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Previous Article | Next Article
Volume 16, Number 15, Issue of August 1, 1996 pp. 4684-4695
Copyright ©1996 Society for NeuroscienceFunctional GABAergic Synaptic Connection in Neonatal Mouse Barrel Cortex
Ariel Agmon1, Greg Hollrigel1, and Diane K. O'Dowd1, 2 Departments of 1 Anatomy and Neurobiology and 2 Developmental and Cell Biology, University of California, Irvine, California 92717
ABSTRACT
Intracortical inhibition is crucial to proper functioning of the mature neocortex, yet, paradoxically, is reported to be rare or absent in the neonatal animal. We reexamined this issue by recording whole-cell postsynaptic currents (PSCs) of barrel cortex neurons in thalamocortical brain slices from neonatal mice. Monosynaptic, excitatory thalamocortical responses were elicited in layers V/VI neurons as early as postnatal day 0 (P0, the first 24 hr after birth) and in presumptive layer IV as early as P2. At very low stimulation frequencies, the monosynaptic response was invariably followed by a prolonged (up to 1 sec) synaptic barrage, which fatigued at stimulus repetition rates of 2/min or higher. This barrage consisted of postsynaptic responses to spiking activity in neighboring cortical cells, because (1) it could also be evoked by intracortical stimulation in coronal slices and (2) it was abolished by antagonists to NMDA receptors (NMDARs), even when NMDARs on the recorded cell were under a voltage-dependent block. Some of the larger polysynaptic events changed polarity at a negative reversal potential and were blocked by GABAA receptor (GABAAR) antagonists, with a concurrent enhancement of the extracellular field potential, indicating that they were GABAAR- mediated, Cl-dependent inhibitory PSCs (IPSCs). We conclude that a network of functional intracortical GABAAR-mediated synaptic connections exists from the earliest postnatal ages, although it gives rise to responses that differ from mature IPSCs in reversal potential and latency.
Key words: GABA synapses; synaptic inhibition; postnatal development; barrel cortex; whole-cell recording; synaptic fatigue
INTRODUCTION
GABA-using inhibitory cells comprise, depending on species, 15-25% of the total neuronal population of the mammalian cerebral cortex (Hendry et al., 1987; Meinecke and Peters, 1987
Unlike the situation in the mature cortex, the neonatal cortex is reported to be nearly devoid of structural and functional inhibitory connections. Anatomical studies indicate paucity of axosomatic (putative inhibitory) synaptic contacts in first-week neocortex (Blue and Parnavelas, 1983
MATERIALS AND METHODS
Slice preparation and maintenance. Timed pregnant ICR mice dams were monitored at 12 hr intervals to determine time of birth. The first 24 hr after birth were designated P0. Pups were anesthetized by cooling on ice (P4 and younger) or by halothane inhalation (P5 and older) and were decapitated, and the brain was removed into ice-cold artificial cerebrospinal fluid (ACSF) (see below for composition). Brain slices (500 µm thick) were cut on a vibrating tissue slicer in a plane that preserves thalamocortical connectivity (Agmon and Connors, 1991ACSF and drug application. ACSF contained (in mM): 126 NaCl, 3 KCl, 1.25 NaH2PO4, 1.3 MgSO4, 2.5 CaCl2, 26 NaHCO3, and 20 dextrose, equilibrated with a 95:5 mixture of O2/CO2 to pH 7.4. CaCl2 was added to the solution just before use. Osmolarity of the final solution was 305 ± 5 mOsm. The drugs that were used were D(
)-2-amino-5-phosphonopentanoic acid (APV), 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), and bicuculline methochloride (BMC), all from RBI (Natick, MA), and they were applied by superfusing the slice with the appropriate concentration of drug dissolved in oxygenated ACSF. When CNQX was used, 1 mM glycine (Sigma, St. Louis, MO) was added to the ACSF .
Whole-cell pipettes and internal solutions. Whole-cell recording pipettes were pulled on a horizontal puller (Sutter Instrument, Novato, CA) from thin-wall, 1.5 mm outer diameter borosilicate glass tubing without filament (WPI, Sarasota, FL) and not modified further. Pipette resistance was typically 10 M
(usable range was 5-20 M
Electrophysiological recordings and data acquisition. At the start of each experiment, an extracellular field potential pipette (filled with 0.9% NaCl) was placed in layer IV, or in very young animals, in the middle cortical layers. Field potentials were recorded at a gain of 1000× and filtered between 0.1 Hz and 5 KHz. In thalamocortical slices, a tungsten microelectrode (AM Systems, Everett, WA) was placed in VB or at the border of VB and RTN, and 0.1 msec cathodal voltage pulses of increasing intensity were delivered at 30 sec intervals. The positions of the stimulating and recording pipettes were adjusted to achieve the largest amplitude field response to a 5-12 V stimulus (Agmon and Connors, 1991
After the seal was ruptured, current responses to a series of 0.5 sec voltage steps at 10 mV intervals were immediately recorded. These responses, taken before any effects of the backfilled cesium-based QX-314-containing solution were apparent, were used later to determine the resting potential, input resistance, and firing threshold of the cells (see below). Synaptic stimulation was usually initiated at least 20 min after seal rupture to allow for diffusion of the cesium-based solution into the cell. Before this equilibration, current traces recorded during a depolarizing voltage step were noisy and contaminated with spiking activity, and it was not possible to demonstrate reversal of synaptic responses. Extracellular stimuli, at the intensity determined previously when recording the field potential, were delivered with interstimulus intervals of 20-300 sec, and synaptic currents were recorded at several different holding potentials. Extracellular field potential responses were recorded simultaneously with the current responses.
Data were digitized directly and stored in a desktop computer, using the CED data acquisition system (Cambridge, UK). Digital sampling frequency was typically 5 kHz, but for particularly long sweeps, sampling frequency had to be reduced. Stimuli protocols for voltage steps and for synaptic activation were generated using a Master-8 stimulator (AMPI, Jerusalem, Israel).
Junction potential corrections. To correct for junction potentials introduced by our recording solutions, we measured the voltage shift seen by an open-ended pipette when the bath solution was changed from physiological saline to an internal solution (Neher, 1992
Data analysis. Steady-state current responses to 0.5 sec subthreshold voltage steps were used to construct the I-V relationship of the cell. Input impedance (Rin) was calculated as the slope of the I-V curve at
RESULTS
Membrane properties of neonatal cortical cells
The present report is based on whole-cell current records from a sample of 116 neocortical neurons from 34 animals, newborn to 8-d-old. The P0-8 period is defined as ``neonatal'' for the purpose of this report; it is characterized by a predominantly excitatory short-latency response of layer IV neurons to thalamic stimulation (Agmon and O'Dowd, 1992Figure 1 summarizes the resting potentials and input resistances of the cells, grouped according to age and laminar position. There was a distinct difference between layer IV and deep layers neurons. As in CA1 neurons (Spigelman et al., 1992
Fig. 1. Age-dependent changes in electrophysiological parameters. Resting potentials (top) and input resistance (bottom) of sampled cells, pooled into three age groups for layers V/VI (L. V/VI) cells (left), and into two age groups for layer IV (L. IV) cells (right). (The number of layer IV cells in the youngest age group was too small for analysis.) The center line represents the median value; box and whisker lines represent the 25-75th and 5-95th percentiles, respectively. Asterisks denote a statistical significance between one age group and the immediately preceding one, as determined by a two-tailed Mann-Whitney test, with p < 0.05 and p < 0.01 denoted by one asterisk and two asterisks, respectively. The number of cells included in each group is indicated in parentheses; the discrepancy between the numbers in the upper and lower panels reflects cells for which resting potentials could not be determined, as explained in Materials and Methods.
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Mono- and polysynaptic responses
Neonatal cortical cells exhibited a complex response to a thalamocortical volley. The initial component of the response (Fig. 2, arrowheads), exhibited by 82% of layer IV cells and 91% of layers V/VI cells sampled, had a latency of 6-13 msec from stimulus onset (at room temperature) and was identified as monosynaptic by the negligible (<1 msec) trial-to-trial variance in this latency, demonstrated by the superimposed expanded traces in Figure 2B. The monosynaptic response was inward-going at all negative holding potentials and often exhibited a nonlinear voltage dependency typical of NMDAR-mediated currents (see Fig. 5B, arrowheads), consistent with previous pharmacological evidence (Agmon and O'Dowd, 1992
Fig. 2. Monosynaptic and polysynaptic components of thalamocortical responses. A, Whole-cell postsynaptic current responses of a layer V/VI P2 neuron (P2, L. V/VI) to thalamocortical stimulation. Holding potential indicated to the left of the trace. The monosynaptic response (its peak marked by arrowhead) was followed by a barrage of long-latency events (selected events marked by asterisks), in this case lasting >600 msec. Boxed region is expanded in B. B, Superimposed responses to repeated thalamocortical stimulation, at an expanded time base. Compare the small variance in the latency of the monosynaptic component (onset marked by arrowhead) with the jitter in the onset of the polysynaptic events (double arrow).
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Fig. 5. Reversal potentials of unitary polysynaptic events. A, Whole-cell postsynaptic currents in a P5 neuron (P5, L. V/VI) that exhibited unitary polysynaptic events (largest events marked by asterisks) but no monosynaptic response. B, Records from a P6 neuron (P6, L. IV) that exhibited a monosynaptic response (onset marked by arrowheads) followed by a polysynaptic barrage (largest polysynaptic events marked by asterisks). The monosynaptic response was inward at all negative potentials and had a voltage dependency characteristic of NMDA receptor-mediated currents. C, The largest polysynaptic events in the P5 cell (asterisks in A) reversed at approximately
[View Larger Version of this Image (18K GIF file)]
The monosynaptic response of 94% of all cells that responded monosynaptically to thalamocortical stimulation (including cells as young as P0) was followed by a barrage of long-latency synaptic events (Fig. 2A, asterisks), in some cases lasting >1 sec (Fig. 3). Two additional cells exhibited a long-lasting barrage that was not preceded by a monosynaptic response (one shown in Fig. 5A). As demonstrated by the superimposed traces in Figure 2B, there was considerable trial-to-trial variability in the temporal pattern of this barrage as well as its onset (range indicated by double-sided arrow), indicating that it was most likely a barrage of polysynaptic events, i.e., synaptic responses to action potentials elicited in surrounding cortical neurons, the latter directly or indirectly activated by the thalamic input. Two alternative interpretations of the prolonged barrage, however, were considered. The first was that it was a monosynaptic response to oscillatory activity in the thalamus, resulting from the reciprocal but inverse connectivity between VB and RTN (Huguenard and Prince, 1994
Fig. 3. The long-latency PSCs depended on activation of presynaptic neurons through both NMDA and non-NMDA receptors. A, Whole-cell currents in response to thalamocortical stimulation of a P6 neuron (P6, L. IV), in control ACSF (light traces), after addition of 12.5 µM APV (marked by arrow) and after drug washout (heavy traces). Holding potentials indicated to the left of each set of traces. The NMDA antagonist reversibly blocked most of the polysynaptic responses, even at
[View Larger Version of this Image (20K GIF file)]
To test the first possibility, we recorded postsynaptic responses to intracortical stimulation from 21 neurons (ages P0-7) in coronal slices, which lacked the oscillatory thalamic circuitry. Ninety percent of all cells sampled in coronal slices responded to intracortical stimulation with a prolonged barrage (for examples see Fig. 7), indicating that the barrage originated within the cortex. The second possibility was that the barrage was attributable to temporally dispersed transmitter release from immature thalamocortical axon terminals. Had this been the case, then events in the barrage should have had the same pharmacological sensitivities as monosynaptic thalamocortical responses, i.e., they should have been sensitive to non-NMDA antagonists at all holding potentials, but to NMDA antagonists only at depolarized holding potentials (Agmon and O'Dowd, 1992
Fig. 7. The larger polysynaptic events were GABAergic. A, Superimposed whole-cell current responses of a P3 neuron (P3, L. V/VI) to intracortical stimulation, in control ACSF (light trace) and after addition of 6 µM of the GABAAR antagonist BMC (heavy trace). The polysynaptic events (asterisk) were blocked by the drug, revealing a barrage of small, presumably excitatory events. The monosynaptic response (arrowhead) was slightly enhanced, indicating no deterioration in the recording. B, Postsynaptic currents in a P7 neuron (P7, L. IV). Addition of 2 µM BMC (heavy trace) caused a de novo appearance of inward, presumably excitatory synaptic events (asterisk). C, D, Averaged field potentials recorded during the experiments shown in A and B, respectively. Heavy trace is the recording taken after drug washout, indicating that the BMC effect was reversible. In both experiments the drug caused a pronounced increase in field potential amplitude, indicating a disinhibitory effect of the drug and therefore an inhibitory effect of GABA.
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Frequency-dependent fatigue of the polysynaptic barrage
The polysynaptic barrage exhibited a pronounced frequency-dependent fatigue (Fig. 4). At a stimulation rate of 33 mHz (2/min) or higher, consecutive trials elicited an increasingly delayed and shorter barrage, leading to its almost complete failure within two to four trials (Fig. 4A). The fatigue was reversible: reducing the rate of stimulation to 5.5 mHz fully restored the response to its previous level at the same stimulation frequency (Fig. 4B). Even at 5.5 mHz (i.e., 1/3 per min), however, some fatigue was present, because breaks in the stimulation protocol lasting 5 min or more were followed by an even larger response (not shown). At 33 mHz, the monosynaptic response was unchanged or even enhanced (Fig. 4C,D, arrowheads; the heavy trace is the fatigued response); thus the fatigue was not attributable to a reduction in the excitatory drive from the thalamus.
Fig. 4. Fatigue of the long-latency responses. Whole-cell postsynaptic responses of two layer IV neurons from different P6 animals (P6, L IV). A, Superimposed first, third, and fourth responses to thalamocortical stimulation at 33 mHz (2/min); note that the polysynaptic events (asterisks in first and third trials) are virtually gone by the fourth repetition of the stimulus. B, Representative responses to thalamocortical stimuli from three consecutive trains, delivered at 5.5 mHz and 33 mHz and again at 5.5 mHz. Note the dramatic but reversible fatigue of the polysynaptic responses (asterisks) at 33 mHz. The boxed regions are expanded in C and D, showing that the monosynaptic responses (arrowheads) were unchanged or even enhanced when the polysynaptic events were maximally fatigued (heavy line represents fatigued response).
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Reversal potentials of the polysynaptic responses
When the membrane potential was clamped at increasingly depolarized voltages, at least some of the larger events comprising the polysynaptic barrage reversed polarity from inward to outward currents (Fig. 5A,B, asterisks). The reversal occurred at negative holding potentials at which the excitatory, monosynaptic response was still inward-going (Fig. 5B, arrowheads). To obtain a quantitative estimate of the reversal potential of these PSCs, we chose 12 P3-7 cells, all recorded with cesium gluconate as the main salt and with QX-314 in the pipette, for which it was possible to identify putative unitary PSCs (uPSCs), i.e., responses to individual presynaptic action potentials. We defined putative uPSCs as events with a short (3-5 msec) rising phase lacking any inflection points and followed by an asymptotic decay phase (Fig. 5A,B, asterisks). There was considerable variability in the sizes of these events in any given trial, probably attributable to variability in neurotransmitter release among different presynaptic axons and during sequential spikes of a single axon. To select a uniform population of uPSCs for reversal potential analysis, we chose from each cell the largest event at each holding potential and plotted its amplitude against the holding potentials. The I-V plots for all 12 cells could be fitted with linear regression lines with a good quality of fit (r2 >0.98; Fig. 5C,D). The slope and zero-intercept of the linear regression line provided an estimate of the synaptic conductance and reversal potential, respectively, of each uPSC. The reversal potentials fell into two nonoverlapping groups (Fig. 6). In the P3-5 age group (n = 4), they were
Fig. 6. Reversal potentials plotted against synaptic conductance of 12 unitary PSCs. UPSCs in the P3-5 group reversed at or more positive to
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To predict the physiological effect of these PSCs on neonatal cortical cells, we compared the reversal potential of the uPSCs, EuPSC, with the resting potential in the same cells, Vrest, on a cell-by-cell basis, for three P3-5 and six P6-7 cells for which both quantities were available. In all P3-5 cells, EuPSC was more positive than Vrest by 12 mV, on average. In five of six P6-7 cells, EuPSC was more negative than Vrest by 7 mV, on average (in one P7 cell, EuPSC was 7 mV more positive than resting potential). Thus, under physiological conditions, these large synaptic events would be expected to be mostly depolarizing in P5 and younger animals and mostly hyperpolarizing in P6 and older animals.
Pharmacology of the polysynaptic responses
The negative reversal potential of the uPSCs suggested that they were Cl-dependent events activated by GABA. We tested the sensitivity of the neonatal long-latency PSCs to the GABAAR antagonist BMC (Fig. 7). The drug had a clear effect in five out of six cells from three animals. Of these, in two P3 cells the large polysynaptic events were blocked by BMC, revealing a barrage of small-amplitude events (Fig. 7A, heavy trace). These small events were presumably glutamate-meditated, although we cannot rule out the possibility that they were GABAergic PSCs, which were only partially blocked by the drug. The monosynaptic excitatory event (Fig. 7A, arrowhead) was unchanged in BMC, indicating no nonspecific deterioration in preparation viability or recording quality. In three P6-7 cells, application of BMC resulted in an apparently opposite effect, the appearance de novo of a large inward synaptic current (Fig. 7B, heavy trace), suggesting an increased excitability in presynaptic neurons as a result of their release from GABAergic inhibition. In both age groups, but more prominently in the older one, the extracellular record (Fig. 7C,D) showed a pronounced and reversible increase in the long-latency negativity in layer IV after BMC application, consistent with disinhibition of the neuronal population.
DISCUSSION
Functional glutamatergic and GABAergic intrinsic connections in neonatal cortex
The major new finding reported here is the existence of functional GABAergic synaptic connections in the neonatal neocortex. These connections were expressed in our experiments as long-lasting polysynaptic barrages triggered by single thalamocortical or intracortical volleys. Long-latency, repetitive synaptic events were reported previously by Kim et al. (1995)Because both glutamatergic and GABAergic cells were presumably activated by the thalamocortical volley, the polysynaptic barrages probably consisted of both excitatory and inhibitory events. Here we presented direct evidence for inhibitory events. The existence of excitatory synaptic connections in the neonatal neocortex was nevertheless evident in the data demonstrated in Figure 7, in which application of a GABA antagonist gave rise to a large, reversible negativity in the field potential, indicative of a synchronous excitatory response in a large population of neurons and suggesting a recurrent excitatory network unchecked by inhibition. The fact that the whole-cell records showed a large inward current event only in the older animals may indicate that this excitatory network was still underdeveloped in the P3 animals.
Fatigue of polysynaptic barrage
The polysynaptic response was dramatically reduced even at low rates of repetitive stimulation. At the same rates of stimulation, the monosynaptic excitatory response was unaltered, suggesting that the fatigue was not attributable to a reduction in the thalamocortical excitatory drive. More likely, the fatigue was caused by fewer cortical cells firing in response to the same excitatory drive: in other words, by a general reduction in the excitability of the cortical neurons. The cellular mechanism underlying this effect remains to be determined. This fatigability may have contributed to the failure of previous studies to recognize the existence of inhibitory synaptic connections in the neonatal rodent neocortex.Reversal potential of neonatal uPSCs
Assuming full equilibration between the intracellular milieu and the pipette solution, and assuming a 0.75 coefficient of activity for extracellular Cl (Bormann et al., 1987Physiological effect of GABAergic PSCs
The functional effect of a synaptic input depends on its reversal potential relative to spike threshold. In P6 and older preparations, the reversal potential of the uPSCs was more negative thanThe situation in P5 and younger preparations was somewhat different. In these cases, EuPSC was equal or positive to
Maturation of short-latency intracortical inhibition
In a previous study (Agmon and O'Dowd, 1992The role of GABA in the neonatal cortex
A general feature of the embryonic and neonatal CNS is that onset of neurotransmitter synthesis and neurotransmitter receptor expression often precedes the appearance of structural and functional synaptic connections (Woodward et al., 1971
FOOTNOTES
Received Feb. 23, 1996; revised May 7, 1996; accepted May 13, 1996.
This work was supported by National Institutes of Health, U.S. Public Health Service, Grant NS30109 to D.K.O'D., with additional support from NS27501 to D.K.O'D. and from NS30109 and NS21377 to E. G. Jones. We thank Drs. Barry Connors, Edward Jones, Yasuo Kawaguchi, Paul Rhodes, and Ivan Soltesz for critical comments on earlier versions of this manuscript.
Correspondence should be sent to Dr. Ariel Agmon's present address: De- partment of Anatomy, Box 9128, West Virginia University, Morgantown, WV 26506-9128.
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