issn = {0022-3751},
	year = {2002},
	eissn = {1469-7793},
	pages = {193-210}
}

@article{MTMT:2941547,
	title = {Long-term plasticity in interneurons of the dentate gyrus},
	url = {https://m2.mtmt.hu/api/publication/2941547},
	author = {Ross, ST and Soltesz, Ivan},
	doi = {10.1073/pnas.141042398},
	journal-iso = {P NATL ACAD SCI USA},
	journal = {PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA},
	volume = {98},
	unique-id = {2941547},
	issn = {0027-8424},
	abstract = {Single interneurons influence thousands of postsynaptic principal cells, and the control of interneuronal excitability is an important regulator of the computational properties of the hippocampus. However, the mechanisms underlying long-term alterations in the input-output functions of interneurons are not fully understood. We report a mechanism of interneuronal plasticity that leads to the functional enhancement of the gain of glutamatergic inputs in the absence of long-term potentiation of the excitatory synaptic currents. Interneurons in the dentate gyrus exhibit a characteristic, limited (approximate to8 mV) depolarization of their resting membrane potential after high-frequency stimulation of the perforant path. The depolarization can be observed with either whole-cell or perforated patch electrodes, and it lasts in excess of 3 h. The long-term depolarization is specific to interneurons, because granule cells do not show it. The depolarization requires the activation of Ca2+-permeable alpha -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors and the rise of intracellular Ca2+, but not N-methyl-o-aspartate (NMDA) receptor activation. Data on the maintenance of the depolarization point to a major role for a long-term change in the rate of electrogenic Na+/K+-ATPase pump function in interneurons. As a result of the depolarization, interneurons after the tetanus respond with action potential discharges to previously subthreshold excitatory postsynaptic potentials (EPSPs), even though the EPSPs are not potentiated. These results demonstrate that the plastic nature of the interneuronal resting membrane potential underlies a unique form of long-term regulation of the gain of excitatory inputs to gamma -aminobutyric acid (CABA)ergic neurons.},
	keywords = {INHIBITION; glutamate; TEMPORAL-LOBE EPILEPSY; PUMP; DEPOLARIZATION; POTENTIATION; GRANULE CELLS; Pyramidal Neurons; hippocampal interneurons; INCREASED NUMBER},
	year = {2001},
	eissn = {1091-6490},
	pages = {8874-8879}
}

@article{MTMT:2138095,
	title = {Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro.},
	url = {https://m2.mtmt.hu/api/publication/2138095},
	author = {Maccaferri, G and Roberts, JD and Szűcs, Péter and Cottingham, CA and Somogyi, Péter Pál},
	doi = {10.1111/j.1469-7793.2000.t01-3-00091.x},
	journal-iso = {J PHYSIOL-LONDON},
	journal = {JOURNAL OF PHYSIOLOGY-LONDON},
	volume = {524},
	unique-id = {2138095},
	issn = {0022-3751},
	abstract = {1. Inhibitory postsynaptic currents (IPSCs) evoked in CA1 pyramidal cells (n = 46) by identified interneurones (n = 43) located in str. oriens were recorded in order to compare their functional properties and to determine the effect of synapse location on the apparent IPSC kinetics as recorded using somatic voltage clamp at -70 mV and nearly symmetrical [Cl-]. 2. Five types of visualised presynaptic interneurone, oriens-lacunosum moleculare (O-LMC), basket (BC), axo-axonic (AAC), bistratified (BiC) and oriens-bistratified (O-BiC) cells, were distinguished by immunocytochemistry and/or synapse location using light and electron microscopy. 3. Somatostatin immunoreactive O-LMCs, innervating the most distal dendritic shafts and spines, evoked the smallest amplitude (26 +/- 10 pA, s.e.m., n = 8) and slowest IPSCs (10-90 % rise time, 6.2 +/- 0.6 ms; decay, 20.8 +/- 1.7 ms, n = 8), with no paired-pulse modulation of the second IPSC (93 +/- 4 %) at 100 ms interspike interval. In contrast, parvalbumin-positive AACs evoked larger amplitude (308 +/- 103 pA, n = 7) and kinetically faster (rise time, 0.8 +/- 0.1 ms; decay 11.2 +/- 0.9 ms, n = 7) IPSCs showing paired-pulse depression (to 68 +/- 5 %, n = 6). Parvalbumin- or CCK-positive BCs (n = 9) terminating on soma/dendrites, BiCs (n = 4) and O-BiCs (n = 7) innervating dendrites evoked IPSCs with intermediate kinetic parameters. The properties of IPSCs and sensitivity to bicuculline indicated that they were mediated by GABAA receptors. 4. In three cases, kinetically complex, multiphasic IPSCs, evoked by an action potential in the recorded basket cells, suggested that coupled interneurones, possibly through electrotonic junctions, converged on the same postsynaptic neurone. 5. The population of O-BiCs (4 of 4 somatostatin positive) characterised in this study had horizontal dendrites restricted to str. oriens/alveus and innervated stratum radiatum and oriens. Other BiCs had radial dendrites as described earlier. The parameters of IPSCs evoked by BiCs and O-BiCs showed the largest cell to cell variation, and a single interneurone could evoke both small and slow as well as large and relatively fast IPSCs. 6. The kinetic properties of the somatically recorded postsynaptic current are correlated with the innervated cell surface domain. A significant correlation of rise and decay times for the overall population of unitary IPSCs suggests that electrotonic filtering of distal responses is a major factor for the location and cell type specific differences of unitary IPSCs, but molecular heterogeneity of postsynaptic GABAA receptors may also contribute to the observed kinetic differences. Furthermore, domain specific differences in the short-term plasticity of the postsynaptic response indicate a differentiation of interneurones in activity-dependent responses.},
	keywords = {Animals; RATS; KINETICS; Parvalbumins/analysis; Synaptic Transmission/*physiology; gamma-Aminobutyric Acid/*physiology; Rats, Wistar; Cell Membrane/physiology; Excitatory Postsynaptic Potentials/*physiology; Neurons/cytology/*physiology; Hippocampus/*physiology; Receptors, GABA-A/physiology; Patch-Clamp Techniques; Bicuculline/pharmacology; Synapses/*physiology/ultrastructure; Somatostatin/analysis; Axons/physiology/ultrastructure; Dendrites/physiology/ultrastructure; Cholecystokinin/pharmacology; Interneurons/cytology/physiology},
	year = {2000},
	eissn = {1469-7793},
	pages = {91-116},
	orcid-numbers = {Szűcs, Péter/0000-0003-4635-6427}
}

@article{MTMT:108723,
	title = {Changes in excitatory and inhibitory circuits of the rat hippocampus 12-14 months after complete forebrain ischemia},
	url = {https://m2.mtmt.hu/api/publication/108723},
	author = {Arabadzisz, Dimitrula and Freund, Tamás},
	doi = {10.1016/S0306-4522(98)00736-2},
	journal-iso = {NEUROSCIENCE},
	journal = {NEUROSCIENCE},
	volume = {92},
	unique-id = {108723},
	issn = {0306-4522},
	abstract = {Changes in interneuron distribution and excitatory connectivity have been investigated in animals which bad survived 12-14 months after complete forebrain ischemia, induced by four-vessel occlusion. Anterograde tracing with Phaseolus vulgaris leucoagglutinin revealed massive Schaffer collateral input even to those regions of the CA1 subfield where hardly any surviving pyramidal cells were found. Boutons of these Schaffer collaterals formed conventional synaptic contacts on dendritic spines and shafts, many of which likely belong to interneurons. Mossy fibres survived the ischemic challenge, however, large mossy terminals showed altered morphology, namely, the number of filopodiae on these terminals decreased significantly. The entorhinal input to the hippocampus did not show any morphological alterations. The distribution of interneurons was investigated by neurochemical markers known to label functionally distinct GABAergic cell populations. In the hilus, spiny interneurons showed a profound decrease in number. This phenomenon was not as obvious in CA3, but the spiny metabotropic glutamate receptor 1α- positive non-pyramidal cells, some of which contain calretinin or substance P receptor, disappeared from stratum lucidum of this area. In the CA1 region, somatostatin immunoreactivity disappeared from stratum oriens/lacunosum- moleculare-associated cells, while in metabotropic glutamate receptor 1α- stained sections these cells seemed unaffected in number. Other interneurons did not show an obvious decrease in number. In stratum radiatum of the CA1 subfield, some interneuron types had altered morphology: the substance P receptor-positive dendrites lost their characteristic radial orientation, and the metabotropic glutamate receptor 1α-expressing cells became extremely spiny. The loss of inhibitory interneurons at the first two stages of the trisynaptic loop coupled with a well-preserved excitatory connectivity among the subfields suggests that hyperexcitability in the surviving dentate gyms and CA3 may persist even a year after the ischemic impact. The dorsal CA1 region is lost; nevertheless hyperactivity, if it occurs, may have a route to leave the hippocampus via the longitudinally extensive axon collaterals of CA3 pyramidal cells, which may activate the subiculum and entorhinal cortex with a relay in the surviving ventral hippocampal CA1 region.},
	keywords = {Animals; Male; Male; INHIBITION; immunohistochemistry; CALCIUM-BINDING PROTEINS; neuropeptides; SOMATOSTATIN; ISCHEMIA; hippocampus; hippocampus; hippocampus; RATS; EPILEPSY; ARTICLE; Neural Pathways; priority journal; controlled study; Time Factors; nonhuman; animal tissue; animal model; animal experiment; brain ischemia; brain ischemia; Neural Inhibition; PYRAMIDAL CELLS; ENTORHINAL CORTEX; synaptic transmission; dentate gyrus; Rats, Wistar; nerve projection; Reference Values; substance P receptor; Cell Death; neuromodulation; pyramidal nerve cell; interneuron; Perforant Pathway; nerve cell excitability; Mossy Fibers, Hippocampal; metabotropic receptor; subiculum; rat; interneurons},
	year = {1999},
	eissn = {1873-7544},
	pages = {27-45}
}

@article{MTMT:108862,
	title = {Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus},
	url = {https://m2.mtmt.hu/api/publication/108862},
	author = {Gulyás, Attila and Megías, M and Emri, Zsuzsa and Freund, Tamás},
	doi = {10.1523/jneurosci.19-22-10082.1999},
	journal-iso = {J NEUROSCI},
	journal = {JOURNAL OF NEUROSCIENCE},
	volume = {19},
	unique-id = {108862},
	issn = {0270-6474},
	year = {1999},
	eissn = {1529-2401},
	pages = {10082-10097},
	orcid-numbers = {Gulyás, Attila/0000-0003-4961-636X}
}

@article{MTMT:108648,
	title = {Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus},
	url = {https://m2.mtmt.hu/api/publication/108648},
	author = {Katona, István and Acsády, László and Freund, Tamás},
	doi = {10.1016/S0306-4522(98)00302-9},
	journal-iso = {NEUROSCIENCE},
	journal = {NEUROSCIENCE},
	volume = {88},
	unique-id = {108648},
	issn = {0306-4522},
	year = {1999},
	eissn = {1873-7544},
	pages = {37-55}
}

@article{MTMT:2966610,
	title = {The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation.},
	url = {https://m2.mtmt.hu/api/publication/2966610},
	author = {Rivera, C and Voipio, J and Payne, JA and Ruusuvuori, E and Lahtinen, H and Lamsa, Karri and Pirvola, U and Saarma, M and Kaila, K},
	doi = {10.1038/16697},
	journal-iso = {NATURE},
	journal = {NATURE},
	volume = {397},
	unique-id = {2966610},
	issn = {0028-0836},
	abstract = {GABA (gamma-aminobutyric acid) is the main inhibitory transmitter in the adult brain, and it exerts its fast hyperpolarizing effect through activation of anion (predominantly Cl-)-permeant GABA(A) receptors. However, during early neuronal development, GABA(A)-receptor-mediated responses are often depolarizing, which may be a key factor in the control of several Ca2+-dependent developmental phenomena, including neuronal proliferation, migration and targeting. To date, however, the molecular mechanism underlying this shift in neuronal electrophysiological phenotype is unknown. Here we show that, in pyramidal neurons of the rat hippocampus, the ontogenetic change in GABA(A)-mediated responses from depolarizing to hyperpolarizing is coupled to a developmental induction of the expression of the neuronal (Cl-)-extruding K+/Cl- co-transporter, KCC2. Antisense oligonucleotide inhibition of KCC2 expression produces a marked positive shift in the reversal potential of GABAA responses in functionally mature hippocampal pyramidal neurons. These data support the conclusion that KCC2 is the main Cl- extruder to promote fast hyperpolarizing postsynaptic inhibition in the brain.},
	keywords = {Animals; RATS; Guinea Pigs; Electrophysiology; gamma-Aminobutyric Acid/*physiology; Cell Differentiation; RNA, Messenger/analysis; Gene Expression Regulation, Developmental; reverse transcriptase polymerase chain reaction; Potassium/metabolism; Blotting, Southern; Chlorides/metabolism; GABA Agonists/pharmacology; Muscimol/pharmacology; *Symporters; In Vitro Techniques; Pyramidal Cells/cytology/drug effects/*physiology; Hippocampus/cytology/embryology/metabolism; Carrier Proteins/biosynthesis/genetics/*physiology},
	year = {1999},
	eissn = {1476-4687},
	pages = {251-255},
	orcid-numbers = {Lamsa, Karri/0000-0002-4609-1337}
}

@article{MTMT:108447,
	title = {How many subtypes of inhibitory cells in the hippocampus?},
	url = {https://m2.mtmt.hu/api/publication/108447},
	author = {Parra, P and Gulyás, Attila and Miles, R},
	doi = {10.1016/S0896-6273(00)80479-1},
	journal-iso = {NEURON},
	journal = {NEURON},
	volume = {20},
	unique-id = {108447},
	issn = {0896-6273},
	year = {1998},
	eissn = {1097-4199},
	pages = {983-993},
	orcid-numbers = {Gulyás, Attila/0000-0003-4961-636X}
}

@article{MTMT:2138098,
	title = {Target-cell-specific facilitation and depression in neocortical circuits.},
	url = {https://m2.mtmt.hu/api/publication/2138098},
	author = {Reyes, A and Lujan, R and Rozov, A and Burnashev, N and Somogyi, Péter Pál and Sakmann, B},
	journal-iso = {NAT NEUROSCI},
	journal = {NATURE NEUROSCIENCE},
	volume = {1},
	unique-id = {2138098},
	issn = {1097-6256},
	abstract = {In neocortical circuits, repetitively active neurons evoke unitary postsynaptic potentials (PSPs) whose peak amplitudes either increase (facilitate) or decrease (depress) progressively. To examine the basis for these different synaptic responses, we made simultaneous recordings from three classes of neurons in cortical layer 2/3. We induced repetitive action potentials in pyramidal cells and recorded the evoked unitary excitatory (E)PSPs in two classes of GABAergic neurons. We observed facilitation of EPSPs in bitufted GABAergic interneurons, many of which expressed somatostatin immunoreactivity. EPSPs recorded from multipolar interneurons, however, showed depression. Some of these neurons were immunopositive for parvalbumin. Unitary inhibitory (I)PSPs evoked by repetitive stimulation of a bitufted neuron also showed a less pronounced but significant difference between the two target neurons. Facilitation and depression involve presynaptic mechanisms, and because a single neuron can express both behaviors simultaneously, we infer that local differences in the molecular structure of presynaptic nerve terminals are induced by retrograde signals from different classes of target neurons. Because bitufted and multipolar neurons both formed reciprocal inhibitory connections with pyramidal cells, the results imply that the balance of activation between two recurrent inhibitory pathways in the neocortex depends on the frequency of action potentials in pyramidal cells.},
	keywords = {Animals; RATS; Excitatory Postsynaptic Potentials/physiology; Pyramidal Cells/physiology; Electric Stimulation; Neural Pathways/cytology/physiology; Action Potentials/physiology; Synapses/physiology; Electrophysiology; Neural Inhibition/physiology; gamma-Aminobutyric Acid/physiology; Neocortex/cytology/*physiology; Neurons/physiology; Somatostatin/metabolism; Interneurons/metabolism/physiology},
	year = {1998},
	eissn = {1546-1726},
	pages = {279-285}
}

@article{MTMT:1661006,
	title = {Unitary IPSPs evoked by interneurons at the stratum radiatum stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro},
	url = {https://m2.mtmt.hu/api/publication/1661006},
	author = {Vida, I and Halasy, Katalin and Szinyei, C and Somogyi, Péter Pál and Buhl, EH},
	doi = {10.1111/j.1469-7793.1998.755bv.x},
	journal-iso = {J PHYSIOL-LONDON},
	journal = {JOURNAL OF PHYSIOLOGY-LONDON},
	volume = {506},
	unique-id = {1661006},
	issn = {0022-3751},
	abstract = {1. Hippocampal non-principal neurons at the stratum radiatum-stratum lacunosum-moleculare border (R-LM interneurons) of the CA1 area may constitute several cell classes and have been implicated in the generation of GABAergic unitary IPSPs. Using biocytin filled electrodes we recorded R-LM interneurons intracellularly in vitro and determined their postsynaptic effects in concomitantly recorded pyramidal cells. 2. Light microscopic analysis revealed four populations of R-LM interneurons with distinct axons: (1) basket cells (n = 4) with axons predominantly ramifying in the pyramidal cell layer; (2) Schaffer collateral/commissural pathway-associated interneurons (n = 10) stratifying in stratum radiatum and, to a lesser extent, stratum oriens; (3) perforant pathway-associated interneurons (n = 6) innervating the perforant path termination zone in stratum lacunosum-moleculare of the CA1 area as well as equivalent portions of the dentate gyrus and subiculum; and (4) neurogliaform interneurons (n = 2) characterized by their dense, compact axonal and dendritic arbour. 3. Random electron microscopic sampling of synaptic targets revealed a preponderance of pyramidal neurons as postsynaptic elements. Basket cells had a synaptic target preference for somata and proximal dendrites, whereas the remainder of R-LM interneurons innervated dendritic shafts and spines. The axon of dendrite-targeting cells formed up to six putative contacts with individual postsynaptic pyramidal cells. 4. Anatomically recovered R-LM interneurons (n = 22) had a mean resting membrane potential of -56.7 +/- 3.6 mV, a membrane time constant of 12.9 +/- 7.7 ms and an input resistance of 86.4 +/- 29.2 M Ohm. Depolarizing current pulses generally elicited overshooting action potentials (70.8 +/- 6.9 mV) which had a mean duration, when measured at half-amplitude, of 0.7 +/- 0.1 ms. In response to prolonged (> 200 ms) depolarizing current pulses all R-LM interneurons displayed (a varying degree of) spike frequency adaptation. 5. Basket cells, Schaffer-associated and neurogliaform interneurons elicited small-amplitude (< 2 mV), short-latency IPSPs in postsynaptic pyramids (n = 5, 13 and 1, respectively). Those interactions in which an effect was elicited with the repetitive activation of the presynaptic neuron (n = 13) showed a substantial degree of postsynaptic response summation. Unitary IPSPs had fast kinetics and, whenever tested (n = 5; 1 basket cell and 4 Schaffer-associated interneurons), were abolished by the GABA(A) receptor antagonist bicuculline. 6. Thus, R-LM interneurons comprise several distinct populations which evoke fast GABA(A) receptor-mediated IPSPs. The domain-specific innervation of postsynaptic pyramidal cells suggests functionally diverse effects on the integration of afferent information in functionally non-equivalent compartments of pyramidal cells.},
	keywords = {Animals; RATS; Electric Stimulation; Microscopy, Electron; Interneurons/*physiology/ultrastructure; Synapses/physiology/ultrastructure; Action Potentials/physiology; Electrophysiology; Rats, Wistar; Excitatory Postsynaptic Potentials/*physiology; Patch-Clamp Techniques; Membrane Potentials/physiology; Axons/physiology/ultrastructure; Hippocampus/cytology/*physiology/ultrastructure; Neuroglia/physiology/ultrastructure},
	year = {1998},
	eissn = {1469-7793},
	pages = {755-773}
}

@article{MTMT:108671,
	title = {Synaptic communication among hippocampal interneurons: Properties of spontaneous IPSCs in morphologically identified cells},
	url = {https://m2.mtmt.hu/api/publication/108671},
	author = {Hájos, Norbert and Mody, I},
	doi = {10.1523/jneurosci.17-21-08427.1997},
	journal-iso = {J NEUROSCI},
	journal = {JOURNAL OF NEUROSCIENCE},
	volume = {17},
	unique-id = {108671},
	issn = {0270-6474},
	year = {1997},
	eissn = {1529-2401},
	pages = {8427-8442}
}

@article{MTMT:107931,
	title = {Interneurons of the hippocampus},
	url = {https://m2.mtmt.hu/api/publication/107931},
	author = {Freund, Tamás and Buzsáki, György},
	doi = {10.1002/(SICI)1098-1063(1996)6:4<347::AID-HIPO1>3.0.CO;2-I},
	journal-iso = {HIPPOCAMPUS},
	journal = {HIPPOCAMPUS},
	volume = {6},
	unique-id = {107931},
	issn = {1050-9631},
	year = {1996},
	eissn = {1098-1063},
	pages = {347-470}
}

@article{MTMT:107721,
	title = {Differences between somatic and dendritic inhibition in the hippocampus},
	url = {https://m2.mtmt.hu/api/publication/107721},
	author = {Miles, R and Tóth, Katalin and Gulyás, Attila and Hájos, Norbert and Freund, Tamás},
	doi = {10.1016/S0896-6273(00)80101-4},
	journal-iso = {NEURON},
	journal = {NEURON},
	volume = {16},
	unique-id = {107721},
	issn = {0896-6273},
	year = {1996},
	eissn = {1097-4199},
	pages = {815-823},
	orcid-numbers = {Gulyás, Attila/0000-0003-4961-636X}
}

@article{MTMT:107793,
	title = {Synaptic input of horizontal interneurons in striatum oriens of the hippocampal CA1 subfield: Structural basis of feed-back activation},
	url = {https://m2.mtmt.hu/api/publication/107793},
	author = {Blasco-Ibanez, Jose Miguel and Freund, Tamás},
	doi = {10.1111/j.1460-9568.1995.tb00638.x},
	journal-iso = {EUR J NEUROSCI},
	journal = {EUROPEAN JOURNAL OF NEUROSCIENCE},
	volume = {7},
	unique-id = {107793},
	issn = {0953-816X},
	year = {1995},
	eissn = {1460-9568},
	pages = {2170-2180}
}

@article{MTMT:1661000,
	title = {SYNCHRONIZATION OF NEURONAL-ACTIVITY IN HIPPOCAMPUS BY INDIVIDUAL GABAERGIC INTERNEURONS},
	url = {https://m2.mtmt.hu/api/publication/1661000},
	author = {COBB, SR and BUHL, EH and Halasy, Katalin and PAULSEN, O and Somogyi, Péter Pál},
	doi = {10.1038/378075a0},
	journal-iso = {NATURE},
	journal = {NATURE},
	volume = {378},
	unique-id = {1661000},
	issn = {0028-0836},
	abstract = {SYNCHRONIZATION Of neuronal activity is fundamental in the operation of cortical networks(1). With respect to an ongoing synchronized oscillation, the precise timing of action potentials is an attractive candidate mechanism for information coding(2-5) Networks of inhibitory interneurons have been proposed to have a role in entraining cortical, synchronized 40-Hz activity(6,7). Here we demonstrate that individual GABAergic interneurons(8) can effectively phase spontaneous firing and subthreshold oscillations in hippocampal pyramidal cells at theta frequencies (4-7 Hz). The efficiency of this entrainment is due to interaction of GABA(A)-receptor-mediated hyperpolarizing synaptic events with intrinsic oscillatory mechanisms tuned to this frequency range in pyramidal cells. Moreover, this GABAergic mechanism is sufficient to synchronize the firing of pyramidal cells. Thus, owing to the divergence of each GABAergic interneuron(9,10), more than a thousand pyramidal cells may share a common temporal reference established by an individual interneuron.},
	year = {1995},
	eissn = {1476-4687},
	pages = {75-78}
}

@article{MTMT:1660995,
	title = {DIVERSE SOURCES OF HIPPOCAMPAL UNITARY INHIBITORY POSTSYNAPTIC POTENTIALS AND THE NUMBER OF SYNAPTIC RELEASE SITES},
	url = {https://m2.mtmt.hu/api/publication/1660995},
	author = {BUHL, EH and Halasy, Katalin and Somogyi, Péter Pál},
	doi = {10.1038/368823a0},
	journal-iso = {NATURE},
	journal = {NATURE},
	volume = {368},
	unique-id = {1660995},
	issn = {0028-0836},
	abstract = {Dual intracellular recordings from microscopically identified neurons in the hippocampus reveal that the synaptic terminals of three morphologically distinct types of interneuron act through GABA(A) receptors. Each type of interneuron forms up to 12 synaptic contacts with a postsynaptic principal neuron, but each interneuron innervates a different domain of the surface of the postsynaptic neuron. Different kinetics of the postsynaptic effects, together with the strategic placement of synapses, indicate that these GABAergic interneurons serve distinct functions in the cortical network.},
	year = {1994},
	eissn = {1476-4687},
	pages = {823-828}
}

@article{MTMT:108532,
	title = {The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction},
	url = {https://m2.mtmt.hu/api/publication/108532},
	author = {Baude, A and Nusser, Zoltán and Roberts, JDB and Mulvihill, E and McIIhinney, RAJ and Somogyi, Péter Pál},
	doi = {10.1016/0896-6273(93)90086-7},
	journal-iso = {NEURON},
	journal = {NEURON},
	volume = {11},
	unique-id = {108532},
	issn = {0896-6273},
	abstract = {An antiserum to mGluR1α labeled a 160 kd protein in immunoblots of membranes derived from rat brain or cells transfected with mGluRlα. Immunoreactivity for mGluR1 a was present in discrete subpopulations of neurons. The GABAergic neurons of the cerebellar cortex were strongly immunoreactive; only some Golgi cells were immunonegative. Somatostatin/GABA-immunopositive cells in the neocortex and hippocampus were enriched in mGluR1α. The hippocampal cells had spiny dendrites that were precisely codistributed with the local axon collaterals of pyramidal and granule cells. Electron microscopic immunometal detection of mGluR1α showed a preferential localization at the periphery of the extensive postsynaptic densities of type 1 synapses in both the cerebellum and the hippocampus. The receptor was also present at sites in the dendritic and somatic membrane where synapses were not located. © 1993.},
	year = {1993},
	eissn = {1097-4199},
	pages = {771-787}
}

@article{MTMT:107599,
	title = {Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region},
	url = {https://m2.mtmt.hu/api/publication/107599},
	author = {Gulyás, Attila and Miles, R and Hájos, Norbert and Freund, Tamás},
	doi = {10.1111/j.1460-9568.1993.tb00240.x},
	journal-iso = {EUR J NEUROSCI},
	journal = {EUROPEAN JOURNAL OF NEUROSCIENCE},
	volume = {5},
	unique-id = {107599},
	issn = {0953-816X},
	year = {1993},
	eissn = {1460-9568},
	pages = {1729-1751},
	orcid-numbers = {Gulyás, Attila/0000-0003-4961-636X}
}

@article{MTMT:107244,
	title = {Pattern of neuronal death in the rat hippocampus after status epilepticus. Relationship to calcium binding protein content and ischemic vulnerability},
	url = {https://m2.mtmt.hu/api/publication/107244},
	author = {Freund, Tamás and Ylinen, A and Miettinen, R and Pitkänen, A and Lahtinen, H and Baimbridge, KG and Riekkinen, PJ},
	doi = {10.1016/0361-9230(92)90227-O},
	journal-iso = {BRAIN RES BULL},
	journal = {BRAIN RESEARCH BULLETIN},
	volume = {28},
	unique-id = {107244},
	issn = {0361-9230},
	year = {1992},
	eissn = {1873-2747},
	pages = {27-38}
}