Electrical properties of neocortical neurons in slices from children with intractable epilepsy

1996 ◽  
Vol 75 (2) ◽  
pp. 931-939 ◽  
Author(s):  
J. G. Tasker ◽  
N. W. Hoffman ◽  
Y. I. Kim ◽  
R. S. Fisher ◽  
W. J. Peacock ◽  
...  

1. The intrinsic electrical properties of human neocortical neurons were studied with current-clamp and single-electrode voltage-clamp techniques in slices obtained from children, aged 3 mo to 15 yr, undergoing surgical treatment of intractable epilepsy. Neocortical samples were classified as most or least abnormal based on clinical data. Recorded neurons were labeled with biocytin for correlation of electrical properties with morphological characteristics and laminar position. All recorded neurons were divided into three cell types--fast-spiking, low-threshold spiking (LTS) and non-LTS cells--on the basis of their electrical characteristics. 2. Fast-spiking cells generated brief, rapidly repolarizing action potentials. Most of these cells showed only weak spike-frequency adaptation. Fast-spiking cells labeled with biocytin were aspiny or sparsely spiny nonpyramidal neurons located in cortical layers 2-4. 3. LTS cells generated Ca(2+)-dependent low-threshold potentials and were the most numerous of the three cell types. Their Na(+)-dependent action potentials were broader than those of fast-spiking cells and showed marked spike-frequency adaptation. The size of low-threshold Ca2+ potentials and currents varied across cells, but they never supported more than two or, occasionally, three fast action potentials. LTS cells were pyramidal neurons located throughout cortical layers 2-6. Unlike the bursting neocortical cells described in lower mammals, LTS neurons in neocortex from children failed to generate bursts of inactivating Na+ action potentials. 4. Non-LTS cells also had relatively broad Na(+)-dependent action potentials and showed spike-frequency adaptation, but they did not generate detectable low-threshold potentials or currents. Non-LTS cells were also pyramidal neurons located throughout layers 2-6. 5. The electrical properties of cells from different age groups (< or = 1, 2-8, and 9-15 yr) and from most-abnormal and least-abnormal tissue samples were compared. A statistically significant trend toward a lower input resistance, a faster membrane time constant, and a decreased spike duration was observed with increasing age. There were no significant differences between the electrical properties of cells from the most-abnormal tissue and cells from the least-abnormal tissue. 6. These data indicate that the intrinsic electrical properties of neocortical neurons from children vary according to cell morphology and change with increasing age, as has been observed in rodent and feline neocortical neurons. No obvious evidence of epileptogenicity was detected in the intrinsic electrical properties of any of the neurons studied.

1992 ◽  
Vol 67 (2) ◽  
pp. 350-363 ◽  
Author(s):  
N. M. Lorenzon ◽  
R. C. Foehring

1. Human neocortical neurons fire repetitively in response to long depolarizing current injections. The slope of the relationship between average firing frequency and injected current (f-I slope) was linear or bilinear in these cells. The mean steady-state f-I slope (average of the last 500 ms of a 1-s firing episode) was 57.8 Hz/nA. The instantaneous firing rate decreased with time during a 1-s constant-current injection (spike frequency adaptation). Also, human neurons exhibited habituation in response to a 1-s current stimulus repeated every 2 s. 2. Afterhyperpolarizations (AHPs) reflect the active ionic conductances after action potentials. We studied AHPs with the use of intracellular recordings and pharmacological manipulations in the in vitro slice preparation to 1) gain insight into the ionic mechanisms underlying the AHPs and 2) elucidate the role that the underlying currents play in the functional behavior of human cortical neurons. 3. We have classified three AHPs in human neocortical neurons on the basis of their time courses: fast, medium, and slow. The amplitude of the AHPs was dependent on stimulus intensity and duration, number and frequency of spikes, and membrane potential. 4. The fast AHP had a reversal potential of -65 mV and was eliminated in extracellular Co2+, tetraethylammonium (TEA) or 4-aminopyridine, and intracellular TEA or CsCl. These manipulations also caused an increase in spike width. 5. The medium AHP had a reversal potential of -90 to -93 mV (22-24 mV hyperpolarized from mean resting potential). This AHP was reduced by Co2+, apamin, tubocurare, muscarine, norepinephrine (NE), and serotonin (5-HT). Pharmacological manipulations suggest that the medium AHP is produced in part by 1) a Ca-dependent K+ current and 2) a time-dependent anomalous rectifier (IH). 6. The slow AHP reversed at -83 to -87 mV (14-18 mV hyperpolarized from mean resting potential). This AHP was diminished by Co2+, muscarine, NE, and 5-HT. The pharmacology of the slow AHP suggests that a Ca-dependent K+ current with slow kinetics contributes to this AHP. 7. The currents involved in the fast AHP are important in spike repolarization, control of interspike interval during repetitive firing, and prevention of burst firing. Currents underlying the medium and slow AHPs influence the interspike interval during repetitive firing and produce spike frequency adaptation and habituation.


2003 ◽  
Vol 89 (3) ◽  
pp. 1541-1566 ◽  
Author(s):  
Lionel G. Nowak ◽  
Rony Azouz ◽  
Maria V. Sanchez-Vives ◽  
Charles M. Gray ◽  
David A. McCormick

To facilitate the characterization of cortical neuronal function, the responses of cells in cat area 17 to intracellular injection of current pulses were quantitatively analyzed. A variety of response variables were used to separate the cells into subtypes using cluster analysis. Four main classes of neurons could be clearly distinguished: regular spiking (RS), fast spiking (FS), intrinsic bursting (IB), and chattering (CH). Each of these contained significant subclasses. RS neurons were characterized by trains of action potentials that exhibited spike frequency adaptation. Morphologically, these cells were spiny stellate cells in layer 4 and pyramidal cells in layers 2, 3, 5, and 6. FS neurons had short-duration action potentials (<0.5 ms at half height), little or no spike frequency adaptation, and a steep relationship between injected current intensity and spike discharge frequency. Morphologically, these cells were sparsely spiny or aspiny nonpyramidal cells. IB neurons typically generated a low frequency (<425 Hz) burst of spikes at the beginning of a depolarizing current pulse followed by a tonic train of action potentials for the remainder of the pulse. These cells were observed in all cortical layers, but were most abundant in layer 5. Finally, CH neurons generated repetitive, high-frequency (350–700 Hz) bursts of short-duration (<0.55 ms) action potentials. Morphologically, these cells were layer 2–4 (mainly layer 3) pyramidal or spiny stellate neurons. These results indicate that firing properties do not form a continuum and that cortical neurons are members of distinct electrophysiological classes and subclasses.


1988 ◽  
Vol 60 (3) ◽  
pp. 869-878 ◽  
Author(s):  
R. Llinás ◽  
J. Lopez-Barneo

1. The long-term adaptation of repetitive firing in guinea pig superior colliculus neurons was studied in a mesencephalic slice preparation using intracellular recording techniques. 2. This long-term adaptation was characterized by a decrease in the number of action potentials generated by a depolarizing pulse of constant amplitude applied at frequencies of 0.5-2 Hz. Long-term adaptation appeared in all cells tested regardless of whether they showed short-term spike frequency adaptation during each pulse. 3. Long-term adaptation had a close-to-exponential time course with a time constant of 4.085 +/- 0.675 s (mean +/- SD, n = 8). This phenomenon developed more rapidly as the stimulus frequency increased and was paralleled by a progressive hyperpolarization of the membrane potential which, at the termination of the train of stimuli, remained 6-10 mV more negative than the resting value. 4. The hyperpolarization and the spike frequency adaptation recovered spontaneously in approximately 60 s. The time constant of recovery was 14.66 +/- 1.189 s (n = 4). 5. The afterhyperpolarization (AHP) was also paralleled by a decrease in the input resistance of the cells. This response and the adaptation disappeared after removal of Ca2+ or after addition of Cd2+ to the external solution. This suggests that Ca2+ entry during trains of action potentials activates a Ca2+-dependent K+ conductance with an unusually slow kinetics. 6. This conductance appears to differ from other Ca2+-dependent K+ conductances in that it was blocked by 4-aminopyridine. 7. The properties of this long-term adaptation are remarkably similar to those reported for visual habituation; thus this newly described K+ conductance may be pertinent to the understanding of this behavioral phenomenon.


2005 ◽  
Vol 93 (2) ◽  
pp. 1111-1118 ◽  
Author(s):  
V. F. Descalzo ◽  
L. G. Nowak ◽  
J. C. Brumberg ◽  
D. A. McCormick ◽  
M. V. Sanchez-Vives

Fast-spiking (FS) neurons are a class of inhibitory interneurons classically characterized as having short-duration action potentials (<0.5 ms at half height) and displaying little to no spike-frequency adaptation during short (<500 ms) depolarizing current pulses. As a consequence, the resulting injected current intensity versus firing frequency relationship is typically steep, and they can achieve firing frequencies of ≤1 kHz. Here we have investigated the properties of FS neurons discharges on a longer time scale. Twenty second discharges were induced in electrophysiologically identified FS neurons by means of current injection either with sinusoidal current or with square pulses. We found that virtually all FS neurons recorded in cortical slices do show spike-frequency adaptation but with a slow time course (τ = 2–19 s). This slow time course has precluded the observation of this property in previous studies that used shorter pulses. Contrary to the classical view of FS neurons functional properties, long-duration discharges were followed by a slow afterhyperpolarization lasting ≤23 s. During this postadaptation period, the excitability of the neurons was decreased on average for 16.7 ± 6.8 s, therefore rendering the cell less responsive to subsequent afferent inputs. Slow adaptation is also reported here for FS neurons recorded in vivo. This longer time scale of adaptation in FS neurons may be critical for balancing excitation and inhibition as well as for the understanding of cortical network computations.


Sign in / Sign up

Export Citation Format

Share Document