Role of cortical inhibition in heterosensory interaction of neurons of the cat sensorimotor cortex

Background and evoked neuronal activity in the cat sensorimotor cortex was recorded under a-chloralose anesthesia. Pairs of heterogeneous stimuli were applied, spaced at intervals of 0, 100, 200, 300, and 400 msec. A clicking sound, flashing light, and electroshock to the contralateral forepaw were used as stimuli. Partial or complete blockade of response to test stimuli presentations spaced 100–200 msec apart were observed when using stimulation of varying modality. The greatest test response was recorded at interstimulus intervals of 200–300 msec. Intracellular mechanisms of heterosensory interaction were investigated by applying the inhibitory transmitter antagonist picrotoxin microiontophoretically to the test cell to produce local attenuation of inhibitory effects. This substance also reduced the duration of blockage following the conditioning stimulus and the occurrence of peak level test response at a lower interstimulus interval than in the controls. Either a consistent increase in the number of spikes per response at one of the interstimulus intervals or a uniform reinforcement in unit response to several different interstimulus intervals were observed in a proportion of the cells. The contribution of intracortical inhibitory influences to the mechanisms of heterosensory interaction on neurons of the cat sensorimotor cortex is discussed in the light of our findings.A. A. Ukhtomskii Institute of Physiology, A. A. Zhdanov State University, Leningrad. Translated from Neirofiziologiya, Vol. 19, No. 2, pp. 147–156, March–April, 1987.     

Reflection of temporal parameters of an optical stimulus in unitary responses of the sensomotor and visual cortex in cats

Unit activity in the visual (area 17) and sensomotor (areas 4 and 6) cortex in response to an optical stimulus up to 1000 msec in duration was investigated by extracellular recording in acute experiments on cats anesthetized with chloralose (70 mg/kg body weight). Comparative analysis of the types of unitary responses and the durations of the intervals of functional changes showed that: 1) The number of neurons generating on-off responses was about 25% in the visual cortex and 100% in the sensomotor cortex; 2) the intervals of functional changes of the neurons were equal in length to the time intervals of on-off discharges; 3) together with a single time range (200–500 msec), for each area studied specific ranges also exist: from 0 to 200 msec for the visual cortex and from 500 msec and more for the sensomotor cortex; 4) the latent period of after-discharge is equal to the duration of the intervals of functional changes. The results were analyzed from the standpoint of reflection of temporal parameters of optical stimuli by neurons of the sensomotor cortex.A. A. Zhdanov Leningrad State University. Translated from Neirofiziologiya, Vol. 7, No. 4, pp. 365–371, July–August, 1975.     

Effect of intracortical chemical stimulation on spontaneous sensomotor cortical unit activity in cats

The effect of microelectrophoresis of glutamate on spontaneous activity of sensomotor cortical neurons located 80–250 µ from the point of application of glutamate was studied in cats anesthetized with pentobarbital. If glutamate was applied at distances of under 100 µ from the neurons the predominant response was one of excitation, evidently due to the direct action of the excitatory mediator. With more distant application inhibition of spontaneous activity predominated: at distances from 100 to 200 µ it was observed in 57%, and between 200 and 250 µ, in 70% of cases. Application of picrotoxin close to the neuron weakened inhibition induced by microelectrophoresis of glutamate through a neighboring microelectrode.A. A. Ukhtomskii Physiological Research Institute, A. A. Zhdanov Leningrad State University. Translated from Neirofiziologiya, Vol. 14, No. 4, pp. 347–352, July–August, 1982.     

Characteristics of inhibition in the kitten sensory-motor cortex

Responses of 340 neurons of the sensory-motor cortex to electric shocks applied to the limbs were investigated in kittens aged 3–30 days. In 9.4% of cells of kittens aged 3–10 days and in 17.1% of cells in kittens aged 21–30 days pauses were observed immediately after the excitatory component of the extracellular response. Intra- and quasiintracellular recording showed that postsynaptic inhibition participates in the genesis of these pauses. The IPSPs which, as a rule, followed the excitatory component of the response were of much longer duration (up to 250–380 msec) than the analogous IPSPs in the sensory-motor cortex of adult cats. Usually the amplitude of the IPSP in kittens did not exceed 5 mV.A. A. Zhdanov Leningrad State University. Translated from Neirofiziologiya, Vol. 9, No. 3, pp. 227–231, May–June, 1977.     

Conditions of appearance of off responses of sensomotor cortical neurons to photic stimulation in cats

In acute experiments on cats under chloralose anesthesia (70 mg/kg) unit activity was recorded extra- and intracellularly in the sensomotor cortex (areas 4 and 6) during prolonged (up to 1000 msec) photic stimulation. Responses of on-off type were generated by 100% of neurons tested to photic stimuli whose duration corresponded to the recovery cycle of functional changes after a single flash, determined by the paired stimulation method. Cutaneous stimulation affected the appearance of the photic off response if it led to a spike discharge of the neuron before the off response. It is suggested that IPSPs of cortical neurons largely determine both the duration of the cycle of functional recovery after a single flash and also differences in the pattern of generation of the off response and its interaction with responses to cutaneous stimulation.A. A. Zhdanov Leningrad State University. Translated from Neirofiziologiya, Vol. 9, No. 4, pp. 355–360, July–August, 1977.     

Influence of afferent impulses from the nerves of the anterior limbs on the insertion neurons of the lumbar section of the spinal cord

In anesthetized cats in conditions of muscular relaxation we have studied the participation of the interneurons of the lumbar section of the spinal cord in the interaction of the FRA systems of the fore and hind limbs. Using microelectrodes we have made extra- and intracellular recordings of the potentials. It has been shown that from the flexor afferents of the fore limbs both facilitating and inhibitory influences are transmitted. The former are expressed in increased frequency of the background impulse activity of the neurons, in the appearance of evoked responses of the "silent" cells and intensification of the test responses for short time intervals with paired heteronymous stimulation. The inhibitory influences prevail over the facilitating and are manifest in depression of the background activity and evoked segmental responses of the neurons. The maximum inhibition of the segmental responses was noted for intervals of 40–140 msec. The duration of inhibition varied from 100–500 msec and more. Depending on the intensity and duration of the inhibitory influences two groups of interneurons have been isolated. The role of the pre- and postsynaptic mechanisms in the transmission of inhibitory influences from the afferents of the fore limbs on the afferents of the hind limbs is discussed.Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 1, No. 3, pp. 235–242, November–December, 1969.     

Multisensory convergence on neurons of the motor cortex in unanesthetized cats

Postsynaptic potentials (PSPs) of 83 neurons in the motor cortex of unanesthetized cats in response to electrodermal, photic, and acoustic stimulation were investigated by intra-and quasi-intracellular recording methods. Most cells responded to stimulation of at least one limb. About 60% of neurons of the posterior and over 75% of neurons of the anterior sigmoid gyrus responded to stimulation of two (or more) limbs. In 29 of 39 neurons of the anterior and 12 of 44 of the posterior sigmoid gyrus PSPs with a short (less than 50 msec) and stable latent period were evoked by flashes and clicks. On presentation of two somesthetic stimuli complete blocking (if the interval was less than 30–60 msec) or weakening (interval 30–200 msec) of responses to the second (testing) stimulus was observed. On presentation of paired photic (or acoustic) stimuli or paired stimuli of different modalities at various intervals from 0 to 100 msec, the testing response was often potentiated. The character of the responses and their interaction thus differed from those obtained under chloralose anesthesia [6, 7]. It is postulated that under the action of chloralose a system of neurons with strong excitatory feedback is formed in the motor cortex which may respond to stimuli of different modalities by something resembling the "all or nothing" principle.Brain Institute, Academy of Medical Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 3, No. 6, pp. 563–573, November–December, 1971.     

Response of cat auditory cortex neurons to tonal stimulation during and after nembutal anesthesia

During acute experiments on 20 cats a comparative study was made of neuronal reaction to a tone, as recorded during the first few hours after administration of Nembutal and after an interval of 10–30 h. No spontaneous activity was seen in 89% of auditory cortex neurons of the anesthetized cats; these produced a sterotyped on- response to the optimal frequency tone. Late neuronal spike discharges at distinct intervals of 100–150 msec appeared in response to the setting up of acoustic stimulation after a brief latent reaction lasting 9–15 msec. It was shown that this stimulation did not produce an off-response in the cortical neurons. When the animals emerged from Nembutal anesthesia, the neurons reacted very differently to the optimal frequency tone. About 76% of the cells produced an on, on-off or off response, while about 21% responded with either tonic spike discharges or total inhibition of these throughout the acoustic stimulation. In unanesthetized cats the vast majority of AI cortical neurons were capable of reacting as long as the stimulus lasted. It is shown how this ability is lost under deep Nembutal anesthetic.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 17, No. 6, pp. 728–737, November–December, 1985.     

Unit responses of the sensomotor cortex to paired electrical stimuli

Unit responses of the sensomotor cortex to paired electrical stimulation and visual cortex, applied either simultaneously or after various delays (from 0 to 200 msec) depend on the order of application of the stimuli and on the interval between them. If stimulation of the sensomotor cortex was used in a conditioning role the response continued unchanged when the intervals between stimuli were increased to 200 msec. If, however, stimulation of the sensomotor cortex had a testing role interaction was observed between the stimuli so that responses to both first and second stimuli were blocked; this was exhibited most clearly for intervals of 40–80 msec between stimuli. The blocking effect persisted on some neurons with delays of up to 200 msec between stimuli, while the response of others to both the first and the second stimulus was restored.Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 5, No. 6, pp. 628–635, November–December, 1973.     

Mechanism of inhibition following reflex discharge in spinal cord interneurons

Using the method of microelectrode (intracellular and extracellular) recording, the mechanism of inhibition following reflex discharge in interneurons of the lumbosacral section of the spinal cord of cats on activation of cutaneous and high-threshold muscle afferents was studied. It was shown that the postdischarge depression of the reflex responses 10–20 msec after the moment of activation of the neuron is due to afterprocesses in the same neuron and presynaptic pathways. The depression of spike potentials from the 20th to the 100th msec is produced by inhibitory postsynaptic potentials (IPSP). During the development of IPSP the inhibition of spike potentials can be due to both a decrease of the depolarization of the postsynaptic membrane below the critical threshold and a decrease of sensitivity of the cell membrane to the depolarizing action of the excitatory postsynaptic potential (EPSP). At intervals between the stimuli of 30–100 msec the duration of EPSP after the first stimulus does not differ from that after the second stimulus. Hence, it is suggested that the presynaptic mechanisms do not play an essential part in this type of inhibition of interneurons. The inhibition following the excitation favors the formation of a discrete message to the neurons of higher orders.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 2, No. 1, pp. 3–9, January–February, 1970.     

Functional properties distinguishing individual auditory cortical neurons

Responses of 246 auditory cortical neurons to paired and repetitive stimulation of geniculo-cortical fibers were studied in experiments on cats immobilized with tubocurarine. The refractory period (RP) varied from 1 to 200 msec in different neurons. For neurons excited antidromically it varied from 1 to 3 msec. Among neurons excited monosynaptically there were some with a short (1.3–6 msec), medium, (8–16 msec) or long (30–100 msec) refractory period. Most neurons excited polysynaptically had a RP of mean length. RPs 30–200 msec in length were due to inhibition arising in the neuron after conditioning stimulation. In some neurons, after a short (1.5–2.0 msec) initial period of refractoriness there was a temporary (for 2–3 msec) recovery of responsiveness, followed by another period of ineffectiveness of the testing stimulus lasting 30–100 msec. Barbiturates selectively inhibited long-latency unit responses in the auditory cortex and during their action the number of responding neurons with a mean RP decreased sharply. The results demonstrate functional heterogeneity of auditory cortical neurons responding to an incoming volley of afferent impulses.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 5, No. 3, pp. 236–245, May–June, 1973.     

Transformation of the afferent tactile signal into a motor command in the cat motor cortex

Activity of 112 neurons of the precruciate motor cortex in cats was studied during a forelimb placing reaction to tactile stimulation of its distal parts. The latent period of response of the limb to tactile stimulation was: for flexors of the elbow (biceps brachii) 30–40 msec, for the earliest reponses of cortical motor neurons about 20 msec. The biceps response was observed 5–10 msec after the end of stimulation of the cortex with a series of pulses lasting 25 msec. Two types of excitatory responses of the neurons were identified: responses of sensory type observed to each tactile stimulation of the limb and independent of the presence or absence of motion, and responses of motor type, which developed parallel with the motor response of the limb and were not observed in the absence of motion. The minimal latent period of the responses of motor type was equal to the latent period of the sensory responses to tactile stimulation (20±10 msec). Stimulation of the cortex through the recording microelectrode at the site of derivation of unit activity, which increased during active flexion of the forelimb at the elbow (11 stimuli at intervals of 2.5 msec, current not exceeding 25 µA), in 70% of cases evoked an electrical response in the flexor muscle of the elbow.M. V. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 9, No. 2, pp. 115–123, March–April, 1977.     

Analysis of evoked discharges in hypothalamic neurons to somatosensory,acoustic, and photic stimulation

Single unit activity in the supramammillary, mammillary, and anterior hypothalamic areas in response to acoustic, photic, and sciatic nerve stimulation was recorded in cats anesthetized with chloralose and immobilized with succinylcholine. In response to sensory stimulation the spontaneous firing rate was increased or decreased, and silent neurons were activated. Evoked potentials of the silent neurons had the shortest latent period to acoustic and somatosensory stimulation (15 msec), and rather longer to photic stimulation (30 msec); in some cases their latent period was 200 msec. Histograms of interspike interval distribution showed a maximum for intervals of up to 50 msec. Histograms of spike distribution relative to the beginning of stimulation showed maximal density between 100 and 200 msec. A high degree of convergence of excitation was found on units of the anterior as well as the posterior hypothalamus. Unit responses in the hypothalamus to sensory stimuli of all three modalities are regarded as being of secondary, nonspecific type.L. A. Orbeli Institute of Physiology, Academy of Sciences of the Armenian SSR, Erevan. Translated from Neirofiziologiya, Vol. 3, No. 6, pp. 592–598, November–December, 1971.     

Monosynaptic inhibitory postsynaptic potentials of cortical neurons

Monopolar intracortical stimulation of the auditory cortex was carried out in cats immobilized with D-tubocurarine. A macroelectrode (tip diameter 100 µ) or a microelectrode (tip diameter 10–15 µ) was used for stimulation. In both cases, besides excitatory responses, primary IPSPs with latent periods of 0.4–1.2 and 1.4–6.0 msec were recorded in cortical neurons close to the point of stimulation. The first group of IPSPs are considered to be generated in response to direct stimulation of bodies or axons of inhibitory cortical neurons, i.e., monosynaptically. The amplitude of these IPSPs varied in different neurons from 3 to 15 mV, and their duration from 4 to 150 msec. Additional later inhibitory responses were superposed on many of them. Of the IPSPs generated in auditory cortical neurons in response to stimulation of geniculocortical fibers 1.5% had a latency of 0.8–1.3 msec. They also are assumed to be monosynaptic. It is concluded that the duration of synaptic delay of IPSPs in cortical neurons and spinal motoneurons is the same, namely 0.3–0.4 msec. Axons of auditory cortical inhibitory neurons may be 1.5 mm long. The velocity of impulse conduction along these axons is 1.6–2.8 m/sec. The genesis of some special features of IPSPs of cortical neurons is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 7, No. 5, pp. 458–467, September–October, 1975.     

Recurrent inhibition of sympathetic preganglionic neurons of the lateral horns of the spinal cord

Experiments on anesthetized and immobilized cats showed that repeated antidromic discharges can be evoked in 32.5% of sympathetic preganglionic neurons of the lateral horns in segments T3, T8–9, and L2 of the spinal cord, with intervals of 16 msec or more between them, which is much greater than the refractory period of these neurons. This feature was shown not to be connected with the properties of axons of that group of neurons and, in particular, with their after-subnormality. After orthodromic discharges in neurons of this group, for a much longer period of time than could be accounted for by possible collision, no antidromic discharges likewise were evoked. As a result of antidromic activation of some of these neurons in one segment, definite inhibition of the orthodromic response of other neurons of the same segment appeared, etiher by a reflex mechanism or through stimulation of descending pathways. The results point definitely to the existence of a mechanism of recurrent inhibition in some sympathetic preganglionic neurons of the lateral horns.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 9, No. 4, pp. 382–389, July–August, 1977.     

Unit responses of the ventral cochlear nucleus in bats of the rhinolophidae family to ultrasonic stimuli after destruction of the ipsilateral cochlea

Investigation of single unit responses in the ventral cochlear nucleus of the Rhinolophidae to ultrasonic stimuli after destruction of the ipsilateral cochlea revealed two groups of neurons with latent periods of: 1) 2–4 msec and 2) 5–32 msec. The first group has responses of low thresholds confined to narrow regions of the spectrum, the second has responses with high thresholds in wide regions. Neurons of the second group are also characterized by small changes in latent period and number of action potentials in response to a change in stimulus strength, large changes in threshold at characteristic frequencies depending on the stimulus duration, but only slight dependence of the thresholds on the time of the increase in strength. The pathways of activation of these neurons and their functional role are discussed.A. A. Zhdanov Leningrad State University. Translated from Neirofiziologiya, Vol. 1, No. 1, pp. 32–40, January–February, 1972.     

Neuronal and synaptic mechanisms of cortical inhibition

The latent periods, amplitude, and duration of IPSPs arising in neurons in different parts of the cat cortex in response to afferent stimuli, stimulation of thalamocortical fibers, and intracortical microstimulation are described. The duration of IPSPs evoked in cortical neurons in response to single afferent stimuli varied from 20 to 250 msec (most common frequency 30–60 msec). During intracortical microstimulation of the auditory cortex, IPSPs with a duration of 5–10 msec also appeared. Barbiturates and chloralose increased the duration of the IPSPs to 300–500 msec. The latent period of 73% of IPSPs arising in auditory cortical neurons in response to stimulation of thalamocortical fibers was 1.2 msec longer than the latent period of monosynaptic EPSPs evoked in the same way. It is concluded from these data that inhibition arising in most neurons of cortical projection areas as a result of the arrival of corresponding afferent impulsation is direct afferent inhibition involving the participation of cortical inhibitory interneurons. A mechanism of recurrent inhibition takes part in the development of inhibition in a certain proportion of neurons. IPSPs arise monosynaptically in 2% of cells. A study of responses of cortical neurons to intracortical microstimulation showed that synaptic delay of IPSPs in these cells is 0.3–0.4 msec. The length of axons of inhibitory neurons in layer IV of the auditory cortex reaches 1.5 mm. The velocity of spread of excitation along these axons is 1.6–2.8 msec (mean 2.2 msec).A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 16, No. 3, pp. 394–403, May–June, 1984.     

Neuronal response in nucleus reticularis thalami and neighboring thalamic structures to natural stimulation during chronic experiments on cats

Spike response was investigated in 104 neurons of the nucleus reticularis thalami (R) and adjoining thalamic nuclei to acoustic, tactile, and visual stimuli during chronic experiments on cats. Of the test neurons, 29% responded to acoustic stimulation and 11% showed no preference in relation to different acoustic stimuli. Minimum latencies of response to sounds measured 12–37 msec in excitatory and 18–27 msec in inhibitory cells. Duration of excitation produced by acoustic stimuli reached 50–250 msec; inhibition lasted 27–190 msec. Most cells belonging to this nucleus were excited by different stimuli; the proportion of inhibitory neurons did not exceed 4–10%.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 21, No. 4, pp. 451–461, July–August, 1989.     

Analysis of spike discharge of a neuron population in the cat motor cortex during a conditioned change of posture reflex

Spike responses of area 4 neurons in the projection area of the contralateral forelimb to acoustic stimulation (1 sec), which became the conditioned stimulus after training, and to dropping of the platform beneath the test limb, which served as reinforcing stimulus, were studied in trained and untrained cats. Responses only of those neurons which were activated during a passive movement caused by dropping of the platform were studied. In trained animals the number of these neurons which responded to the conditioned stimulus if a reflex occurred was 100%, and in the absence of conditioned-reflex movements to the conditioned stimulus it was 70%, much greater than the number of neurons responding to the same acoustic stimulus in untrained animals (45%). On peristimulus histograms of responses of the test neuron population in untrained and trained animals to acoustic stimulation (in the absence of movements) only the initial spike response with a latent period of under 50 msec and a duration of up to 100 msec could be clearly distinguished. In the presence of reflex movement multicomponent spike responses were observed: an initial spike response and early and late after-responses linked with performance of conditioned-reflex limb flexion. Early after-responses 100–200 msec in duration, appearing after a latent period of 100–150 msec, were linked to the time of application of the conditioned stimulus, whereas the appearance and duration of late after-responses were determined by the time of onset of conditioned-reflex movement. The magnitude of the neuronal response to reinforcement in trained animals does not depend on the appearance of the conditioned movement.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 17, No. 1, pp. 93–102, January–February, 1985.     

Conduction of excitation in the cat visual system

Unit responses in area 17 of the visual cortex to stimulation of the lateral geniculate body and optic tract were studied in experiments on unanesthetized cats immobilized with D-tubocurarine. Of the neurons tested, 53.6% responded to stimulation of the lateral geniculate body. In 92% of these cells the responses were orthodromic with latent periods of between 2 and 12.5 msec. Most cells responded with latent periods of 2.0–2.5, 3.0–3.5, and 4.0–4.5 msec, corresponding to latent periods of the components of the electropositive wave of the primary response. Antidromic responses to stimulation of the lateral geniculate body were given by 8% of neurons. The difference between the latent periods of responses of the same visual cortical neurons to stimulation of the optic tract and lateral geniculate body was 0.1–1.8 msec, but for most neurons (55.8%) it was 0.5–1 msec. The histograms of response latencies of visual cortical neurons to stimulation of the above-mentioned formations were found to be similar. It is concluded that the optic radiation contains three principal groups of fibers with conduction velocities of 28.5–16.6, 11.7–8.9, and 7.4–6.0 m/sec, respectively.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 7, No. 6, pp. 589–596, November–December, 1975.