Types Of Firing Patterns Research Articles

Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive.

Principal neurons of the lateral superior olive (LSO) detect interaural intensity differences by integration of excitatory projections from ipsilateral bushy cells and inhibitory inputs from the medial nucleus of the trapezoid body. The intrinsic membrane currents active around firing threshold will form an important component of this binaural computation. Whole cell patch recording in an in vitro brain slice preparation was employed to study conductances regulating action potential (AP) firing in principal neurons. Current-clamp recordings from different neurons showed two types of firing pattern on depolarization, one group fired only a single initial AP and had low input resistance while the second group fired multiple APs and had a high input resistance. Under voltage-clamp, single-spiking neurons showed significantly higher levels of a dendrotoxin-sensitive, low threshold potassium current (ILT). Block of ILT by dendrotoxin-I allowed single-spiking cells to fire multiple APs and indicated that this current was mediated by Kv1 channels. Both neuronal types were morphologically similar and possessed similar amounts of the hyperpolarization-activated nonspecific cation conductance (Ih). However, single-spiking cells predominated in the lateral limb of the LSO (receiving low frequency sound inputs) while multiple-firing cells dominated the medial limb. This functional gradient was mirrored by a medio-lateral distribution of Kv1.1 immunolabelling. We conclude that Kv1 channels underlie the gradient of LSO principal neuron firing properties. The properties of single-spiking neurons would render them particularly suited to preserving timing information.

Nucleus accumbens cell firing during goal-directed behaviors for cocaine vs. ‘natural’ reinforcement

Numerous investigations indicate that the nucleus accumbens (Acb) is an important neural substrate mediating the reinforcing properties of ‘natural’ rewards (food or water) as well as abused substances. Here, our electrophysiological studies that examined Acb cell firing within seconds of lever press responding for intravenous cocaine vs. water or food reinforcement in rats are reviewed. Initial investigations revealed that a subset of Acb neurons exhibits four types of firing patterns within seconds of the reinforced response for intravenous cocaine during self-administration sessions. Three of those four cell types were also observed during water reinforcement sessions. In a subsequent study, the activity of the same Acb neurons was examined in rats responding on multiple schedules for either two distinct ‘natural’ reinforcers (water and food), or one of those ‘natural’ reinforcers and the intravenous self-administration of cocaine. The results showed that the majority of neurons tested exhibited similar, overlapping neuronal firing patterns across the two ‘natural’ reinforcer conditions. In contrast, the majority of neurons examined displayed differential, nonoverlapping firing patterns relative to operant responding for water (or food) vs. cocaine reinforcement. Additional studies that examined the role of associative factors on Acb cell firing during cocaine self-administration sessions are reviewed. Collectively, these findings illustrate the dynamic nature of Acb cell firing in behaving animals, and provide insight into how Acb neurons process information about goal-directed behaviors for ‘natural’ reinforcers vs. abused substances.

Lamina-specific membrane and discharge properties of rat spinal dorsal horn neurones in vitro.

Membrane and discharge properties determine the input-output relationship of neurones and are therefore of paramount importance for the functions of neural circuits. Here, we have tested the hypothesis that neurones in different laminae of the spinal dorsal horn differ in their electrophysiological properties. Whole-cell patch-clamp recordings from dorsal horn neurones in a rat transverse spinal cord slice preparation were used to record active and passive membrane properties. Neurones from superficial dorsal horn laminae had higher membrane resistances and broader action potentials than deep dorsal horn neurones. Action potential thresholds were highest in lamina II neurones, representing low membrane excitability. Five types of firing patterns were identified in response to depolarising current injections. Tonic-firing neurones discharged action potentials at regular intervals throughout the current pulse. Delayed-firing neurones showed a delayed onset of firing in response to current injections that was due to activation of a transient voltage-dependent outward current, presumably an A-current. Another group of neurones fired a short initial burst of action potentials. Single-spiking neurones discharged only one action potential at the onset of a depolarising pulse. Phasic-bursting neurones showed irregular bursts of action potentials. Firing patterns were unequally distributed among laminae. Tonic-firing neurones were numerous in lamina I and deeper laminae but were not found in lamina II. Delayed-firing neurones were encountered in laminae I and II but not in deeper laminae. Most of the neurones showing an initial burst were found in lamina II. These differences in membrane and discharge properties probably contribute to lamina-specific processing of sensory, including nociceptive, information.

Transitions between different synchronous firing modes using synaptic depression

Bistability of different synchronous firing patterns arising in networks of pyramidal cells and interneurons which include depressing synapses is demonstrated. The firing modes differ in their frequencies, in the type of firing pattern and in their degree of synchrony. The network elements governing the frequency of each mode are identified and ways to transition between modes are discussed.

Neural Correlates for Angular Head Velocity in the Rat Dorsal Tegmental Nucleus

Many neurons in the rat lateral mammillary nuclei (LMN) fire selectively in relation to the animal's head direction (HD) in the horizontal plane independent of the rat's location or behavior. One hypothesis of how this representation is generated and updated is via subcortical projections from the dorsal tegmental nucleus (DTN). Here we report the type of activity in DTN neurons. The majority of cells (75%) fired as a function of the rat's angular head velocity (AHV). Cells exhibited one of two types of firing patterns: (1) symmetric, in which the firing rate was positively correlated with AHV during head turns in both directions, and (2) asymmetric, in which the firing rate was positively correlated with head turns in one direction and correlated either negatively or not at all in the opposite direction. In addition to modulation by AHV, some of the AHV cells (40.1%) were weakly modulated by the rat's linear velocity, and a smaller number were modulated by HD (11%) or head pitch (15.9%). Autocorrelation analyses indicated that with the head stationary, AHV cells displayed irregular discharge patterns. Because afferents from the DTN are the major source of information projecting to the LMN, these results suggest that AHV information from the DTN plays a significant role in generating the HD signal in LMN. A model is proposed showing how DTN AHV cells can generate and update the LMN HD cell signal.

Evidence that Trigeminal Brainstem Interneurons Form Subpopulations to Produce Different Forms of Mastication in the Rabbit

To determine how trigeminal brainstem interneurons pattern different forms of rhythmical jaw movements, four types of motor patterns were induced by electrical stimulation within the cortical masticatory areas of rabbits. After these were recorded, animals were paralyzed and fictive motor output was recorded with an extracellular microelectrode in the trigeminal motor nucleus. A second electrode was used to record from interneurons within the lateral part of the parvocellular reticular formation (Rpc-alpha, n = 28) and gamma- subnucleus of the oral nucleus of the spinal trigeminal tract (NVspo-gamma, n = 68). Both of these areas contain many interneurons projecting to the trigeminal motor nucleus. The basic characteristics of the four movement types evoked before paralysis were similar to those seen after the neuromuscular blockade, although cycle duration was significantly decreased for all patterns. Interneurons showed three types of firing pattern: 54% were inactive, 42% were rhythmically active, and 4% had a tonic firing pattern. Neurons within the first two categories were intermingled in Rpc-alpha and NVspo-gamma: 48% of rhythmic neurons were active during one movement type, 35% were active during two, and 13% were active during three or four patterns. Most units fired during either the middle of the masseter burst or interburst phases during fictive movements evoked from the left caudal cortex. In contrast, there were no tendencies toward a preferred coupling of interneuron activity to any particular phase of the cycle during stimulation of other cortical sites. It was concluded that the premotoneurons that form the final commands to trigeminal motoneurons are organized into subpopulations according to movement pattern.

Electrophysiological properties of cultured neonatal rat dorsal horn neurons containing GABA and met-enkephalin-like immunoreactivity.

We have developed a culture of neurons dissociated from the most superficial laminae of the neonatal rat spinal cord dorsal horn (DH). By using the perforated patch-clamp technique, we distinguished four types of neurons based on their firing properties in response to intracellular injection of 900 ms lasting current pulses. Type 1 neurons were characterized by a tonic firing. Type 2 neurons displayed marked spike accommodation and fired brief (<500 ms) bursts of action potentials, whereas type 3 neurons fired a single spike. Type 4 neurons exhibited different types of firing patterns, but all of them possessed a time-dependent inwardly rectifying current activated by membrane hyperpolarization. Met-enkephalin-like immunoreactivity (met-ENK-LI) and glutamic acid decarboxylase-like immunoreactivity (GAD-LI) were colocalized in 42% of the neurons (n = 59), which were previously identified electrophysiologically. Type 1-4 neurons represented respectively 4, 64, 20, and 12% of the population of neurons colocalizing met-ENK-LI and GAD-LI. We conclude that the electrophysiological properties of DH neurons present in our cultures are similar to those described in acute slice or hemisected spinal cord preparations and that met-ENK-LI and GABA-LI are preferentially colocalized in type 2 neurons.

Intracellular recordings from intramural neurons in the guinea pig urinary bladder.

1. Intracellular recordings were made from intramural neurons in the urinary bladder of guinea pigs. 2. The neurons were located in two types of ganglia: those where the cells were densely packed and those where the neurons were loosely packed. Staining of the cells by intracellular injections of markers showed that the cells had between one to three long processes and several short dendrites. 3. The resting potential measured in 230 neurons was -55.20 +/- 0.67 (SE) mV, and the input resistance was 58.37 +/- 1.78 M omega. 4. Injection of depolarizing currents from the recording electrode evoked two types of firing patterns. In 86.2% of the neurons, depolarizing currents evoked a prolonged firing of action potentials (tonic cells). In the rest of the neurons, a depolarization elicited one to three action potentials only (phasic cells). In all the cells tested, the action potentials were reversibly blocked by tetrodotoxin (TTX; 1 microM). In the presence of TTX. Ca2+ spikes were observed in 50% of the cases. 5. Single action potentials were followed by fast hyperpolarizations having mean duration of 92.7 +/- 6.0 ms and amplitude of 13.3 +/- 1.0 mV. In 62.5% of the cells repetitive firing of action potentials was followed by delayed, slow hyperpolarizations (duration 3.8 +/- 0.5 s), which were diminished by the K+ channel blocker 4-aminopyridine and in Ca+2-free high-Mg2+ medium. These results indicate that the prolonged after-spike hyperpolarizations were due to opening of Ca(2+)-induced K+ channels. 6. Electrical stimulation of nerve fiber tracts evoked fast excitatory synaptic potentials that were blocked by the nicotinic receptor antagonist hexamethonium (0.2 mM). Exogenous acetylcholine elicited depolarizations that were also blocked by hexamethonium. Nerve stimulation at frequencies of 0.1 Hz or higher caused strong facilitation of the synaptic potentials. Stimulation at 10-20 Hz did not evoke slow synaptic potentials.

Regenerative properties of pyramidal cell dendrites in area CA1 of the rat hippocampus.

1. Intracellular recordings were obtained from 184 distal apical dendrites and twenty-six somata of CA1 pyramidal neurones in the rat hippocampal slice preparation. In the presence of 3.25 mM K+ 200 ms suprathreshold current pulses evoked three different types of firing patterns in the apical dendrites, all of which were distinct from regular somatic firing. Fast tetrodotoxin (TTX)-sensitive spiking was evoked in 38.8% of the dendrites. Compound spiking, consisting of an initial fast spike followed by one or more secondary slow spikes of variable amplitude and duration, was seen in 44.1% of dendrites. 'Classical' burst firing, resembling intrinsic somatic bursts, was evoked in 17.1% of the dendrites. 2. In fast spiking dendrites, the spikes evoked by long depolarizing pulses were rarely overshooting, showed prominent accommodation and declined progressively to about one-third of the initial amplitude. The amplitude of single dendritic fast spikes (50.6 +/- 1.5 mV; mean +/- S.E.M.) was smaller than that of somatic spikes (82.2 +/- 1.9 mV) and their rate of rise (81.3 +/- 4.3 V s-1) was markedly slower than that of somatic spikes (291.5 +/- 17.8 V s-1). However, the thresholds were not significantly different (dendrites, -49.8 +/- 0.8 mV; somata, -50.8 +/- 1.3 mV). These results indicate that fast spikes in the distal parts of apical dendrites are generated by a local regenerative Na+ current. 3. 4-Aminopyridine (4-AP, 0.1-0.5 mM) caused a dose-dependent slowing of the repolarization of the fast spikes, while tetraethylammonium (TEA, 2 mM) and Co2+ (2 mM) induced a slowing of the late phase of the repolarization. These results indicate that the transient outward K+ current, IA, and the Ca(2+)-activated K+ current, IC, are involved in the repolarization of dendritic Na(+)-dependent spikes. 4. Compound spiking was completely blocked by TTX (0.5-1 microM). The secondary slow spikes within the complex were blocked by Co2+ (2 mM), nifedipine (10 microM) and high concentrations (> 50 microM) of verapamil, while Ni2+ (100-300 microM) had no effect. Thus, compound spiking consists of an initial Na(+)-dependent spike followed by one or more slow Ca(2+)-dependent spikes mediated by L-type Ca2+ channels located in the apical dendrites. 5. In fast spiking dendrites, 4-AP (0.5-2.5 mM) changed the firing pattern from regular fast spiking to compound spiking. In the presence of 4-AP (0.1-0.5 mM), the single fast spike evoked by a short (20 ms), threshold current pulse, was followed by secondary slow spikes of variable amplitude and duration.(ABSTRACT TRUNCATED AT 400 WORDS)

Contralateral projections of thoracic respiratory interneurones in the cat.

1. Retrograde neuronal transport following small iontophoretic injections of horseradish peroxidase was used to investigate the location of neurones projecting to the thoracic ventral horn of the cat. 2. A concentration of labelled neurones was seen in the contralateral medial ventral horn at the immediately opposite rostrocaudal position. 3. The participation of respiratory interneurones in the projection was investigated by means of spike-triggered averaging, as follows. 4. Spike trains of single interneurones whose firing patterns were related to the central respiratory cycle were recorded extracellularly in the thoracic ventral horn of anaesthetized, paralysed cats. Firing patterns were defined by the construction of cycle-triggered histograms. 5. Spike-triggered averaging of the signal from an extracellular tungsten microelectrode in the opposite ventral horn was performed to test for the presence of axonal, terminal or focal synaptic potentials. 6. At least one of these types of potential was found for 34/55 units. Terminal potentials were found for thirty-one units, accompanied by focal synaptic potentials for twenty-seven units. Potentials were found for units with all types of firing patterns. Units whose activity elicited these potentials were generally located in the medial half of the ventral horn. 7. We conclude that at least 60% of the respiratory interneurones project to the immediately opposite ventral horn.

Control of abdominal and expiratory intercostal muscle activity during vomiting: role of ventral respiratory group expiratory neurons.

The role of ventral respiratory group (VRG) expiratory (E) neurons in the control of abdominal and internal intercostal (expiratory) muscle activity during vomiting was examined in decerebrate cats by recording from these neurons during fictive vomiting in paralyzed animals and comparing abdominal muscle activity during vomiting before and after sectioning the axons of these descending neurons. Fictive vomiting was defined by a series of bursts of coactivation of abdominal and phrenic nerves elicited by either subdiaphragmatic vagus nerve stimulation or emetic drugs. Such coordinated activity would be expected to produce vomiting if the animals were not paralyzed. Data were recorded from 27 VRG E neurons that were antidromically activated from the lower thoracic (T13) or lumbar spinal cord. During fictive vomiting, almost two-thirds of these neurons (17/27) were mainly active in between periods of abdominal and phrenic nerve coactivation, when the internal intercostal motoneurons are known to be active. This group of neurons was termed INT neurons. INT neurons were subdivided according to whether they were active between every burst of phrenic and abdominal nerve coactivation (INTa neurons, n = 10) or only between some bursts (INTb neurons, n = 7). Another one-third of the VRG E neurons had normal or increased levels of activity when the abdominal nerves were active during fictive vomiting (ABD neurons). The one remaining neuron was mainly silent throughout fictive vomiting. ABD neurons were indistinguishable from INT neurons on the basis of their location in the VRG, type of firing pattern (ramp versus step ramp), conduction velocity, or extent of projection in the lumbar cord. However, INTa neurons had a significantly higher discharge rate during respiration than either ABD or INTb neurons. Abdominal muscle EMG and nerve activity were recorded from six unparalyzed cats before and after cutting the axons of VRG E neurons as they cross the midline between C1 and the obex. The lesions abolished or almost eliminated expiratory modulation of abdominal muscle activity. In contrast, the abdominal muscles were always active during vomiting; however, the amplitude of postlesion abdominal activity varied from approximately 70-100% of prelesion values in three cats to 60-70% of normal in a fourth animal to only approximately 20% of prelesion values in two other cats.(ABSTRACT TRUNCATED AT 400 WORDS)

Suprachiasmatic neurons in tissue slices from ovariectomized rats: Electrophysiological and neuropharmacological characterization and the effects of estrogen treatment

Single-unit activity and unit responses to putative neurotransmitters were recorded from suprachiasmatic nucleus (SCN) neurons in brain tissue slices from ovariectomized rats either treated or untreated with estrogen. Altogether, 204 units were studied from estrogen-treated and untreated preparations, and at the resting state, 37% of these units fired regularly, 57% fired irregularly, and 6% were silent but evokable by electrical stimulation. Most of the irregular units fired continuously ( n=100), while the rest fired intermittently ( n=12) or phasically ( n=4). Neurons with different types of firing patterns also varied significantly in resting firing rate and in responsiveness to transmitters and to estrogen treatment. The average resting firing rate decreased significantly from regular, irregular and continuous, intermittent, to silent units. Acetylcholine (ACh) and/or serotonin (5-HT) injected directly into the perfusion chamber evoked responses from more irregular (69% of 61 units) than regular units (20% of 46 units). None of the 5 silent units tested was activated by ACh or 5-HT. Responses to ACh (predominantly inhibitory) and 5-HT (predominantly excitatory) seen here in vitro were opposite to those observed in vivo with iontophoretic application, and were not reversed or abolished by the blockade of synaptic transmission. Comparisons of data between the two types of preparations showed that only the responsiveness of the irregular units to ACh and to 5-HT were significantly different: both types of responsiveness were higher in estrogen-treated than in untreated preparations. No significant difference was found in the responsiveness of regular units, or in firing patterns or firing rate. Thus, the present in vitro studies have demonstrated that SCN contains a heterogeneous population of neurons distinguishable by their electrophysiological and neuropharmacological characteristics, and that estrogen has a specific action on specic types of SCN neurons.

Evidence for two types of firing pattern during the sleep-waking cycle in the reticular thalamic nucleus of the cat

The activity of 23 neurons was recorded extracellularly in the nucleus reticularis thalami (RT) of four chronically implanted cats. Patterns of discharge were studied and their relationship to wakefulness (W), slow-wave sleep (SS), and paradoxical sleep (PS) were examined. The firing pattern was analyzed using zero-order (firing rate), first-order (interspike interval histogram), and second-order (joint interval histogram and autocorrelogram histogram) statistics. The SS bursting pattern was investigated taking into account the duration of the intervals between the bursts, the number of spikes per burst, and the duration of the bursts. Zero- and first-order characterizations during W and PS were found to be comparable. However, the joint interval histogram revealed a state-specific pattern during W for 74% of the cells. This pattern was characterized by a nonrandom occurrence of some categories of adjacent intervals. This was not found during PS. Two-thirds of the cells recorded, called “fast” neurons, exhibited firing rates higher than 15 spikes/s during W and PS. Those remaining, called “slow” neurons, showed a mean discharge rate lower than 10 spikes/s. In SS “fast” neurons fired long-duration bursts with interburst intervals generally shorter than 1 s. Conversely, “slow” neurons discharged shortduration bursts interrupted by long interburst intervals (greater than 1 s). Nevertheless, both types of cells had the same number of spikes within the burst and a similar intraburst pattern. Approximately half of the cells studied depicted a “slow rhythm” in the autocorrelogram histogram. Its periodicity was independent of firing rates and behavioral states.

Electrophysiological investigation of medullary neurons connected with lateral line organs of the catfish (Ictalurus nebulosus)

Unit responses in the acoustic-lateral region of the medulla to electrical and mechanical stimulation of the lateral line organs were investigated in acute experiments on curarized catfish. Of the total number of neurons 70% possessed spontaneous activity. An electrical stimulus evoked a tonic response both in spontaneously active and in "silent" cells. Three main types of firing pattern of the neurons were distinguished: fast-adapting, slow-adapting, and grouped. As regards the relation of the neurons to polarity of the stimulus they were subdivided into two groups. The thresholds of unit responses to electrical stimulation varied considerably: from 2.5·10−9 to 5·10−12 A/mm2. The effect of intensity of the electrical stimulation on unit responses in the medulla is analyzed. The precise dependence of on- and off-responses of each neuron on stimulus intensity of any polarity was determined. The neurons were shown to be sensitive to both electrical and mechanical stimuli. It is postulated that this phenomenon is due to convergence of impulses from electrical and mechanical receptors of the lateral line on the neurons. The properties of the central neurons are compared with those of the peripheral electroreceptor system in catfish.

Single Auditory Units in the Superior Olivary Complex: I: Responses to Sounds and Classifications Based on Physiological Properties

Response properties to sounds were examined in single auditory units in the superior olivary complex and the ventral nucleus of the lateral lemniscus. Units were divided into ten ‘classes’; four classes were defined by single properties (spike waveshape or the timing of responses to sound bursts) and the remaining six classes were defined by which ear excited or inhibited the units. Units were also divided according to the types of poststimulus-time histograms they produced in response to sound bursts, and they were separately divided according to the shape of their inter-spike interval histograms. These latter two groupings were highly correlated with each other and with unit class, and were combined into a single classification scheme called ‘firing-pattern type’.Units were divided into six groups based on the shapes of their tuning curves; data on the bandwidths of tuning curves are also presented. Data are presented on spontaneous firing rate, thresholds to best-frequency tones, and latency of responses to clicks. Spontaneous firing rate was found to be correlated with firing-pattern type and best frequency.We discuss the differences between our unit categories and previously reported unit categories, and the possibility that some units may be fibers. Neural mechanisms which might bring about the correlation of firing-pattern type with spontaneous rate are also discussed. Finally, we note which unit categories appear likely to correspond to neural populations which can be distinguished anatomically.

RELATION OF DISCHARGE FREQUENCY TO CONDUCTION VELOCITY IN PYRAMIDAL TRACT NEURONS.

RELATION OF DISCHARGE FREQUENCY TO CONDUCTION VELOCITY IN PYRAMIDAL TRACT NEURONS.