Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta

Intracellular recordings were made from the major neurites of local interneurons in the moth antennal lobe. Antennal nerve stimulation evoked 3 patterns of postsynaptic activity: (i) a short-latency compound excitatory postsynaptic potential that, based on electrical stimulation of the antennal nerve and stimulation of the antenna with odors, represents a monosynaptic input from olfactory afferent axons (71 out of 86 neurons), (ii) a delayed activation of firing in response to both electrical- and odor-driven input (11 neurons), and (iii) a delayed membrane hyperpolarization in response to antennal nerve input (4 neurons).Simultaneous intracellular recordings from a local interneuron with short-latency responses and a projection (output) neuron revealed unidirectional synaptic interactions between these two cell types. In 20% of the 30 pairs studied, spontaneous and current-induced spiking activity in a local interneuron correlated with hyperpolarization and suppression of firing in a projection neuron. No evidence for recurrent or feedback inhibition of projection neurons was found. Furthermore, suppression of firing in an inhibitory local interneuron led to an increase in firing in the normally quiescent projection neuron, suggesting that a disinhibitory pathway may mediate excitation in projection neurons. This is the first direct evidence of an inhibitory role for local interneurons in olfactory information processing in insects. Through different types of multisynaptic interactions with projection neurons, local interneurons help to generate and shape the output from olfactory glomeruli in the antennal lobe.Abbreviations AL antennal lobe - EPSP excitatory postsynaptic potential - GABA -aminobutyric acid - IPSP inhibitory postsynaptic potential - LN local interneuron - MGC macroglomerular complex - OB olfactory bulb - PN projection neuron - TES N-tris[hydroxymethyl]methyl-2-aminoethane-sulfonic acid     

Corticofugal postsynaptic influences on red nucleus neurons

The responses of red nucleus neurons to stimulation of the sensorimotor cortex was studied on nembutal-anesthetized cats. Most of the rubrospinal neurons were identified according to their antidromic activation. Stimulation of the sensorimotor cortex was shown to evoke in the red nucleus neurons monosynaptic excitatory potentials with a latency of 1.85 msec, polysynaptic excitatory potentials (EPSP), and inhibitory postsynaptic potentials (IPSP) with a latency of 9–24 msec. The EPSP often produced spikes. The probability of generation of spreading excitation is greater with motor cortex stimulation. The monosynaptic EPSP are assumed to arise under the influence of the impulses arriving over the corticorubral neurons as a result of excitation of axodendritic synapses. The radial type of branching of red nucleus neurons facilitates the transition from electrotonically spreading local depolarization to an action potential triggered by the initial axonal segment. Polysynaptic EPSP and IPSP seem to be a result of activation of fast pyramidal neurons whose axon collaterals are connected via interneurons with the soma of the red nucleus neurons.L. A. Orbeli Institute of Physiology of the Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 3, No. 1, pp. 43–51, January–February, 1971.     

Rubrospinal synaptic influences on the lumbar motoneurons of the rat

Intracellular recording was employed in experiments on rats with the nervous system intact and after acute pyramidotomy to study the postsynaptic effects produced in the lumbar motoneurons on stimulation of the nucleus ruber. Stimulation of this nucleus with single stimuli and with a short series of stimuli caused excitatory and inhibitory postsynaptic potentials (EPSP and IPSP) to develop in the motoneurons. Most of the EPSP recorded were disynaptic, but response development involved a monosynaptic segmental delay in five of the 124 cells that exhibited EPSP. A capacity for high-frequency potentiation was a characteristic feature of the disynaptic excitatory and inhibitory effects. Transmembrane polarization of the motoneurons had a marked influence on the amplitude of the disynaptic EPSP and IPSP. The properties of the disynaptic rubrospinal influences were similar to those described for the cat.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 3, No. 3, pp. 266–273, May–June, 1971.     

Effects of ketamine on neuronal epileptiform responses in the cat neocortex

The effects of ketamine, an antagonist of NMDA receptors, on the neuronal epileptiform responses evoked by applications of strychnine, penicillin, or bicuculline to the suprasylvian gyrus were studied in cats. Ketamine either exerted no effect, or slightly decreased interictal high-amplitude depolarizing shifts of the membrane potential and depolarizing afterpotentials, which appeared spontaneously or were evoked by intracortical stimulation. Repetitive electrical stimulation of the epileptogenic cortical regions resulted in the appearance of autogenerated ictal activity lasting up to several tens of seconds; this activity was produced against the background of a depolarization of neuronal membranes. After ketamine injections, such stimulations evoked no ictal activity in the neurons, or the discharges became much shorter. The results of our study show that the NMDA-dependent postsynaptic components play a more important role in the development of neocortical ictal activity compared with the interictal activity.Neirofiziologiya/Neurophysiology, Vol. 27, No. 1, pp. 32–35, January–February, 1995.     

Protracted depolarizing potentials of neurons in a strychninized cortical slab isolated from the cat

Neuronal response in a cortical slab isolated from the cat during surface application of strychnine was investigated in experiments on immobilized unanesthetized animals by means of intracellular recording techniques. Protracted depolarizing potentials (PDP) were found to occur spontaneously and in response to a single intracortical electrical stimulus in a proportion of the neurons. These potentials could be triggered by transformation of response along the lines of "paroxysmal depolarizing shift" (PDS) — hyperpolarization, with hyperpolarization replaced by depolarizing potentials. A further increase in depolarizing after-potentials resulted in the generation of PDP. These changes were normally accompanied by enhanced summated epileptiform activity in the isolated cortical slab. It is postulated that PDP were triggered by increased calcium conductance at the neuronal membrane during intensification of paroxysmal response in the isolated cortical slab.I. I. Mechnikov University, Odessa. Translated from Neirofiziologiya, Vol. 22, No. 1, pp. 19–23, January–February, 1990.     

Postsynaptic components of paroxysmal neuronal response in the strychninized neocortex

Neuronal response in the strychninized cortical suprasylvian gyrus was investigated in experiments on immobilized and unanesthetized cats using intracellular techniques. Paroxysmal depolarizing shifts (PDS) in neuronal membrane potential were recorded, consisting of a bursting discharge and slow depolarization wave. It was found when using intracortical stimulation that PDS can accumulate and change in shape and size. Bursting discharges in PDS were induced by large-scale EPSP which could be distinguished from paroxysmal response. Data from presumably intradendritic readings demonstrated the presence of large-scale EPSP during the generation of epileptiform discharges in the cortex. In a proportion of cells, PDS were accompanied by hyperpolarizing potentials — apparently IPSP, since they undergo reversal with intercellular administration of Cl^–. The contribution of excitatory and inhibitory synaptic influences to paroxysmal neuronal response is discussed.I. I. Mechnikov State University, Odessa. Translated from Neirofiologiya, Vol. 22, No. 5, pp. 642–649, September–October, 1990.     

Effect of direct and transcallosal stimulation on inhibition of unit activity in the cat association cortex

Inhibition of association cortical neurons (in the form of inhibition of spontaneous activity or of IPSPs) during direct and transcallosal stimulation was studied in cats immobilized with muscle relaxants. The duration of inhibition of stimulation and the number of stimuli. With an increase in the strength of stimulation inhibition deepened to a certain level for a particular neuron, after which it could be further lengthened with an increase in the number of stimuli. In the case of repeated stimulation by volleys of stimuli, very prolonged inhibition developed gradually in the neurons, during which spontaneous activity was inhibited for 2–5 sec. The duration of the IPSP depended on the intensity of stimulation and number of stimuli and its amplitude depended on the intensity and frequency of stimulation and on the number of stimuli. In some cases the amplitude of the IPSP continued to rise after a short volley of stimuli, even after the end of stimulation. An increase in the number of stimuli in the volley lengthened the IPSPs, but their amplitude remained constant throughout the period of stimulation. Prolonged inhibition (up to a few seconds) was connected with the development of a hyperpolarization postsynaptic potential in the neurons. It is suggested that neurons exerting a monosynaptic inhibitory influence on cells of the association cortex may be located in the opposite hemisphere.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 13, No. 2, pp. 133–141, March–April, 1981.     

Post-tetanic changes in intracellular response to direct cortical stimulation

Changes in responses to single stimulations of the cortical surface after tetanization (frequency 50/sec, duration 1–10 sec) were studied in sensorimotor cortical neurons of an unanesthetized rabbit on intracellular and "quasiintracellular" recordings. After tetanization insufficient to generate epileptiform after-discharges, an increase was observed in the amplitude and duration of exciting postsynaptic potentials (EPSP) induced by a single test stimulus. This increase is considered as post-tetanic potentiation (PTP). Its duration did not exceed 1 min. The amplitude of inhibitory postsynaptic potentials (IPSP) showed a considerably smaller increase or did not change or even decreased. The PTP increased with an increase in the strength and duration of the tetanization, reaching especially high values during tetanization sufficiently intensive to evoke epileptiform after-discharges. In this case the response to a single test stimulus was identical to an epileptiform intracellular discharge. The data obtained confirm the important role of PTP of the exciting synapses in the generation of epileptiform after-discharges. A simple model of a neuron network with exciting and inhibiting feedbacks which accounts for the generation of epileptiform activity is examined.Institute of the Brain, Academy of Medical Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 2, No. 6, pp. 601–610, November–December, 1970.     

Neuronal response in a strychninized cortical slab isolated from the cat

Intracellular response in neurons and glial cells of an isolated cortical slab to direct electrical stimulation of the slab following surface application of strychnine was investigated during experiments on immobilized unanesthetized cats. Strychnine induced single epileptiform discharges and after-discharges in the slab and in the neurons it contained in the form of large-scale paroxysmal depolarization shifts (PDS) in membrane potential (MP). Spontaneous summated epileptiform discharges and neuronal activity in the units examined were not very synchronized. Electrical stimulation induced generalized paroxysmal activity in the isolated slab. Neuronal PDS were accompanied by refractory periods, onset of which did not depend on MP level. Strychnine increased the number of neurons manifesting background activity in which action potentials were generated by rhythmic depolarizing MP waves of extrasynaptic origin. Epileptiform response in strychninized cortical isolated slabs to presentation of single stimuli is accompanied by major depolarization shifts in the MP of glial cells. Paroxysmal excitation is thought to be triggered in strychninized isolated cortical slabs by extrasynaptic factors and closely linked to altered concentration of extracellular potassium.I. I. Mechnikov University, Odessa. Translated from Neirofiziologiya, Vol. 22, No. 1, pp. 23–29, January–February, 1990.     

Postsynaptic neuronal response of a cat sensorimotor cortex during evoked and self-sustained rhythmic "spike and wave" activity

Intracellular correlates of complex sets of rhythmic cortical "spike and wave" potentials evoked in sensorimotor cortex and of self-sustained rhythmic "spike and wave" activity were examined during acute experiments on cats immobilized by myorelaxants. Rhythmic spike-wave activity was produced by stimulating the thalamic relay (ventroposterolateral) nucleus (VPLN) at the rate of 3 Hz; self-sustained afterdischarges were recorded following 8–14 Hz stimulation of the same nucleus. Components of the spike and wave afterdischarge mainly correspond to the paroxysmal depolarizing shifts of the membrane potential of cortical neurons in length. After cessation of self-sustained spike and wave activity, prolonged hyperpolarization accompanied by inhibition of spike discharges and subsequent reinstatement of background activity was observed in cortical neurons. It is postulated that the negative slow wave of induced spike and wave activity as well as slow negative potentials of direct cortical and primary response reflect IPSP in more deep-lying areas of the cell bodies, while the wave of self-sustained rhythmic activity is due to paroxysmal depolarizing shifts in the membrane potential of cortical neurons.I. S. Beritashvili Institute of Physiology, Academy of Sciences of the Georgian SSR, Tbilisi. Translated from Neirofiziologiya, Vol. 18, No. 3, pp. 298–306, May–June, 1986.     

Ephaptic feedback in identified synapses of terrestrial snails

A hypothesis for the existence of the intrasynaptic ephaptic feedback (EFB) in the invertebrate central nervous sytem was tested. Excitatory postsynaptic potentials (EPSPs) and currents (EPSCs) evoked by the activation of the recently described monosynaptic connection between the identified snail neurons were recorded intracellularly. In case of the EFB presence, the postsynaptic tetanization with hyperpolarization pulses could activate presynaptic Ca2+ channels and enhance the EPSP amplitude, whereas a steady postsynaptic hyperpolarization should induce a "supralinear" increase in EPSC amplitudes as it has been found in the rat hippocampus. In the first series of the experiments, 10 trains of hyperpolarizing pulses (40-50 mV, 1 Hz, pulse duration 0.5 s, train duration 45 s) were delivered postsynaptically. No significant changes in EPSP amplitudes were found. In the second series of the experiments, the EPSC amplitudes were measured during varying postsynaptic hyperpolarization. At the membrane potential 100 mV, the EPSP amplitude was significantly higher than theoretically predicted from the classical linear dependence. Such a "supralinear" effect of postsynaptic depolarization can be explained by the presence of the EFB. This finding is the first evidence for the EFB existence in the invertebrate central nervous system.     

Origin of slow negative potential of direct cortical response in cats

To investigate mechanisms of formation of the electrocorticographic slow negative potential (SNP) evoked by direct electrical stimulation of the cortical surface, poststimulus single unit activity in the stimulated area was studied in anesthetized cats and changes in SNP in the depth of the cortex were analyzed. The results showed that membrane hyperpolarization, accompanied by cessation of action potential generation, develops parallel with SNP in neuron bodies in the stimulated area. Investigation of the nature of this hyperpolarization showed that during its development excitability of the neuron and resistance of the postsynaptic membrane fall. It is concluded from the results that this membrane hyperpolarization is an indicator of IPSP development in the neuron bodies. The results of laminar recording showed that SNP may diminish or even disappear in the depth of the cortex without subsequent reversal. Determination of dipoles formed along an axis perpendicular to the cortical surface showed that SNP has one source and two sinks, which are located symmetrically relative to it. The presence of two symmetrical sinks must indicate an active source, formed as a result of hyperpolarization of the neuron membrane. On the basis of the results SNP can be regarded as a field potential formed on the cortical surface as a result of IPSP development in the neuron bodies.Institute of Clinical and Experimental Neurology, Ministry of Health of the Georgian SSR, Tbilisi. Translated from Neirofiziologiya, Vol. 15, No. 3, pp. 314–320, May–June, 1983.     

Monosynaptic excitory postsynaptic potentials in thoracic motoneurons under reticulospinal influences

We studied synaptic processes in motoneurons of thoracic segments (T_IX-T_XI) evoked by stimulation of the medial area of the giant-cell reticular nucleus in decerebrated cats. Monosynaptic EPSP were recorded in the majority of investigated motoneurons upon activation of the most rapidly conducting reticulospinal fibers. In some cells, such monosynaptic EPSP were accompanied by late EPSP or IPSP. Amplitude of monosynaptic EPSP attained 5 mV, but this value usually was insufficient for development of an action potential. Upon summation of single monosynaptic EPSP, the membrane potential reached the critical level and an action potential arose in the motoneuron. The efficiency of summary processes evoked by stimulation of the reticular formation exceeded the intensity of synaptic processes that arise in thoracic motoneurons on stimulating the nucleus of Deiters. Functional characteristics of reticular and vestibular monosynaptic EPSP are discussed in the work.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 1, No. 3, pp. 243–252, November–December, 1969.     

Aspects of excitation and inhibition produced in parietal association cortex neurons by stimulating thalamic association nuclei

Neuronal response to single stimuli applied to the thalamic dorsolateral and posterolateral nuclei (DLN and PLN resepctively) was investigated in the parietal association cortex. Primary IPSP following DLN and PLN stimulation was noted in 62.5% and 79.6% of instances respectively. Latencies of EPSP and IPSP when stimulating the two nuclei were longer for the DLN. The amplitude of EPSP evoked by stimulating association nuclei rose and declined smoothly, while that of IPSP showed a fast rise and a more steady decline. The EPSP appearing during the evolution of IPSP were of higher amplitude than control level of resting potential. Both amplitude and duration of IPSP induced in a single unit by stimulating different association nuclei were extremely similar, thus confirming the involvement in this operation of the same inhibitory cortical interneurons. Duration of IPSP was shorter than that of inhibitory background spike activity. It is postulated that the discrepancy in duration can largely be ascribed to properties of the neurons themselves.State University, Odessa. Translated from Neirofiziologiya, Vol. 23, No. 5, pp. 529–536, September–October, 1991.     

Electrical characteristics of granule cells of the carp olfactory bulb

Intracellular responses of granule cells and secondary neurons of the carp olfactory bulb to electrical stimulation of the olfactory nerve and olfactory tract were investigated. Synaptic responses of granule cells to both types of stimuli consisted of an early and late EPSP and IPSP. Comparison of responses of the secondary and granule neurons indicated that the granule cells are interneurons of postsynaptic inhibition of secondary neurons. The results suggest that dendro-dendritic and recurrent collateral pathways exist for the activation of granule cells and that inhibitory synapses are located on those dendrites of the secondary neurons that are in contact with endings of olfactory nerve fibers.M. V. Lomonosov State University, Moscow. Translated from Neirofiziologiya, Vol. 7, No. 6, pp. 597–602, November–December, 1975.     

Responses of neurons in the vibrissae projection area of the cat somatosensory cortex to afferent activation

Responses of 375 primary somatosensory cortical neurons located in the projection area of the vibrissae to electrical stimulation of the infraorbital nerve and also to adequate stimulation of the vibrissae were investigated in unanesthetized cats immobilized with tubocurarine. Stimulation of the nerve and vibrissae most frequently evoked synaptic responses in the neurons, in the form of a short EPSP followed by an IPSP or, less frequently, as a primary IPSP; during extracellular recordings corresponding changes were observed in spike activity. In response to stimulation of the vibrissae, initial inhibition was found more often than to stimulation of the nerve (in 45 and 16% of neurons respectively). The difference between the minimal values of latent periods of IPSP and EPSP evoked by stimulation of the infraorbital nerve was 0.8 msec in different neurons, and the difference between the mean values 1.4 msec. Directional sensitivity of the cortical neurons was demonstrated (to a change in the direction of deflection of the vibrissae). Neurons located close together could differ in the character of their directional sensitivity during stimulation of the same vibrissae. It is concluded that short-latency inhibition arising in the primary projection area of the cat somatosensory cortex is predominantly afferent and not recurrent. The probable mechanisms of directional sensitivity of the neurons studied are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSSR, Kiev. Translated from Neirofiziologia, Vol. 11, No. 6, pp. 550–559, November, 1979.     

Inhibition in hippocampal pyramidal neurons during peripheral stimulation

Responses of hippocampal pyramidal neurons were investigated intracellularly in unanesthetized rabbits immobilized with tubocurarine. A single stimulus, applied to the sciatic nerve, evoked prolonged (up to 2.5 sec) hyperpolarization of the cell membrane, accompanied by inhibition of action potentials. The latent period of the evoked hyperpolarization was 48±16.4 msec, and its amplitude 2.5±1.9 mV. In some neurons the development of hyperpolarization potentials was preceded by excitation. The suggestion is made that hyperpolarization of the membrane of pyramidal cells during peripheral stimulation is manifested as an inhibitory postsynaptic potential (IPSP), generated with the participation of hippocampal interneurons. The possibility of prolonged tonic action of interneurons from outside as a cause of prolonged inhibition of the pyramidal neurons is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 1, No. 3, pp. 278–284, November–December, 1969.     

Postsynaptic potentials of neurons of the cat auditory cortex

The electrical reactions of 294 neurons of the auditory cortex to a click were recorded in experiments on cats immobilized with tubocurarine (174 intra- and 120 extracellularly). The value of the membrane potential varied from 30 to 70 mV with intracellular leads. The following types of reactions were obtained (the number of neurons is given in parentheses): a peak without slow oscillations in the membrane potential (4), EPSP (3), EPSP-peak (6), EPSP-peak-IPSP (17), EPSP-IPSP (9), primary IPSP (114, including 23 with an after-discharge). Twenty one neurons did not react to a click. The amplitude of the sub-threshold EPSP was 1–1.5 mV, the duration of the ascending part was about 10 and of the descending part 20–30 msec. The peak potential on the ascending part of the EPSP developed at the critical level of 3–4 mV. The amplitude of the peaks varied from several millivolts to 50–60. In 17 neurons prolonged hyperpolarization having all the properties of an IPSP, developed after the peak. The amplitude of these IPSP varied in different neurons from 1 to 10 mV and the duration varied from 20 to 80 msec. IPSP without preceding excitation of the given neuron were the predominant types of reaction. The latent period of these primary IPSP varied from 7 to 20 msec and the amplitude from 1 to 15 msec with a duration of 30–200, more frequently 80–100 msec. It is suggested that two types of inhibition develop in neurons of the auditory cortex in response to a click: recurrent and afferent. The functional significance of the first consists in limiting the duration of the discharge in the reacting neurons, the second prevents the development of excitation in adjacent neurons, thereby limiting the area of neuronal activity.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSSR, Kiev. Translated from Neirofiziologiya, Vol. 3, No. 4, pp. 339–349, July–August, 1971.     

Mechanisms of epileptogenic effects of some convulsants on the neuronal activity in the neocortex

The data obtained in the studies of neurophysiological aspects of epileptogenesis in the brain cortex, which have been carried out in our laboratory for many years, are used for the analysis of epileptogenic effects of a few convulsants (penicillin, strychnine, and d-tubocurarine) on the activity of neocortical neurons. It has been demonstrated that the development of the epileptiform activity in the cortex is accompanied by suppression of IPSP, and the above convulsants directly influence the mechanisms of postsynaptic inhibition. Epileptogenic effects of strychine and penicillin are based on blocking of chloride ion channels and depend on the direction of chloride currents. The role of excitatory and inhibitory synaptic interactions among neurons in generation of the epileptiform activity is discussed.     

Reticulospinal and vestibulospinal synaptic effects on the lumbar motor neurons of the monkey

It was established in experiments on rhesus monkeys by intracellular recording and computer averaging that fast-conducting reticulo- and vestibulospinal fibers form monosynaptic excitatory links with lumbar alpha-motor neurons. The monosynaptic bulbospinal effects are retained after sectioning of the pyramids or after chronic destruction of the motor cortex. The mean amplitude of the reticulomotor neuronal EPSP is less than that of the corticomotor neuronal EPSP, however, the mean amplitudes of the EPSP of individual motor neurons can reach similar values. In contrast to the corticomotor neuronal projections, the bulbomotor neuronal projections are directed primarily toward the motor neurons of the proximal muscles. In addition to monosynaptic EPSP, reticulo- and vestibulospinal impulses evoke disynaptic EPSP and IPSP in the lumbar motor neurons of monkeys which are very similar to the disynaptic effects found in subprimates.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 3, No. 4, pp. 408–417, July–August, 1971.