Low-frequency oscillatory activities intrinsic to rat and cat thalamocortical cells.

1. Low-frequency membrane potential oscillations recorded intracellularly from thalamocortical (TC) cells of the rat and cat dorsal lateral geniculate nucleus (dLGN) and of the rat ventrobasal nucleus (VB) maintained in vitro were investigated. On the basis of their electrophysiological and pharmacological properties, four types of activity were distinguished and named: the pacemaker oscillations, the spindle-like oscillations, the 'very slow' oscillations and the 'N-methyl-D-aspartate' (NMDA) oscillations. 2. The pacemaker oscillations (95 out of 173 cells) consisted of rhythmic, large-amplitude (10-30 mV) depolarizations which occurred at a frequency of 1.8 +/- 0.3 Hz (range, 0.5-2.9 Hz) and could often give rise to single or a burst of action potentials. Pacemaker oscillations were observed when the membrane potential was moved negative to -55 and positive to -80 mV, but in a given cell the upper and lower limits of this voltage range were separated by only 13.1 +/- 0.5 mV. Above -45 mV tonic firing consisting of single action potentials was seen in the cells showing this or the other types of low-frequency oscillations. 3. The spindle-like oscillations were observed in thirty-nine (out of 173) TC cells and consisted of rhythmic (2.1 +/- 0.3 Hz), large-amplitude depolarizations (and often associated burst firing) similar to the pacemaker oscillations but occurring in discrete periods every 5-25 s and lasting for 1.5-28 s. The spindle-like oscillations were observed when the membrane potential was moved negative to -55 and positive to -80 mV and in two cells they were transformed into continuous pacemaker oscillations by depolarization of the membrane potential to -60 mV. 4. Pacemaker and spindle-like oscillations were unaffected by tetrodotoxin (TTX) or by selective blockade of NMDA, non-NMDA, GABAA, GABAB, nicotinic, muscarinic, alpha- and beta-noradrenergic receptors. 5. The 'very slow' oscillations consisted of a TTX-insensitive, slow hyperpolarization-depolarization sequence (5-15 mV in amplitude) which lasted up to 90 s and was observed in nine dLGN cells and in two VB cells. The pacemaker and the spindle-like oscillations were recorded in one cell each which also showed the 'very slow' oscillations. 6. The 'NMDA' oscillations were observed only in a 'Mg(2+)-free' medium (0 mM-Mg2+, 2-4 mM-Ca2+; 64 out of 72 cells) and consisted of large-amplitude (10-25 mV) depolarizations that did not occur at regular intervals and were intermixed with smaller depolarizations present on the baseline and on the falling phase of the larger ones.(ABSTRACT TRUNCATED AT 400 WORDS)

Two inward currents and the transformation of low-frequency oscillations of rat and cat thalamocortical cells.

1. The contribution of a slow, mixed Na(+)-K+, inward rectifying current (Ih) and the T-type Ca2+ current (IT) (that underlies low-threshold Ca2+ potentials) to the low-frequency oscillations observed in rat and cat thalamocortical (TC) cells in vitro was studied using current clamp and single-electrode voltage clamp recordings. 2. From a holding potential of -50 mV, voltage steps negative to -60 mV showed the presence of a slow, non-inactivating inward current, Ih. This current was unaffected by Ba2+ (1-4 mM), tetrodotoxin (0.5-1 microM) and TEA (20 mM, n = 6), reversibly blocked by Cs+ (1-3 mM), and its reversal potential (-33.0 +/- 1.2 mV) followed changes in the extracellular Na+ and K+, but not Cl-, concentration. 3. Application of Cs+ (1-3 mM) abolished the pacemaker oscillations (n = 9), while in six cells that did not show any oscillatory activity Cs+ first evoked the spindle-like oscillations that, in the continuous presence of these ions, were then transformed into the pacemaker oscillations before all activities were finally blocked: all these effects were accompanied by a hyperpolarization and a progressive decrease and final blockade of Ih. Cs+ had no effect on the 'N-methyl-D-aspartate' (NMDA) oscillations (n = 5) and Ba2+ (2 mM, n = 8) did not block the pacemaker, the spindle-like and the 'NMDA' oscillations. 4. In ten cells that showed the pacemaker oscillations selective activation of beta-adrenoceptors by 10-50 microM-noradrenaline (in the presence of alpha-noradrenergic antagonists) or by 20 microM-isoprenaline first transformed the pacemaker oscillations into the spindle-like oscillations that, in the continuous activation of beta-receptors, were finally abolished: all these effects were accompanied by a depolarization and a progressive increase of Ih. 5. In TC cells that showed the pacemaker oscillations application of 1-octanol (50-100 microM), an antagonist of T-type Ca2+ currents, reversibly blocked this activity but concomitantly decreased (50%) the cell input resistance (n = 5). Application of Ni2+ (0.2-0.5 mM, n = 13), another antagonist of IT reversibly blocked the pacemaker, the spindle-like and the 'NMDA' oscillations. 7. In cells showing the pacemaker oscillations it was found that the current developing from the most hyperpolarized potential of an oscillation cycle was an inward relaxation whose time course differed from that of Ih evoked at the same potential.(ABSTRACT TRUNCATED AT 400 WORDS)

Pacemaker-like and other types of spontaneous membrane potential oscillations of thalamocortical cells.

During EEG-synchronized sleep, thalamic activity is characterized by rhythmic oscillations that till recently have been suggested to require the contribution of intra- and extra-thalamic inputs. The present experiments show that thalamocortical (TC) cells, mechanically and pharmacologically isolated from their intra-thalamic, cortical and brainstem inputs, are capable of different types of spontaneous membrane potential oscillations some of which resemble those observed in TC cells of the living animal during EEG-synchronization.

Differential burst firing modes in neurons of the mammalian visual cortex in vitro.

The firing patterns of visual cortical neurons were studied by intracellular recording in in vitro guinea pig brain slices. On depolarization 57% of the cells exhibited tonic firing of action potentials while the remaining cells (43%) had a phasic component in their response. Phasic cells exhibited a large diversity in their burst characteristics as well as in the burst dependence on the membrane potential. Ionic conductances underlying burst generation appeared to be also diverse, thus bursting neurons in the visual cortex cannot be grouped in a single, homogeneous population.

Cl- - and K+-dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus.

1. Hyperpolarizing potentials evoked by electrical stimulation of the optic tract were studied in projection cells of the rat dorsal lateral geniculate nucleus (LGN) in vitro. In the same cells the effects of gamma-amino butyric acid (GABA), baclofen and acetylcholine (ACh) were also investigated. 2. In the majority of cells a short- (SHP) (34 ms) and a long-lasting (LHP) (240 ms) hyperpolarizing potential could be recorded in the presence and in the absence of a preceding EPSP. They were blocked by tetrodotoxin (1 microM) and were more sensitive than the monosynaptic EPSP to a low-Ca2+-high-Mg2+ solution. 3. The SHP was associated with a marked decrease (75%) in input resistance, was blocked by bicuculline (1-100 microM) and its reversal potential (-67 mV) was dependent on the extracellular Cl- concentration. 4. The LHP was associated with a smaller decrease (45%) in input resistance and its reversal potential (-76 mV) was dependent on the extracellular K+ concentration. It was increased by bicuculline (100% at 50 microM) and nipecotic acid (30% at 10 microM), blocked by Ba2+ (1 mM), and unaffected by eserine (1-10 microM), neostigmine (1-10 microM) or by recording with EGTA-filled electrodes. In the presence of bicuculline, a single LHP was able to evoke, as a rebound response, a low-threshold Ca2+ spike that was, however, not followed by another LHP (or any other long-lasting hyperpolarization). 5. Ionophoretic applications of GABA evoked in the same cell a Cl- -dependent hyperpolarization (reversal potential: -65 mV) and/or depolarization, both of which were associated with a marked decrease (91%) in input resistance and abolished by bicuculline. GABA was also able to evoke a bicuculline-insensitive, K+-dependent hyperpolarization that had a reversal potential of -75 mV and was associated with a smaller decrease (43%) in input resistance. 6. Baclofen, applied by ionophoresis, pressure ejection or in the perfusion medium (1-100 microM), produced a hyperpolarization that had a reversal potential of -79 mV and was associated with a decrease (45%) in input resistance. 7. In the majority of cells (thirty-seven out of forty) ACh evoked a slow depolarization and only in three cells a hyperpolarization which had a reversal potential of -80 mV.(ABSTRACT TRUNCATED AT 400 WORDS)

[Spontaneous rhythmic depolarization in the principal cells of the lateral geniculate body in vitro: the role of NMDA receptors]. / Dépolarisations rythmiques spontanées dans les cellules principales du corps genouillé latéral in vitro: rôle des récepteurs NMDA.

Intracellular recordings using standard current clamp techniques were performed on projection cells of the rat lateral geniculate nucleus (LGN) in vitro. These cells are generally quiescent in vitro but when magnesium was removed from the perfusion medium they invariably showed rhythmic depolarizations (15-20 mV, 210-320 ms) that occurred at a frequency of 1.5-2 Hz and evoked 1 to 4 action potentials. This activity was completely blocked by micromolar concentrations of magnesium (50-150 microM) while tetrodotoxine (1 microM) abolished the action potentials but left the underlying rhythmic depolarizations unchanged. These results demonstrate that rat LGN projection cells are capable of producing rhythmic depolarizations in vitro and suggest the possibility that NMDA receptors might be involved in these rhythmic oscillations.

Electrophysiological properties of neurons recorded intracellularly in slices of the pigeon optic tectum.

The electrical properties of pigeon's optic tectum neurons located in the non-retinorecipient region of layer II have been studied in vitro slice preparations by using intracellular recordings. As judged from the somatodendritic characteristics of cells intracellularly labeled with horseradish peroxidase recordings were obtained from pyramidal neurons, the main morphological type, as well as from ganglion cells. When stimulated with depolarizing current pulses of 300-500 ms duration, three distinct modes of firing were observed. Most neurons (Type I) responded with a continuous firing of fast action potentials whose frequency rate increased regularly when current strength was raised. Another group of cells (Type II) also exhibited sustained firing. However, in Type II cells, grouped discharges formed by 2-6 fast action potentials per group fired in rapid succession were elicited within a certain range of current intensity. Finally, another group of cells (Type III) responded at all intensities tested by a short train of fast action potentials only at the onset of the current step. At current strength close to threshold the spike undershoot of type I neurons was followed by a slow hyperpolarizing afterpotential while the spike undershoot of Type II cells was followed by a hump-like depolarization and a slow hyperpolarizing afterpotential. In Type II cells, we have also observed a pronounced increase of the hyperpolarizing afterpotential after a grouped discharge. Type III cells were characterized by a small amplitude and short duration hyperpolarizing afterpotential, barely visible in most of them. In Type I and II cells the slow hyperpolarizing afterpotential was blocked by replacing Ca2+ with Mg2+ or Cd2+ in the saline. These results support the idea that in these two types of neurons the slow hyperpolarizing afterpotential is primarily caused by a Ca2+-dependent K+ conductance. Furthermore, blocking the slow hyperpolarizing afterpotential provoked a pronounced increase of the firing frequency of Type I cells. In Type II cells blockade of the slow hyperpolarizing afterpotential had a greater effect on firing behavior: i.e. when Ca2+ was replaced with Mg2+ or Cd2+, Type II neurons exhibited repetitively fired action potentials at high frequency but were incapable of discharging repetitive grouped discharges. These observations indicate that the Ca2+-dependent K+ conductance involved in the generation of the slow hyperpolarizing afterpotential is the main modulator of the firing behavior of both types of cells.(ABSTRACT TRUNCATED AT 400 WORDS)

Synaptic transmission of excitation from the retina to cells in the pigeon's optic tectum.

Intracellular recordings were used to study the synaptic excitation of optic tectum neurons in the pigeon. Electrical stimulation of both contralateral optic nerve and ipsilateral optic tract evoked in the tectal neurons EPSPs which in most cases were followed by an IPSP. An extrapolation procedure based on response latency was used to reveal that the EPSPs were mediated by way of mono-, di- and polysynaptic connections with the retinal endings. The laminar location of the recorded cells was estimated according to the field potential and the recording depth with the exception of one cell which was intracellularly stained with HRP. Monosynaptic EPSPs were recorded from cells in the retinorecipient region (sublayers IIa-f) as well as in the non-retinorecipient region (sublayers IIg-j and layer III) of the tectum, while di- and polysynaptic EPSPs were never recorded from the input layers. Tectofugal projections arise largely from layer III neurons. Thus, these results indicate that retinal excitation is transmitted to the output tectal cells by way of mono-, di- or polysynaptic pathways. The conduction velocities of most retinal fibers mediating the EPSP ranged from 4 to 22 m/s (average 12 m/s). However, in a number of retinal fibers the conduction velocities were in a faster range, up to 36 m/s.

Synaptic organization of inhibitory circuits in the pigeon's optic tectum.

The synaptic organization of inhibitory systems in the pigeon's optic tectum was studied with intracellular recording techniques. An extrapolation procedure based on response latency was used to determine the synaptic delay of the postsynaptic potentials (PSPs) and the velocity of conduction of the associated retinal axons. Tectal cells receive mostly disynaptic, trisynaptic or polysynaptic inhibition from retinal ganglion cells. However, evidence was found which together with previous studies raised the possibility of the existence of a direct inhibitory retino-tectal path. Our present results also suggest that inhibition is transmitted from the retina to the tectal cells by way of both, feedforward and feedback pathways.

Morphology and laminar distribution of electrophysiologically identified cells in the pigeon's optic tectum: an intracellular study.

The responses of 65 cells to electrical stimulation of the contralateral optic nerve were intracellularly recorded in the pigeon optic tectum by using micropipettes filled with a solution of horseradish peroxidase. Nineteen of them were successfully labeled. Microscopic examination of the filled cells shows that our sample includes six pyramidal, ten ganglion, two stellate, and one bipolar horizontal cells. Thus, pyramidal and ganglion neurons constitute the most numerous types of cells in our sample. Pyramidal cells were located in layer II but mostly in its non-retinorecipient part, and they had restricted ascending dendritic trees oriented orthogonal to the tectal lamination. Ganglion cells were located in layer III with one exception, which was in sublayer IIi. These cells had non-oriented dendritic trees which ramify over considerable distances. Terminal dendritic branches from a number of pyramidal and ganglion cells extended superficially well within the region of optic fibers termination. In our study, ganglion cells constituted the efferent tectal elements. Pyramidal cells responded to optic nerve stimulation with a pure EPSP, with an EPSP-IPSP sequence, or with a pure IPSP. Ganglion cells always exhibited an IPSP either alone or preceded by an EPSP. Stellate and bipolar cells responded with a pure EPSP. The study of the laminar distribution of labeled and non-labeled cells shows from surface to depth, a gradual increase in the number of cells responding with an EPSP-IPSP or with a pure IPSP and a gradual decrease in the number of those exhibiting a pure EPSP. The analysis of the sensitivity of EPSPs and IPSPs to high frequency optic nerve stimulation shows that monosynaptic as well as polysynaptic EPSPs can be recorded from cells in the non-retinorecipient tectal region, a number of ganglion and pyramidal cells receive a direct retinal excitatory input as their dendrites pass through the region of optic endings, most IPSPs are polysynaptic, some cells located in the retinorecipient region may receive direct retinal inhibitory connections.

[Discharge mechanism of pigeon optic tectum neurons in an in vitro preparation]. / Mode de décharge des neurones du toit optique du pigeon dans une préparation in vitro.

The pattern of discharge of neurones of the pigeon's optic tectum to directly injected depolarizing current was investigated in in vitro slice preparation. Three patterns of discharge were found: some neurones (types I and II) give a tonic response: type I-neurones exhibited a repetitive firing whereas type II-neurones showed grouped discharges (doublets or triplets). Type III-neurones displayed a phasic response formed by a few action potentials of decreasing amplitude, triggered at the onset of the current pulse. Each pattern of response was associated with a specific shape of action potential.

Postsynaptic potentials in neurons of the pigeon's optic tectum in response to afferent stimulation from the retina and other visual structures: an intracellular study.

The responses of the cells in the pigeon's optic tectum to electrical stimulation of the contralateral optic nerve, the ipsilateral visual Wulst and the opposite optic tectum were intracellularly recorded. Optic nerve or visual Wulst stimulation elicited 3 types of responses: (1) a pure EPSP which gave rise to one or two action potentials; (2) an EPSP which sometimes gave rise to a spike, followed by an IPSP; and (3) a pure IPSP. Opposite tectum stimulation evoked in the tectal cells either a pure IPSP or a pure EPSP. The mono- or polysynaptic nature of the pathways involved in the excitatory and inhibitory responses of the tectal cells was assessed by increasing the frequency of the optic nerve stimulation. At low stimulus rates (2-6 Hz), all the excitatory events showing latencies longer than 5 ms were blocked suggesting that they were polysynaptic. Excitatory events having latencies shorter than 5 ms were generally able to follow high rate frequencies of optic nerve stimulation (40, 50 or 90 Hz) and we considered them to be monosynaptic. All but 3 IPSPs evoked by optic nerve stimulation, were blocked by stimulus rates beyond 5 Hz. Thus, although most IPSPs are generated through polysynaptic paths, direct retino-tectal inhibitory paths may also exist. The latency of the responses of individual cells to optic nerve, visual Wulst and opposite tectum stimulation show that the polysynaptic IPSPs to optic nerve stimulation did not involve relays in the visual Wulst or the opposite tectum.

Suppressive regions in the visual receptive fields of single cells of the pigeon's optic tectum.

Single unit extracellular recordings were obtained from non-directional and from directionally selective cells in the pigeon's optic tectum. Non-directional cells were classified according to their excitatory dynamic profiles into three classes. Class A: cells showing spatially superimposed light and dark regions in their fields. Class B: cells showing spatially separated light and dark regions in their fields. Class C: cells which responded exclusively to one sign of contrast. Most of the cells in our sample showed a suppressive region outside the excitatory area from where moving stimuli were able to reduce the units' "spontaneous" background firing. Suppressive regions were found in directionally selective as well as in non-directional cells, regardless of their dynamic excitatory profiles, with the exception of Class C cells. Evidence of spatial overlapping between the excitatory and the suppressive region was obtained with both moving and flashed stimuli. Furthermore, suppressive antagonistic effects were observed in Class B cells.

Receptive field properties of single cells in the pigeon's optic tectum during cooling of the 'visual wulst'.

In birds, efferents from the visual telencephalon (visual wulst) terminate in the ipsilateral and contralateral optic tectum. This study concerns the influence of a bilateral cryogenic block of the wulst on the receptive field properties of the visual tectal cells in the pigeon. Tectal units were tested for their responses to static and moving stimuli before, during and after cooling the wulst. For some units the cryogenic block of the wulst was repeated twice. The responsiveness to static and moving stimuli was decreased in most of the tectal cells when the neural activity of the wulst was blocked. In contrast, in some units cooling the wulst provokes an increase of responsiveness. These results indicate that the wulst-tectum path is able to convey both excitatory and inhibitory influences. Other receptive field properties such as the spatial location of the light and dark excitatory regions in the field, the effect of the surround, the size and shape of the excitatory region, the relative responsiveness to static and moving stimuli and the 'spontaneous activity' were not affected by wulst cooling. Directional tuning curves were obtained in 18 directionally selective cells before, during and after wulst cooling. In 6 of them the cryogenic block provoked a reduction in directional selectivity either by way of a reduction of the preferred response (4 cells) or by way of an increase of the non-preferred responses (2 cells). In two others directionally selective cells, cooling the wulst provoked a total loss of directional selectivity due to a reduction of the response to the preferred direction together with an increase of the response to the null direction. These results show: (1) that the retinal directional selective input to the tectum is affected by the cryogenic block of the wulst; and (2) that the visual wulst provokes a sharpening of the directional tuning at the optic tectum level.

[Influence of visual telencephalon (wulst) on directional selective neurons of pigeon's optic tectum (author's transl)]. / Influence des aires télencéphaliques (wulst) sur la sélectivité directionnelle des cellules tectales chez le pigeon.

The influence of the visual telencephalic projection area (Wulst) upon directional selective cells in the Pigeon's optic tectum was studied through reversible cold block of this telencephalic region. About half of the cells studied were affected during Wulst cooling. The effect was either a total loss or a marked reduction of the cell directional selectivity. These results indicate that the Wulst plays an important role in controlling the directional selectivity in the Pigeon's optic tectum.

The spatial organization of the excitatory regions in the visual receptive fields of the pigeon's optic tectum.

The spatial location of the excitatory regions in the receptive field of cells in the pigeon's optic tectum was analyzed with light and dark edges moving at a constant velocity. The tectal cells were classified into two main groups: 1-cells showing spatially overlapping light and dark excitatory regions in their receptive field (60%); cells showing spatially separated light and dark excitatory regions in their receptive field (32%). A small number of cells discharged only to one sign of contrast. These results were confirmed by testing the cells with light bars of various widths. Latency studies were carried out with single edges moving at a series of constant velocities. In most cases, for any given cell the light and dark edge discharges were shown to have similar latencies. These results also indicate that the relative location of the excitatory regions in the receptive field of most tectal cells was not significantly affected by the latency of the discharges.