Types Of Inhibitory Postsynaptic Potentials Research Articles

Identified sources and targets of slow inhibition in the neocortex.

There are two types of inhibitory postsynaptic potentials in the cerebral cortex. Fast inhibition is mediated by ionotropic gamma-aminobutyric acid type A (GABA(A)) receptors, and slow inhibition is due to metabotropic GABA(B) receptors. Several neuron classes elicit inhibitory postsynaptic potentials through GABA(A) receptors, but possible distinct sources of slow inhibition remain unknown. We identified a class of GABAergic interneurons, the neurogliaform cells, that, in contrast to other GABA-releasing cells, elicited combined GABA(A) and GABA(B) receptor-mediated responses with single action potentials and that predominantly targeted the dendritic spines of pyramidal neurons. Slow inhibition evoked by a distinct interneuron in spatially restricted postsynaptic compartments could locally and selectively modulate cortical excitability.

Medullary reticulospinal tract mediating the generalized motor inhibition in cats: Parallel inhibitory mechanisms acting on motoneurons and on interneuronal transmission in reflex pathways

The present study was designed to elucidate the spinal interneuronal mechanisms of motor inhibition evoked by stimulating the medullary reticular formation. Two questions were addressed. First, whether there is a parallel motor inhibition to motoneurons and to interneurons in reflex pathways. Second, whether the inhibition is mediated by interneurons interposed in known reflex pathways. We recorded the intracellular activity of hindlimb motoneurons in decerebrate cats and examined the effects of medullary stimulation on these neurons and on interneuronal transmission in reflex pathways to them. Stimuli (three pulses at 10–60 μA and 1–10 ms intervals) delivered to the nucleus reticularis gigantocellularis evoked inhibitory postsynaptic potentials in α-motoneurons ( n=147) and γ-motoneurons ( n=5) with both early and late latencies. The early inhibitory postsynaptic potentials were observed in 66.4% of the motoneurons and had a latency of 4.0–5.5 ms with a segmental delay of more than 1.4 ms. The late inhibitory postsynaptic potentials were observed in 98.0% of the motoneurons and had a latency of 30–35 ms, with a peak latency of 50–60 ms. Both types of inhibitory postsynaptic potentials were evoked through fibers descending in the ventrolateral quadrant. The inhibitory postsynaptic potentials were not influenced by recurrent inhibitory pathways, but both types were greatly attenuated by volleys in flexor reflex afferents. Conditioning medullary stimulation, which was subthreshold to evoke inhibitory postsynaptic potentials in the motoneurons, neither evoked primary afferent depolarization of dorsal roots nor reduced the input resistance of the motoneurons. However, the conditioning stimulation often facilitated non-reciprocal group I inhibitory pathways (Ib inhibitory pathways) to the motoneurons in early (<20 ms) and late (30–80 ms) periods. In contrast, it attenuated test postsynaptic potentials evoked through reciprocal Ia inhibitory pathways, and excitatory and inhibitory pathways from flexor reflex afferent and recurrent inhibitory pathways. The inhibitory effects were observed in both early and late periods. The present results provide new information about a parallel inhibitory process from the medullary reticular formation that produces a generalized motor inhibition by acting on α- and γ-motoneurons, and on interneurons in reflex pathways. Interneurons receiving inhibition from flexor reflex afferents and a group of Ib interneurons may mediate the inhibitory effects upon motoneurons.

Slow and fast synaptic inhibition evoked by pattern-generating neurons of the gastric mill network in spiny lobsters.

1. In this paper we begin an assessment of the role of synaptic properties, especially synaptic time course, in the function of the central pattern generator circuit (CPG) that controls rhythmic movements of the gastric mill in the foregut of spiny lobster (Panulirus interruptus). 2. The majority of neurons in the gastric CPG are motor neurons (MNs) that innervate striated muscles of the gastric mill but that also make electrical and inhibitory chemical interconnections within the neuropil of the stomatogastric ganglion. We studied the ionic dependence, pharmacology, and time course of inhibitory postsynaptic potentials (IPSPs) evoked by two such MNs, the dorsal gastric (DG) and lateral gastric (LG), in their central synaptic partners. In the periphery, LG and DG are thought to release glutamate. 3. LG and DG evoke two types of IPSPs in follower neurons. The first, fast type of IPSP rises rapidly (the graded component within 100-300 ms, the spike-mediated components within a few tens of ms), is mediated by increased chloride and potassium conductances, and is blocked by < or = 10 microM picrotoxin (PTX). These fast IPSPs closely resemble the glutamatergic IPSPs described in the pyloric circuit of the same ganglion. 4. The second, slow type of IPSP has a long rise time (1-2 s), is mediated by increased conductance to potassium (with little or no involvement of chloride), and is not blocked by 10 microM PTX, 5 mM tetraethylammonium chloride, or 0.1 mM scopolamine. These properties distinguish slow IPSPs from the forms of glutamatergic and cholinergic inhibition that have been described in the pyloric circuit. 5. Fast inhibition occurs alone at connections from DG and LG to power stroke MNs (median gastric and gastric mill). Slow inhibition occurs in parallel with fast inhibition (producing dual-component responses) at connections from LG to return stroke neurons [lateral posterior gastric MNs, (LPGs) and interneuron 1]. DG seems to evoke only a slow IPSP in LPGs. 6. The transmitter mediating the fast IPSPs is likely to be glutamate. We discuss possible mechanisms for the slow IPSP but have no evidence at present concerning the transmitter(s) involved. Slow inhibition is likely to be an important synaptic "building block" in the gastric CPG; it is "tuned" to the duration of gastric bursts and may contribute to the long cycle period of gastric rhythms.

Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro.

Synaptic inhibition was investigated by stimulating inhibitory neurones with focal microapplications of glutamate, while recording from layer V pyramidal neurones of rat somatosensory cortical slices. One class of inhibitory postsynaptic potentials (IPSPs) thus elicited was characterized as a fast, chloride-mediated, GABAA IPSP in part by its fast time-to-peak (mean 2.5 ms) and brief duration, but primarily on the basis of its reversal potential at -68 mV, and its blockade by picrotoxin. The average peak amplitude for these fast IPSPs was -1.5 mV, measured at -60 mV. The peak conductance calculated for these events was about 10 nS. The conductance change associated with the maximal fast inhibitory postsynaptic potential resulting from electrical stimulation of afferent pathways ranged up to 116 nS. A second class of IPSP was encountered much less frequently. These glutamate-triggered events were characterized as slow, potassium-mediated GABAB IPSPs partly because of their longer times-to-peak (mean, 45 ms) and duration, but especially because of their extrapolated equilibrium potential at about -89 mV and blockade by 2-hydroxysaclofen. The average peak amplitude for these slow IPSPs was -2.3 mV, measured at -60 mV. The peak conductance for these events was about 8 nS. IPSPs resulting from the excitation of individual inhibitory interneurones were elicited by glutamate microapplication at particular locations relative to recording sites. Both fast and slow IPSPs were generated, but these occurred as separate events, and mixed responses were never seen. Thus, the two mechanistically distinct types of IPSPs which result from GABA interaction at GABAA and GABAB receptors on neocortical neurones may be mediated by separate classes of inhibitory neurones.

Various types of inhibitory postsynaptic potentials in anterior thalamic cells are differentially altered by stimulation of laterodorsal tegmental cholinergic nucleus

The effects of stimulating the laterodorsal tegmental cholinergic nucleus upon inhibitory postsynaptic potentials recorded in relay cells of the anterior thalamic complex were studied in urethane-anesthetized cats. The inhibitory postsynaptic potentials induced in anterior thalamic relay cells by stimulating mammillary nuclei or retrosplenial cortex are generated by local-circuit inhibitory neurons since this nuclear complex is devoid of afferents from the other intrathalamic source of inhibition, the reticular thalamic nucleus. In a parallel study from this laboratory, it has been shown that cortical stimulation elicits a biphasic inhibitory postsynaptic potential consisting of two ( A and B) components attributed to axonal firing of local interneurons, whereas mammillary stimulation elicits, in addition to the A-B sequence, an earlier component ( a) presumably generated by presynaptic dendrites in thalamic glomeruli. In the present study, short pulse-trains applied to the laterodorsal tegmental nucleus diminished the amplitudes of A and B inhibitory components or completely suppressed them. The B component was more sensitive to the depressive effect. By contrast with the changes of the A and B components, the mammillary-evoked a inhibitory component was not reduced and, in many instances, was enhanced following laterodorsal tegmental stimulation. The effects of laterodorsal tegmental stimulation survived monoamine depletion by reserpine. We suggest that mesopontine cholinergic depressive actions on A and B inhibitory postsynaptic potentials may be due to an increased conductance in thalamocortical cells during the short-lasting nicotinic action combined with a somatic hyperpolarization of local-circuit cells, whereas the enhancement of the earliest ( a) inhibitory postsynaptic potential reflects a concomitant potentiating action at the level of intraglomerular presynaptic dendrites.

Three types of inhibitory postsynaptic potentials generated by interneurons in the anterior thalamic complex of cat.

1. These experiments were carried out to study how thalamic interneurons generate inhibitory postsynaptic potentials (IPSPs) in relay cells. Intracellular recordings were performed in the anterior thalamic (AT) nuclei, a nuclear group in which interneurons constitute the only intrathalamic source of gamma-aminobutyric acid (GABA). 2. In the AT complex, as in most dorsal thalamic nuclei, interneurons can influence relay cells through their presynaptic dendrites (PSDs) and their axons. This dual mode of action is paralleled by a different termination pattern of prethalamic fibers and cortical axons on interneurons. Prethalamic fibers, which in the AT nuclei arise in the mammillary bodies (MBs), end mostly on PSDs, whereas cortical terminals usually synapse on the parent dendrites of PSDs. We therefore took advantage of the differential mode of termination of cortical and MB afferents on interneurons to infer the respective roles of the axons and PSDs of interneurons in the genesis of the IPSPs recorded from relay cells. 3. In all responsive AT cells, cortical stimuli delivered at low frequency (less than or equal to 0.5 Hz) evoked a biphasic IPSP, with an early and a late phase, having a total duration of 221.96 +/- 8.18 ms (mean +/- SE). The early part of the IPSP (termed A) had a reversal potential (ER) close to the equilibrium potential for Cl- ions: -79.25 +/- 2.14 mV. Furthermore, it reversed in polarity after impalement of the cells with KCl-filled pipettes. The late IPSP (termed B) always began before the end of the early IPSP, 45.93 +/- 2.50 ms after the onset of the A-IPSP. The B-IPSP had an ER of -109 +/- 2.4 mV and was not affected by Cl- injection. 4. By contrast, MB stimuli delivered at low frequency (less than or equal to 0.5 Hz) evoked a triphasic IPSP having a total duration of 220.5 +/- 9.42 ms in most (61.2%) AT cells. The IPSP with the shortest latency (termed a) was evoked only by MB stimuli. Before the return of the membrane potential to the resting level, a second hyperpolarizing potential began (7.41 +/- 0.46 ms after the onset of the a-IPSP). This second inhibitory phase was biphasic and had electrophysiological characteristics similar to the biphasic A- and B-IPSP evoked by cortical stimulation. Both the MB-evoked a- and A-IPSPs had an ER close to the equilibrium potential for Cl- ions (-72.22 +/- 0.68 and -72 +/- 0.82 mV, respectively) and reversed in polarity after impalement of the cells with KCl-filled pipettes.(ABSTRACT TRUNCATED AT 400 WORDS)

Cellular physiology of the turtle visual cortex: synaptic properties and intrinsic circuitry

We have examined the synaptic physiology of the isolated dorsal cortex of the turtle, Pseudemys scripta elegans. Electrical stimulation of afferent pathways elicited distinct, stereotyped responses in pyramidal and stellate neurons. Single shocks evoked a long-lasting barrage of excitatory postsynaptic potentials (EPSPs) in stellate cells, and led to a burst of several action potentials. Under the same circumstances, pyramidal cells displayed a small amount of short-latency excitation, but this was accompanied by a profound and prolonged set of inhibitory post-synaptic potentials (IPSPs). Synaptic excitation of the distal dendrites of pyramidal cells could evoke dendritic action potentials that were visible at the soma as small all-or-none spikes rising from the hyperpolarized level of the IPSP. There appeared to be two mechanistically different types of IPSPs in pyramidal cells. The first occurred at short latency, could produce a very large conductance increase, reversed polarity at -71 mV, and was chloride-dependent. The second was generally smaller and more protracted, had a relatively negative reversal potential of -85 to -95 mV, and was insensitive to chloride injection. Focal application of small doses of the putative inhibitory neurotransmitter gamma-aminobutyric acid (GABA) onto the somata of pyramidal cells caused a conductance increase and hyperpolarization. This response had features in common with the short-latency IPSP, including an identical reversal potential. Application of large doses of GABA to the somata of pyramidal cells or smaller doses to their dendrites elicited multiphasic or purely depolarizing responses that were at least partly due to time- or space-dependent shifts of the equilibrium potential of the response. Bicuculline methiodide, a potent GABA antagonist, depressed both the responses to GABA and the short-latency IPSP, but not the long-latency IPSP; synchronized epileptiform burst discharges also resulted. These findings, together with responses to locally applied electric shocks and the excitatory amino acid glutamate, suggested that inhibition of pyramidal cells was generated intrinsically by stellate cells, and that the cortical circuit provides pathways for both feedforward and feedback GABAergic inhibition. The data also suggest that pyramidal cells are mutually excitatory. These features are similar to the basic intrinsic circuitry in the telencephalic cortices of mammals.

Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system.

Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system.

Inhibitory processes and interneuronal apparatus in motor cortex during sleep and waking. II. Recurrent and afferent inhibition of pyramidal tract neurons.

Inhibitory processes and interneuronal apparatus in motor cortex during sleep and waking. II. Recurrent and afferent inhibition of pyramidal tract neurons.M Steriade, and M DeschênesM Steriade, and M DeschênesPublished Online:01 Sep 1974https://doi.org/10.1152/jn.1974.37.5.1093MoreSectionsPDF (3 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Download PDF FiguresReferencesRelatedInformation Cited ByNeocortical cell classes are flexible entities1 February 2004 | Nature Reviews Neuroscience, Vol. 5, No. 2High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidationActive sleep-related depolarization of feline trigemino-thalamic afferent terminalsNeuroReport, Vol. 9, No. 4Various types of inhibitory postsynaptic potentials in anterior thalamic cells are differentially altered by stimulation of laterodorsal tegmental cholinergic nucleusNeuroscience, Vol. 47, No. 2Influence of stimulus repetition rate on cortical somatosensory potentials evoked by median nerve stimulation: Implications for generation mechanismsJournal of the Neurological Sciences, Vol. 105, No. 1Properties of associative long-lasting potentiation induced by cellular conditioning in the motor cortex of conscious catsNeuroscience, Vol. 42, No. 2Participation of cortical recurrent inhibition in the genesis of spike and wave discharges in feline generalized penicillin epilepsyBrain Research, Vol. 267, No. 1Reticular influences on primary and augmenting responses in the somatosensory cortexBrain Research, Vol. 205, No. 1Epileptic and normal neurons in monkey neocortex: A quantitative study of degree of operant controlBrain Research, Vol. 151, No. 2Firing rates and patterns of output and nonoutput cells in cortical areas 5 and 7 of cat during the sleep-waking cycleExperimental Neurology, Vol. 60, No. 3Reticular influences on lateralis posterior thalamic neuronsBrain Research, Vol. 131, No. 1Afferent and recurrent collateral influences on cortical somatosensory neuronsExperimental Neurology, Vol. 56, No. 2Reticular suppression of flash-evoked IPSPs in visual cortex neuronsBrain Research, Vol. 111, No. 1Firing patterns of epileptic and normal neurons in the chronic alumina focus in undrugged monkeys during different behavioral statesBrain Research, Vol. 98, No. 1 More from this issue > Volume 37Issue 5September 1974Pages 1093-113 https://doi.org/10.1152/jn.1974.37.5.1093PubMed4370113History Published online 1 September 1974 Published in print 1 September 1974 Metrics

Electrotonically Coupled Interneurones produce Two Types of Inhibition in Aplysia Neurones

IN the abdominal ganglion of Aplysia californica, there are two types of inhibitory post-synaptic potentials (IPSPs). There are unitary short-lasting IPSPs which occur as the result of conductance changes during the movement of Cl− across the synaptic membrane—IPSPs which have definite equilibrium potentials and characteristics similar to those described for other neuronal systems1—and there are IPSPs which last much longer and may be much more effective in regulating the activity of the neurone, which Taue has called “inhibitions of long duration” (ILD)2,3. In Aplysia some of these long lasting inhibitory potentials are produced by conductance changes and have definite equilibrium potentials4. Long lasting inhibitions or “slow inhibitory potentials” as well as short lasting IPSPs have also been described in vertebrate sympathetic ganglia5, but in these, long lasting IPSPs are not accompanied by changes in membrane conductance. Some of the long lasting inhibitions (LLI) have been explained on the basis of an ATP-dependent electrogenic Na+ pump6. Presumably this ATP-dependent pump hyperpolarizes the membrane by causing an outflux of Na+ from the cell which is more rapid than the corresponding “active” influx of K+7. There is evidence now for the existence of such an electrogenic Na+ pump in some of the identified neurones of the abdominal ganglion of Aplysia californica8. Pinsker and Kandel9 have found some evidence that in these neurones the electrogenic Na+ pump is activated by the synaptic action of an identified cholinergic inhibitory interneurone, L10, producing the long lasting “late IPSP”. But Kehoe and Ascher10, although agreeing that the same interneurone (L10) produces both types of IPSPs in the follower neurones, have shown that the “late IPSP”9 is due to an increase in the K+ conductance and that it has an equilibrium potential around −90 mV. I have found that in this abdominal ganglion there is another specific interneurone which is electrotonically coupled to L10 and which, when activated, produces a long lasting inhibition (LLI) in a number of follower neurones. Thus L10 produces the LLI or “late IPSP” in some follower neurones not directly, but through the mediation of another interneurone.

Spatial synaptic distribution of recurrent and group Ia inhibitory systems in cat spinal motoneurones.

1. The reversal potentials of several types of inhibitory post-synaptic potentials (IPSPs) have been studied in cat spinal motoneurones with and without modification of intracellular chloride ion (Cl(-)) concentration. Single barrel intracellular micropipette electrodes have been used.2. When studied with potassium citrate filled micropipettes, the reversal potential for IPSPs evoked by stimulation of antagonist group Ia afferents is the same as that for recurrent IPSPs evoked by antidromic stimulation of motoneurone axon collaterals, confirming earlier observations (Araki, Ito & Oscarsson, 1961; Coombs, Eccles & Fatt, 1955).3. Studied with potassium chloride filled micropipettes. the reversal potential for the group Ia IPSP was found to be different from that for the recurrent IPSP when the amount of Cl(-) diffusing or iontophoretically injected into the motoneurone was small. The amount of difference in reversal potential varied from cell to cell but when present the group Ia IPSP reversed to a depolarizing potential more readily than the recurrent IPSP in all cases.4. Interaction between recurrent IPSPs and monosynaptic excitatory post-synaptic potentials (EPSPs) was also studied and the amount of non-linearity of potential summation was measured.5. The results are consistent with the hypothesis that the terminations of Renshaw cells responsible for the recurrent IPSP are located largely on the proximal dendrites of motoneurones, while the terminations of the interneurones generating the group Ia IPSP appear to be closer to or on the cell somata.

Anatomical considerations on monosynaptic reflex arcs.

Anatomical considerations on monosynaptic reflex arcs.