Properties of Unitary IPSCs in Hippocampal Pyramidal Cells Originating From Different Types of Interneurons in Young Rats

1997 ◽  
Vol 77 (4) ◽  
pp. 1939-1949 ◽  
Author(s):  
Mohamed Ouardouz ◽  
Jean-Claude Lacaille
Keyword(s):  
Reversal Potential ◽  
Pyramidal Cells ◽  
Mean Amplitude ◽  
Paired Pulse ◽  
Young Rats ◽  
Different Types ◽  
The Mean ◽  
Paired Pulse Depression ◽  
Types Of Interneurons ◽  
Stimulation Of

Ouardouz, Mohamed and Jean-Claude Lacaille. Properties of unitary IPSCs in hippocampal pyramidal cells originating from different types of interneurons in young rats. J. Neurophysiol. 77: 1939–1949, 1997. Whole cell recordings were used in hippocampal slices of young rats to examine unitary inhibitory postsynaptic currents (uIPSCs) evoked in CA1 pyramidal cells at room temperature. Loose cell-attached stimulation was applied to activate single interneurons of different subtypes located in stratum oriens (OR), near stratum pyramidale (PYR), and at the border of stratum radiatum and lacunosum-moleculare (LM). uIPSCs evoked by stimulation of PYR and OR interneurons had similar onset latency, rise time, peak amplitude, and decay. In contrast, uIPSCs elicited by activation of LM interneurons were significantly smaller in amplitude and had a slower time course. The mean reversal potential of uIPSCs was −53.1 ± 2.1 (SE) mV during recordings with intracellular solution containing potassium gluconate. With the use of recording solution containing the potassium channel blocker cesium, the reversal potential of uIPSCs was not significantly different (−58.5 ± 2.6 mV), suggesting that these synaptic currents were not mediated by potassium conductances. Bath application of the γ-aminobutyric acid-A (GABAA) receptor antagonist bicuculline (25 μM) reversibly blocked uIPSCs evoked by stimulation of all interneuron subtypes. In bicuculline, the mean peak amplitude of uIPSCs recorded with potassium gluconate was reduced to 3.5 ± 4.4% of control ( n = 7). Similarly, with cesium methanesulfonate, the mean amplitude in bicuculline was 2.9 ± 3.1% of control ( n = 13). Application of the GABAB receptor antagonist CGP 55845A (5 μM) resulted in a significant and reversible increase in the mean amplitude of uIPSCs recorded with cesium-containing intracellular solution. Thus uIPSCs from all cell types appeared under tonic presynaptic inhibition by GABAB receptors. Paired stimulation of individual interneurons at 100- to 200-ms intervals did not result in paired pulse depression of uIPSCs. For individual responses, a significant negative correlation was observed between the amplitude of the first and second uIPSCs. A significant paired pulse facilitation (154.0 ± 8.0%) was observed when the first uIPSC was smaller than the mean of all first uIPSCs. A small, but not significant, paired pulse depression (90.8 ± 4.0%) was found when the first uIPSC was larger than the mean of all first uIPSCs. Our results indicate that these different subtypes of hippocampal interneurons generate Cl−-mediated GABAA uIPSCs. uIPSCs originating from different types of interneurons may have heterogeneous properties and may be subject to tonic presynaptic inhibition via heterosynaptic GABAB receptors. These results suggest a specialization of function for inhibitory interneurons and point to complex presynaptic modulation of interneuron function.

Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically

1993 ◽  
Vol 70 (6) ◽  
pp. 2354-2369 ◽  
Author(s):  
A. M. Thomson ◽  
J. Deuchars ◽  
D. C. West
Keyword(s):  
Deep Layer ◽  
Short Interval ◽  
Pyramidal Cells ◽  
Postsynaptic Membrane ◽  
Paired Pulse ◽  
Paired Pulse Facilitation ◽  
Wide Range ◽  
Mean Width ◽  
The Mean ◽  
Paired Pulse Depression

1. In slices of rat sensorimotor cortex, dual intracellular recordings were obtained from 1,952 pairs of deep layer pyramidal neurons. Where action potentials in one neurone elicited excitatory postsynaptic potentials (EPSPs, n = 56) in the other, responses to different presynaptic firing rates and patterns and at different postsynaptic membrane potentials were recorded and on some occasions both neurons were filled with biocytin. 2. Slices were fixed, sectioned again at 60 microns, and incubated with Avidin horseradish peroxidase (HRP), which was then visualized using the 3,3'-diaminobenzidine tetrahydrochloride (DAB) method. All neurones reported here that were identified histologically were pyramidal cells with their somata in the deep layers (V and VI). 3. One in 70 of the tests performed revealed a synaptic connection, 25 of which were studied in detail. Mean EPSP amplitude was 1.67 +/- 1.66 (SD) mV, with some single sweep events as large as 9 mV. For some of the smaller EPSPs the amplitude distributions contained a clear peak around 0 mV, the coefficient of variation (CV) was large, and paired pulse facilitation was apparent. EPSPs with large average amplitudes displayed no apparent failures of transmission, EPSP amplitudes were fairly evenly distributed around the mean, CVs were small, and paired pulse depression was apparent in 2.5 mM extracellular Ca2+. When single sweeps were selected according to the size of the first EPSP, large second EPSPs were found to follow small first EPSPs and small second EPSPs to follow large first EPSPs. Paired pulse effects appeared, in the majority of tests, to be due to a change in presynaptic release probability. 4. Two EPSPs were recorded in three different extracellular Ca2+ concentrations. In 1 mM Ca2+, the first EPSP of a short interval pair was small and paired pulse facilitation was apparent. In 5 mM Ca2+, first EPSPs were between 2.5 and 4 times larger than in 1 mM Ca2+ and paired pulse depression was apparent. In all Ca2+ concentrations however, averaged third and fourth EPSPs of brief bursts were of similar amplitudes and smaller than second EPSPs. If presynaptic inhibition does contribute to paired pulse effects here, it is not overcome by a combination of raised extracellular Ca2+ and repetitive presynaptic firing. 5. These EPSPs displayed a wide range of time courses. The mean 10-90% rise time was 2.49 +/- 1.08 ms, the mean width at half amplitude was 15.39 +/- 5.42 ms (n = 22), and the mean EPSP latency was 1.59 +/- 0.68 ms (n = 18). (ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Ontogenesis of Presynaptic GABAB Receptor-Mediated Inhibition in the CA3 Region of the Rat Hippocampus

1998 ◽  
Vol 79 (3) ◽  
pp. 1341-1348 ◽  
Author(s):  
Olivier Caillard ◽  
Heather A. McLean ◽  
Yehezkel Ben-Ari ◽  
Jean-Luc Gaïarsa
Keyword(s):  
Pyramidal Neurons ◽  
Gabab Receptor ◽  
Hippocampal Slices ◽  
Reversal Potential ◽  
Rat Hippocampus ◽  
Dependent Manner ◽  
Paired Pulse ◽  
Ca3 Pyramidal Neurons ◽  
Paired Pulse Depression ◽  
Ca3 Region

Caillard, Olivier, Heather A. McLean, Yehezkel Ben-Ari, and Jean-Luc Gaı̈arsa. Ontogenesis of presynaptic GABAB receptor-mediated inhibition in the CA3 region of the rat hippocampus. J. Neurophysiol. 79: 1341–1348, 1998. γ-Aminobutyric acid-B(GABAB) receptor-dependent and -independent components of paired-pulse depression (PPD) were investigated in the rat CA3 hippocampal region. Intracellular and whole cell recordings of CA3 pyramidal neurons were performed on hippocampal slices obtained from neonatal (5–7 day old) and adult (27–34 day old) rats. Electrical stimulation in the hilus evoked monosynaptic GABAA postsynaptic currents (eIPSCs) isolated in the presence of the ionotropic glutamate receptor antagonists 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 10 μM) and d(−)2-amino-5-phosphovaleric acid (d-AP5, 50 μM) with 2(triethylamino)- N-(2,6-dimethylphenyl) acetamine (QX314) filled electrodes. In adult CA3 pyramidal neurons, when a pair of identical stimuli was applied at interstimulus intervals (ISIs) ranging from 50 to 1,500 ms the amplitude of the second eIPSC was depressed when compared with the first eIPSC. This paired-pulse depression (PPD) was partially blockedb y  P - 3 - a m i n o p r o p y l - P - d i e t h o x y m e t h y l  p h o s p h o r i c  a c i d(CGP35348, 0.5 mM), a selective GABAB receptor antagonist. In neonates, PPD was restricted to ISIs shorter than 200 ms and was not affected by CGP35348. The GABAB receptor agonist baclofen reduced the amplitude of eIPSCs in a dose-dependent manner with the same efficiency in both adults and neonates. Increasing the probability of transmitter release with high Ca2+ (4 mM)/low Mg2+ (0.3 mM) external solution revealed PPD in neonatal CA3 pyramidal neurons that was 1) partially prevented by CGP35348, 2) independent of the membrane holding potential of the recorded cell, and 3) not resulting from a change in the reversal potential of GABAA eIPSCs. In adults the GABA uptake blocker tiagabine (20 μM) increased the duration of eIPSCs and the magnitude of GABAB receptor-dependent PPD. In neonates, tiagabine also increased duration of eIPSCs but to a lesser extent than in adult and did not reveal a GABAB receptor-dependent PPD. These results demonstrate that although GABAB receptor-dependent and -independent mechanisms of presynaptic inhibition are present onGABAergic terminals and functional, they do not operate at the level of monosynaptic GABAergic synaptic transmission at early stages of development. Absence of presynaptic autoinhibition of GABA release seems to be due to the small amount of transmitter that can access presynaptic regulatory sites.

Effects of chronic spinalization on ankle extensor motoneurons. I. Composite monosynaptic Ia EPSPs in four motoneuron pools

1994 ◽  
Vol 71 (4) ◽  
pp. 1452-1467 ◽  
Author(s):  
S. Hochman ◽  
D. A. McCrea
Keyword(s):  
Rise Time ◽  
Statistical Significance ◽  
Mean Amplitude ◽  
Significant Rise ◽  
Medial Gastrocnemius ◽  
Membrane Properties ◽  
Pooled Data ◽  
Extensor Motoneuron ◽  
The Mean ◽  
Stimulation Of

1. We examined the effects of 6-wk chronic spinalization at the L1-L2 level on composite monosynaptic Ia excitatory postsynaptic potentials (EPSPs) recorded in medial gastrocnemius (MG), lateral gastrocnemius (LG), soleus (SOL), and plantaris (PL) motoneurons. Amplitudes, rise times, and half-widths of composite monosynaptic Ia EPSPs evoked by low-strength electrical stimulation of peripheral nerves were measured in barbiturate-anesthetized cats and compared between unlesioned and chronic spinal preparations. 2. The mean amplitude of homonymous composite Ia EPSPs evoked by 1.2 times threshold (1.2T) stimulation and recorded in all four ankle extensor motoneuron pools increased 26% in chronic spinal animals compared with unlesioned controls. There was also an increased incidence of large-amplitude, short-rise time EPSPs. When the same data were separated according to individual motoneuron species, homonymous EPSP amplitudes in MG motoneurons were found to be unchanged. EPSPs recorded in LG motoneurons and evoked by stimulation of the combined LG and SOL nerve were increased by 46%. Mean EPSP amplitudes recorded in both SOL and PL motoneurons were larger after spinalization but statistical significance was only achieved when values from SOL and PL were combined to produce a larger sample size. 3. In LG motoneurons from chronic spinal animals, all EPSPs evoked by 1.2T stimulation of the LGS nerve were > or = 0.5 mV in amplitude. In unlesioned preparations, one fourth of the LG cells had EPSPs that were < or = 0.2 mV. 4. The mean amplitude of heteronymous EPSPs evoked by 2T stimulation of LGS and MG nerves and recorded in MG and LG motoneurons, respectively, doubled in size after chronic spinalization. Because homonymous EPSP amplitudes were unchanged in MG motoneurons, synaptic mechanisms and not passive membrane properties are likely responsible for increased heteronymous EPSP amplitudes in MG. 5. The mean 10-90% rise time of homonymous composite Ia EPSPs in pooled data from all motoneurons decreased 21% in 6-wk chronic spinal animals. Unlike EPSP amplitude, significant rise time decreases were found in all four motoneuron pools. Compared with the other motoneuron species, the mean homonymous rise time recorded in MG motoneurons was shortest and decreased the least in chronic spinal animals. Rise times of heteronymous Ia EPSPs in MG and LG motoneurons also decreased. The maximum rate of rise of homonymous EPSPs increased in all four motoneuron species. 6. The mean half-widths of Ia composite EPSPs decreased in 6-wk spinalized preparations in all motoneuron species.(ABSTRACT TRUNCATED AT 400 WORDS)

Coordination of Limb Movements: Three Types of Intersegmental Interneurons in the Swimmeret System and Their Responses to Changes in Excitation

1999 ◽  
Vol 81 (5) ◽  
pp. 2437-2450 ◽  
Author(s):  
Hisaaki Namba ◽  
Brian Mulloney
Keyword(s):  
Limb Movements ◽  
Impulse Frequency ◽  
The Third ◽  
Physiological Properties ◽  
Bath Application ◽  
Different Types ◽  
Forward Locomotion ◽  
The Mean ◽  
Necessary And Sufficient ◽  
Types Of Interneurons

Coordination of limb movements: three types of intersegmental interneurons in the swimmeret system and their responses to changes in excitation. During forward locomotion, the movements of swimmerets on different segments of the crayfish abdomen are coordinated so that more posterior swimmerets lead their anterior neighbors by ∼25%. This coordination is accomplished by mechanisms within the abdominal nerve cord. Here we describe three different types of intersegmental swimmeret interneurons that are necessary and sufficient to accomplish this coordination. These interneurons could be identified both by their structures within their home ganglion and by their physiological properties. These interneurons occur as bilateral pairs in each ganglion that innervates swimmerets, and their axons traverse the minuscule tract (MnT) of their home ganglion before leaving to project to neighboring ganglia. Two types, ASCEand ASCL, projected an axon anteriorly; the third type, DSC, projected posteriorly. Each type fires a burst of impulses starting at a different phase of the swimmeret cycle in its home ganglion. In active preparations, excitation of individual ASCE or DSC interneurons at different phases in the cycle affected the timing of the next cycle in the interneuron’s target ganglion. The axons of these interneurons that projected between two ganglia ran close together, and their firing often could be recorded by the same electrode. Experiments in which either this tract or the rest of the intersegmental connectives was cut bilaterally showed that these interneurons were both necessary and sufficient for coordination of neighboring swimmerets. When the level of excitation of the swimmeret system was increased by bath application of carbachol, the period of the system’s cycle shortened, but the characteristic phase difference within and between ganglia was preserved. Each of these interneurons responded to this increase in excitation by increasing the frequency of impulses within each burst, but the phases and relative durations of their bursts did not change, and their activity remained coordinated with the cycle in their home ganglion. The decrease in duration of each burst was matched to the increase in impulse frequency within the burst so that the mean numbers of impulses per burst did not change significantly despite a threefold change in period. These three types of interneurons appear to form a concatenated intersegmental coordinating circuit that imposes a particular intersegmental phase on the local pattern generating modules innervating each swimmeret. This circuit is asymmetric, and forces posterior segments to lead each cycle of output.

scholarly journals Properties of the primary somatosensory cortex projection to the primary motor cortex in the mouse

2015 ◽  
Vol 113 (7) ◽  
pp. 2400-2407 ◽  
Author(s):  
Iraklis Petrof ◽  
Angela N. Viaene ◽  
S. Murray Sherman
Keyword(s):  
Primary Motor Cortex ◽  
Metabotropic Glutamate Receptor ◽  
Pyramidal Cells ◽  
Receptor Activation ◽  
Slice Preparation ◽  
Paired Pulse ◽  
Metabotropic Glutamate ◽  
Driver Pathway ◽  
Synaptic Boutons ◽  
Paired Pulse Depression

The primary somatosensory (S1) and primary motor (M1) cortices are reciprocally connected, and their interaction has long been hypothesized to contribute to coordinated motor output. Very little is known, however, about the nature and synaptic properties of the S1 input to M1. Here we wanted to take advantage of a previously developed sensorimotor slice preparation that preserves much of the S1-to-M1 connectivity (Rocco MM, Brumberg JC. J Neurosci Methods 162: 139–147, 2007), as well as available optogenetic methodologies, in order to investigate the synaptic profile of this projection. Our data show that S1 input to pyramidal cells of M1 is highly homogeneous, possesses many features of a “driver” pathway, such as paired-pulse depression and lack of metabotropic glutamate receptor activation, and is mediated through axons that terminate in both small and large synaptic boutons. Our data suggest that S1 provides M1 with afferents that possess synaptic and anatomical characteristics ideal for the delivery of strong inputs that can “drive” postsynaptic M1 cells, thereby potentially affecting their output.

Differential Effect of Ethanol on NMDA EPSCs in Pyramidal Cells in the Posterior Cingulate Cortex of Juvenile and Adult Rats

2002 ◽  
Vol 87 (2) ◽  
pp. 705-711 ◽  
Author(s):  
Qiang Li ◽  
Wilkie A. Wilson ◽  
H. Scott Swartzwelder
Keyword(s):  
Nmda Receptor ◽  
Pyramidal Cells ◽  
Cingulate Cortex ◽  
Mean Amplitude ◽  
Inhibitory Effect ◽  
Posterior Cingulate Cortex ◽  
Adult Rats ◽  
Posterior Cingulate ◽  
Cellular Analysis ◽  
The Mean

Ethanol (EtOH) is a potent inhibitor of N-methyl-d-aspartate (NMDA) receptor–mediated activity in a number of brain areas, and recent studies have indicated that this inhibitory effect of ethanol is more powerful in the juvenile brain compared with the adult brain. However, previous direct developmental comparisons have been limited to studies of extracellular responses in the hippocampus. To begin an assessment of the mechanisms underlying this developmental sensitivity, we assessed the inhibitory effect of EtOH on NMDA receptor–mediated synaptic transmission in neocortical slices from adult (95–135 days old) and juvenile (28–32 days old) rats using the whole cell patch-clamp recording technique. In the presence of 6,7-dinitroquinoxaline-2,3-dione (20 μM) and bicuculline methiodine (20 μM), NMDA receptor–mediated excitatory postsynaptic currents were isolated from pyramidal cells of the posterior cingulate cortex (PCC). In slices from juvenile rats 5, 10, 30, and 60 mM EtOH reduced the mean amplitude of NMDA receptor–mediated EPSCs by 11, 22, 35, and 46%, respectively. However, the same concentrations of EtOH inhibited the mean amplitude of EPSCs by only 4, 8, 15, and 31% in slices from adult rats. This developmental difference in the potency of EtOH against NMDA receptor–mediated EPSCs was also observed when the holding potential of the neurons was increased to +30 mV, although the inhibitory effect of ethanol on adult neurons was diminished at that voltage. These results provide a cellular analysis of the enhanced potency of ethanol against NMDA receptor–mediated EPSCs in neocortical cells from juvenile animals compared with adults.

Activity-Dependent Depression of Local Excitatory Connections in the CA1 Region of Mouse Hippocampus

2007 ◽  
Vol 97 (6) ◽  
pp. 3926-3936 ◽  
Author(s):  
Ann E. Fink ◽  
Joshua Sariñana ◽  
Erin E. Gray ◽  
Thomas J. O'Dell
Keyword(s):  
Pyramidal Cell ◽  
Adenosine Receptors ◽  
Low Frequency ◽  
Pyramidal Cells ◽  
Paired Pulse ◽  
Ca1 Pyramidal Cells ◽  
Ca1 Region ◽  
Activity Dependent ◽  
Fiber Stimulation ◽  
Paired Pulse Depression

The existence of recurrent excitatory synapses between pyramidal cells in the hippocampal CA1 region has been known for some time yet little is known about activity-dependent forms of plasticity at these synapses. Here we demonstrate that under certain experimental conditions, Schaffer collateral/commissural fiber stimulation can elicit robust polysynaptic excitatory postsynaptic potentials due to recurrent synaptic inputs onto CA1 pyramidal cells. In contrast to CA3 pyramidal cell inputs, recurrent synapses onto CA1 pyramidal cells exhibited robust paired-pulse depression and a sustained, but rapidly reversible, depression in response to low-frequency trains of Schaffer collateral fiber stimulation. Blocking GABAB receptors abolished paired-pulse depression but had little effect on low-frequency stimulation (LFS)-induced depression. Instead, LFS-induced depression was significantly attenuated by an inhibitor of A1 type adenosine receptors. Blocking the postsynaptic effects of GABAB and A1 receptor activation on CA1 pyramidal cell excitability with an inhibitor of G-protein-activated inwardly rectifying potassium channels had no effect on either paired-pulse depression or LFS-induced depression. Thus activation of presynaptic GABAB and adenosine receptors appears to have an important role in activity-dependent depression at recurrent synapses. Together, our results indicate that CA3-CA1 and CA1-CA1 synapses exhibit strikingly different forms of short-term synaptic plasticity and suggest that activity-dependent changes in recurrent synaptic transmission can transform the CA1 region from a sparsely connected recurrent network into a predominantly feedforward circuit.

GABAB autoreceptors mediate activity-dependent disinhibition and enhance signal transmission in the dentate gyrus

1993 ◽  
Vol 69 (3) ◽  
pp. 674-691 ◽  
Author(s):  
D. D. Mott ◽  
C. W. Xie ◽  
W. A. Wilson ◽  
H. S. Swartzwelder ◽  
D. V. Lewis
Keyword(s):  
Dentate Gyrus ◽  
Receptor Antagonist ◽  
Granule Cells ◽  
Gabab Receptor ◽  
Mossy Fiber ◽  
Signal Transmission ◽  
Paired Pulse ◽  
Activity Dependent ◽  
Paired Pulse Depression ◽  
Stimulation Of

1. Activity-dependent depression (fading) of polysynaptic inhibition and the effects of this disinhibition on signal transmission were studied in the dentate gyrus of the rat hippocampal slice with the use of intracellular and extracellular recordings. 2. Polysynaptic inhibitory postsynaptic potentials/currents (IPSP/Cs) were evoked in dentate granule cells by stimulation of mossy fibers in stratum lucidum of area CA3b/c. These mossy fiber-evoked IPSP/Cs consisted of an early GABAA receptor-mediated component (IPSP/CA) and a late GABAB receptor-mediated component (IPSP/CB). 3. When paired stimuli were delivered 200 ms apart under voltage clamp, the amplitude of the IPSCA and IPSCB evoked by the second stimulus was reduced by 37.0 +/- 4.0 and 61.6 +/- 7.8% (mean +/- SE), respectively. Paired-pulse depression of both IPSCA and IPSCB was greatest at interstimulus intervals of 100-400 ms with a maximal effect when stimuli were delivered 200 ms apart. 4. (+/-) Baclofen, a GABAB receptor agonist, suppressed both components of the mossy fiber-evoked IPSP in a concentration-dependent fashion. At a concentration that only partially suppressed the initial IPSP, baclofen occluded paired-pulse depression of IPSPA. In addition, paired-pulse depression of IPSPA was blocked in a concentration-dependent fashion by 2-hydroxy-saclofen (10-400 microM), a GABAB receptor antagonist. 5. The contribution of the IPSPB conductance increase to paired-pulse depression of IPSPA was evaluated. Paired-pulse depression of IPSPA was significantly greater than was the depression of the response to a current pulse delivered 200 ms after the mossy fiber stimulus. In addition, injection of granule cells with GTP gamma S, a nonhydrolyzable guanosine triphosphate (GTP) analogue, occluded both IPSPB as well as the effects of baclofen on the granule cell membrane by activating G proteins but did not reduce paired-pulse depression of IPSPA or suppression of IPSPA by baclofen. Finally, examination of the first and second IPSCA evoked by paired stimuli 200 ms apart revealed no significant differences in response kinetics. Taken together, these results indicate that postsynaptic GABAB receptors on the granule cells are not responsible for paired-pulse depression of IPSPA. 6. Monosynaptic IPSPs were evoked by direct stimulation of inhibitory neurons in the inner molecular layer of the dentate gyrus during pharmacological blockade of excitatory transmission with D(-)-2-amino-5-phosphonovaleric acid (D-APV), an N-methyl-D-aspartate (NMDA) receptor antagonist and 6,7-dinitroquinoxaline-2,3-dione (DNQX), a non-NMDA glutamate receptor antagonist.(ABSTRACT TRUNCATED AT 400 WORDS)

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