The Journal of Neurophysiology Vol. 78 No. 3 September 1997, pp. 1743-1747
Copyright ©1997 by the American Physiological Society

RAPID COMMUNICATION

Selective Cholinergic Modulation of Cortical GABAergic Cell Subtypes

Yasuo Kawaguchi

Laboratory for Neural Circuits, Bio-Mimetic Control Research Center, The Institute of Physical and Chemical Research (RIKEN), Shimoshidami, Moriyama, Nagoya 463, Japan

	ABSTRACT

Abstract Introduction Methods Results Discussion References

Kawaguchi, Yasuo. Selective cholinergic modulation of cortical GABAergic cell subtypes. J. Neurophysiol. 78: 1743-1747, 1997. Acetylcholine from the basal forebrain and -aminobutyric acid (GABA) from intracortical inhibitory interneurons exert strong influence on the cortical activity and may interact with each other. Cholinergic or muscarinic agonists indeed induced GABAergic postsynaptic currents in pyramidal cells by exciting inhibitory interneurons that have recently been classified into several distinct subtypes on the basis of the physiological, chemical, and morphological criteria. Cholinergic effects on GABAergic cell subtypes were investigated of rat frontal cortex by in vitro whole cell recording with intracellular staining in frontal cortex of young rats. GABAergic cell subtypes were identified physiologically by firing responses to depolarizing current pulses and immunohistochemically as containing parvalbumin, somatostatin, vasoactive intestinal polypeptide (VIP), or cholecystokinin (CCK). Carbachol (10 µM) or (+)-muscarine (3 µM) affected the activities of peptide-containing GABAergic cells with regular- or burst-spiking characteristics, but not of GABAergic cells with fast-spiking characteristics containing the calcium-binding protein parvalbumin orGABAergic cells with late-spiking characteristics. Somatostatin- or VIP-immunoreactive cells were depolarized with spike firing. CCK-immunoreactive cells were affected heterogeneously by cholinergic agonists. Larger CCK cells were hyperpolarized, followed by a slow depolarization, whereas smaller CCK cells were only depolarized. These results suggest that the excitability of cortical GABAergic cell subtypes is differentially regulated by acetylcholine. Differences in cholinergic responses suggest a distinct functional role of each GABAergic cell subtype.

	INTRODUCTION

Abstract Introduction Methods Results Discussion References

In the neocortex, acetylcholine and -aminobutyric acid (GABA) are released from afferent fibers originating in basal forebrain cells and from the axons of intrinsic neurons, respectively. Acetylcholine causes depolarizations and increases in input resistance of cortical cells slowly (Krnjevic et al. 1971; McCormick and Prince 1986; Woody et al. 1978) and enhances the response selectivity to sensory stimulation (McKenna et al. 1989; Metherate et al. 1988; Murphy and Sillito 1991). It is suggested that GABA has a role in shaping neuronal receptive fields and response profiles (Sillito 1992).

Thus both acetylcholine and GABA are considered to regulate the response selectivity by changing membrane potentials and firing patterns of cortical cells, and they may interact with each other synergistically. Acetylcholine indeed induces inhibitory postsynaptic potentials in neocortical (McCormick and Prince 1986) and hippocampal (Behrends and ten Bruggencate 1993; Pitler and Alger 1992) pyramidal cells indirectly, through cortical GABAergic cells, which have recently been classified into several distinct subtypes on the basis of the physiological, chemical, and morphological criteria in rat frontal cortex (Kawaguchi and Kubota 1996). These findings raised the following three questions. 1) Are physiologically and morphologically identified GABAergic cells activated directly by acetylcholine? 2) Which GABAergic cell subtypes are excited by acetylcholine? 3) Are there any differences in cholinergic modulations among GABAergic cell subtypes? To answer these questions, cholinergic induction of GABAergic inhibitory postsynaptic currents (IPSCs) in pyramidal cells and cholinergic effects onGABAergic cell subtypes of rat frontal cortex were investigated in the present experiments.

	METHODS

Abstract Introduction Methods Results Discussion References

Sections of rat frontal cortex 200 µm thick (18-22 days postnatal) were cut and put into a solution composed of (in mM) 124.0 NaCl, 3.0 KCl, 2.4 CaCl₂, 1.2 MgCl₂, 26.0 NaHCO₃, 1.0 NaH₂PO₄, and 10.0 glucose (Kawaguchi and Kubota 1996). Cells were recorded from frontal cortex (medial agranular cortex and anterior cingulate cortex) in whole cell mode at 30°C with the use of a ×40 water-immersion objective. Electrode solution for the voltage-clamp recording consisted of (in mM) 120 cesium methanesulfonate, 5.0 KCl, 10.0 ethylene glycol-bis(-aminoethyl ether)-N,N,N,N-tetraacetic acid (EGTA), 1.0 CaCl₂, 2.0 MgCl₂, 4.0 ATP, 0.3 guanosine 5-triphosphate (GTP), 8 N-2-hydroxyethylpiperazine-N-2-ethanesulfonic acid (HEPES), 5.0 lidocaine N-ethyl bromide (QX314), and 20 biocytin. The solution for the current-clamp recording consisted of (in mM) 115 potassium methylsulfate, 5.0 KCl, 0.5 EGTA, 1.7 MgCl₂, 4.0 ATP, 0.3 GTP, 8.5 HEPES, and 17 biocytin. Recordings were made in continuous single-electrode voltage-clamp mode or bridge mode with the use of an Axoclamp-2B (Axon Instruments). Drugs were applied by changing the solution superfusing the slice to one that contained the drug. Drugs used were D-2-amino-5-phosphonovaleric acid (APV; Tocris), atropine(Sigma), ()-bicuculline methiodide (Sigma), carbachol(Sigma), 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX; Tocris),(+)-muscarine chloride (Sigma), and tetrodotoxin (TTX;Sankyo).

The slices were fixed with 4% paraformaldehyde and 0.2% picric acid. The slices were incubated overnight with either one or a mixture of two of the following: a mouse monoclonal antibody against gastrin/cholecystokinin (CCK) (CURE/UCLA/DDC Antibody/RIA Core; 1:5,000), a mouse monoclonal antibody against parvalbumin (Sigma; 1:2,000), a rat monoclonal antibody against somatostatin (Chemicon; 1:500), a rabbit antiserum against parvalbumin (Swant; 1:500), and rabbit antiserum against vasoactive intestinal polypeptide (VIP; Incstar; 1:1,000). The slices were then incubated in either one or a mixture of two of the secondary antibodies conjugated with dichlorotriazinyl-aminofluorescence-dihydrochloride or 7-amino-4-methylcoumarin-3-acetic acid (Chemicon; 1:100) for 4 h and Texas Red-avidin (Amersham; 1:2,000) for 90 min. After fluorescence observations the slices were reacted with avidin-biotin-peroxidase complex and 3,3-diaminobenzidine tetrahydrochloride. Data are given as means ± SD.

	RESULTS

Abstract Introduction Methods Results Discussion References

Spontaneous outward-going currents were recorded at holding potentials of 0 mV in identified pyramidal cells in a solution containing blockers of excitatory transmission (20 µM CNQX and 50 µM APV; Fig. 1). Because of their abolition by the GABA_A receptor antagonist bicuculline (10 µM), these outward-going currents were considered to be GABAergic IPSCs (Salin and Prince 1996).

View larger version (42K): [in this window] [in a new window]   FIG. 1. Cholinergic induction of inhibitory postsynaptic currents in pyramidal cells through muscarinic excitation of GABAergic intrinsic cells in the rat frontal cortex. Pyramidal cells were voltage clamped at 0 mV in a solution containing 20 µM 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and 50 µM D-2-amino-5-phosphonovaleric acid (APV). A: bath-applied carbachol (10 µM) increased the frequency and the magnitude of the outward currents at 0 mV in pyramidal cells. B1: both spontaneously occurring and carbachol-induced outward currents were suppressed by adding the -aminobutyric acid-A (GABAA) receptor antagonist bicuculline (10 µM). B2: after washout of bicuculline, carbachol induced outward currents again in the same cell as in B1. C: carbachol-induced GABAergic currents were suppressed by application of tetrodotoxin (TTX; 1 µM). D1: carbachol induced outward currents reversibly in a pyramidal cell. D2: GABAergic outward currents could not be induced by carbachol in the presence of atropine (1 µM) in the same cell as in D1. E: GABAergic currents were induced reversibly in a pyramidal cell by muscarine (3 µM). Time calibration in B1 applies to B2 and C; time calibration in D1 applies to D2 and E. Current calibration in E is applicable to all traces.

The cholinergic agonist carbachol (10 µM) reversibly induced a prominent increase in the amplitudes and frequencies of outward currents at 0 mV in a solution containing CNQX/APV (Fig. 1, A and D; n = 15; 5 layer II/III and 10 layer V pyramidal cells). In layer II/III pyramidal cells, the frequency of IPSCs >30 pA was 3.4 ± 2.3 (means ± SD) and 16.5 ± 2.8 (SD) per second before and after the application, respectively. In layer V pyramidal cells, it was 2.8 ± 1.7 and 12.9 ± 3.9 per second before and after the application, respectively. The frequency of the outward currents >30 pA increased by 586 ± 448% in layer II/III pyramidal cells and 536 ± 468% in layer V pyramidal cells.

These carbachol-induced outward currents were blocked by prior application of bicuculline (10 µM; n = 3) and were also abolished immediately by bicuculline (10 µM; n = 6; Fig. 1B). The carbachol-induced increase of the outward currents was blocked by prior application of TTX (0.5 µM; n = 5) and was also abolished immediately by TTX (1 µM; n = 3; Fig. 1C). The changes in frequency of the outward currents >30 pA by carbachol application were 581.2 ± 686.2% in the control solution and 21.6 ± 25.6% in the solution containing TTX (n = 5).

The muscarinic receptor antagonist atropine (1 µM) blocked the carbachol-induced increase of the IPSCs (n = 3; Fig. 1D). The changes in frequency of the IPSCs brought about by carbachol application were 520.1 ± 340.5% in the control solution and 12.0 ± 63.1% in the solution containing atropine (n = 3). This showed that the muscarinic receptor was involved in the carbachol induction of IPSCs. The muscarinic receptor agonist (+)-muscarine (3 µM) indeed induced an increase of the IPSCs in a similar way to carbachol (n = 5; Fig. 1E).

The above results indicated that some GABAergic cells were excited by acetylcholine via muscarinic receptors and produced IPSCs in cortical cells. GABAergic nonpyramidal cells in the cortex are classified into several distinct subtypes with specific physiological, chemical, and morphological properties (Kawaguchi and Kubota 1996). To investigate whether cholinergic agonists directly excite GABAergic cells, cholinergic effects on each subtype of GABAergic cells were studied by application of cholinergic agonists.

Among GABAergic nonpyramidal cells, fast-spiking (FS) cells had lower input resistances than other types of cells and showed abrupt episodes of nonadapting repetitive discharges of short-duration action potentials (Fig. 2, A1 and A2). The FS cells (n = 12) had resting potentials of 72 ± 4 mV, input resistances of 135 ± 39 M, and spike widths at half-amplitude of 0.37 ± 0.07 ms. The membrane potentials of FS cells were not affected by the application of carbachol (10 µM) in a solution containing CNQX/APV (n = 8) or TTX (n = 2) or by the application of muscarine (3 µM) in the TTX-containing solution (n = 2; Fig. 2A3). Some FS cells showed an increase in membrane potential fluctuations of 1-2.5 mV during the application of carbachol in a solution containing CNQX/APV. The FS cells not depolarized by cholinergic agonists were immunoreactive for the calcium-binding protein parvalbumin (n = 8), including extended plexus cells with extended axonal arborization and multipolar dendrites.

View larger version (23K): [in this window] [in a new window]   FIG. 2. Parvalbumin-containing fast-spiking (FS) cells, as well as late-spiking (LS) neurogliaform cells, were not depolarized by a cholinergic agonist in a solution containing 20 µM CNQX and 50 µM APV. A1 and A2: spike discharges of an FS cell induced by a current pulse. Resting potential: 70 mV. Note abrupt start of nonadaptive firing from a threshold stimulus (A1). Cell also easily fired repetitive discharges with constant intervals in response to depolarizing pulses when combined with constant depolarization (A2). A3: FS cell did not depolarize, but the membrane potential showed greater fluctuation during application of carbachol (10 µM). This FS cell was immunoreactive for the calcium-binding protein parvalbumin (PV). B1 and B2: voltage responses of an LS cell induced by current pulses. Note the slowly developing ramp depolarization to the spike threshold (B1). Resting potential: 65 mV. B3: LS cell did not depolarize during application of carbachol (10 µM). Calibration in A2 also applies to A1, B1, and B2; calibration in A3 also applies to B3.

Late-spiking (LS) cells were identified by ramp depolarizations to near threshold (Fig. 2, B1 and B2). The LS cells (n = 6) had resting potentials of 64 ± 3 mV, input resistances of 238 ± 83 M, and spike widths at half-amplitude of 0.66 ± 0.13 ms. Like FS cells, LS cells were not affected by the application of carbachol in a solution containing CNQX/APV (n = 3) or TTX (n = 3; Fig. 2B3). The LS cells not depolarized by cholinergic agonists were neurogliaform cells with dendritic fields of 100-200 µm and an axonal arborization twice as wide as that of their dendritic field.

Cholinergic agonists affected the membrane potentials of nonpyramidal cells that could not be categorized as parvalbumin FS cells or LS neurogliaform cells. These cells included burst-spiking nonpyramidal cells and regular-spiking nonpyramidal cells. Burst-spiking nonpyramidal cells fired two or more spikes on slow depolarizing humps from hyperpolarized potentials. Regular-spiking nonpyramidal cells could not be categorized into the above three subgroups. These cells include GABAergic cells containing several peptides (Kawaguchi and Kubota 1996; Kubota and Kawaguchi 1997).

Carbachol depolarized somatostatin-immunoreactive cells in a solution containing CNQX/APV (n = 5), in all cases accompanied by spike firing (Fig. 3A). These somatostatin cells (n = 20) had resting potentials of 51 ± 5 mV, input resistances of 408 ± 184 M, and spike widths at half-amplitude of 0.85 ± 0.15 ms. Carbachol (n = 5) and muscarine (n = 10) in a TTX-containing solution depolarized somatostatin cells by 10-20 and 8-15 mV, respectively (Fig. 3B). Strong depolarizations in some somatostatin cells induced TTX-resistant spikes. Somatostatin cells excited by cholinergic agonists were negative for VIP (n = 19) and CCK (n = 1) and included multipolar and bitufted cells with mainly ascending axonal arbors.

View larger version (33K): [in this window] [in a new window]   FIG. 3. Cholinergic modulation of peptide-containing GABAergic cells. A-D: cholinergic excitation of somatostatin or vasoactive intestinal polypeptide (VIP)-immunoreactive cells. A and C: somatostatin cell and VIP cell were depolarized and fired spikes on application of carbachol (10 µM) in the solution containing 20 µM CNQX and 50 µM APV. Resting potential: 57 mV (A), 55 mV (C). Voltage calibration in C applies to A. B and D: somatostatin cell and VIP cell were depolarized by (+)-muscarine (3 µM) in the solution containing TTX (0.5 µM). Resting potential: 63 mV (B), 67 mV (D). Voltage calibration in D applies to B. E and F: largec h o l e c y s t o k i n i n   ( C C K ) - i m m u n o r e a c t i v ecells were hyperpolarized, followed by slow depolarization by cholinergic agonists, but a few CCK cells were depolarized. E1: large CCK cell was hyperpolarized, followed by slow depolarization by muscarine (3 µM) in the solution containing TTX (0.5 µM). Resting potential: 57 mV. E2: large CCK cell with wide axonal arbors in layer II/III, which was hyperpolarized by muscarine. F1: CCK cell (left cell of F2) was depolarized by muscarine in the solution containing TTX. Resting potential: 54 mV. Voltage calibration in E1 applies to F1. F2: 2 CCK cells with descending axonal arbors depolarized by cholinergic agonists.

VIP cells were also depolarized by carbachol in the presence of CNQX/APV (n = 11), with spike firings in most cases (n = 8; Fig. 3C). VIP cells in a TTX-containing solution were also depolarized 4-14 mV by carbachol (n = 2) or muscarine (n = 3; Fig. 3D). These VIP cells (n = 16) had resting potentials of 58 ± 6 mV, input resistances of 506 ± 184 M, and spike widths at half-amplitude of 0.69 ± 0.18 ms. VIP cells excited by cholinergic agonists were negative for somatostatin (n = 16) and included bitufted cells with descending axonal arbors corresponding to double bouquet cells.

CCK-immunoreactive cells (n = 12) were affected heterogeneously by cholinergic agonists. These CCK cells had resting potentials of 56 ± 4 mV, input resistances of 389 ± 72 M, and spike widths at half-amplitude of 0.79 ± 0.20 ms (n = 12). Some CCK cells (n = 10; resting potential 57 ± 3 mV) exhibited prominent hyperpolarizations followed by slow depolarizations (Fig. 3E1). This hyperpolarization-depolarization sequence was observed with both transient and continuous application of cholinergic agonists in both CNQX/APV- and TTX-containing solutions. Initial hyperpolarizations were 6.8 ± 3.5 mV (n = 10). Spike firings were observed during the slow depolarization in some cases. The other two CCK cells (resting potential 49 and 50 mV) did not exhibit a pronounced hyperpolarization, but were only depolarized by carbachol in a TTX-containing solution (Fig. 3F1) or with firings in a CNQX/APV-containing solution. These two types of CCK cells differed in morphology. CCK cells with prominent initial hyperpolarizations had larger somata (230 ± 55 µm², cross-sectional areas; n = 10) and extensive axonal arbors (Fig. 3E2) and were negative for parvalbumin (n = 2), somatostatin (n = 4), and VIP (n = 4). CCK cells that were only depolarized had smaller somata (125 and 138 µm²) and were negative for parvalbumin (n = 1) and somatostatin (n = 1). These two cells had mainly descending axonal arborizations (Fig. 3F2) and were thought to be double bouquet cells.

	DISCUSSION

Abstract Introduction Methods Results Discussion References

It has been previously revealed that acetylcholine excites cortical pyramidal cells slowly and cortical interneurons rapidly via muscarinic receptors (McCormick and Prince 1986). The present results show that peptide-containingGABAergic cell subtypes were directly depolarized or hyperpolarized by cholinergic agonists, via muscarinic receptors, at a concentration that induced IPSCs in pyramidal cells.

The cholinergic depolarization in pyramidal cells has a slow rate of change of membrane potential, whereas that in interneurons has a more rapid rate of depolarization (McCormick and Prince 1986). Although GABAergic cells were excited enough and fired vigorously by 10 µM carbachol, robust depolarizing responses of pyramidal cells are produced by 30-300 µM carbachol at resting potentials (Haj-Dahmane and Andrade 1996). Application of acetylcholine to pyramidal cells cause more pronounced depolarizations at depolarized potentials than at resting potentials. It was found that the slow depolarization of pyramidal cells and the rapid release of GABA in response to acetylcholine are mediated by different subtypes of muscarinic receptors (McCormick and Prince 1985). These suggest that the cholinergic excitation of pyramidal cells and interneurons may be mediated through different receptors and ionic channels.

The cholinergic depolarization of pyramidal cells has been thought to be largely produced by blockade of potassium conductances, including voltage-dependent currents (Benardo and Prince 1982; McCormick and Prince 1986), or by the activation of a voltage-dependent, cation-nonselective current (Haj-Dahmane and Andrade 1996). The rapid excitation of interneurons is associated with a decrease in membrane resistance (McCormick and Prince 1986). The muscarinic depolarization of GABAergic cells containing peptides may be caused by activating a kind of cation current. On the other hand, the muscarinic hyperpolarization observed in large CCK cells had not been reported in cortical cells. This hyperpolarization may be caused by a muscarinic receptor-mediated increase in potassium conductance, which has been observed in GABAergic interneurons of the thalamus (McCormick and Pape 1988). Muscarinic receptor subtypes are differentially localized in pyramidal and nonpyramidal cells in the hippocampus (Levey et al. 1995). Distinct cholinergic responses among cortical GABAergic cell subtypes may be due to differential expression of muscarinic receptor subtypes.

Cholinergic agonists modulated the activities of peptide-containing GABAergic cells. Somatostatin cells and VIP cells were depolarized with spike firing. Somatostatin cells are Martinotti cells with ascending axonal arbors to layer I or with wide axonal arbors. Martinotti cells make synapses on thin dendritic branches. VIP cells include double bouquet cells with descending axonal arbors; these cells make synapses on dendrites and a few on somata (Kawaguchi and Kubota 1996; Somogyi 1989). This suggests that acetylcholine regulates local dendritic excitability by GABAergic inhibition from somatostatin or VIP cells. VIP facilitates the optimal responses to visual stimulation like acetylcholine (Murphy et al. 1993). VIP released from double bouquet cells may be related to the cholinergic enhancement of the response selectivity.

Recently we identified several cortical GABAergic cell subtypes on the basis of their firing response to depolarizing current, axon arborization pattern, and coexpression of neuroactive substances (Kawaguchi and Kubota 1996). Differences in cholinergic responses suggest a distinct functional role of each GABAergic cell subtype.

	ACKNOWLEDGEMENTS

  The author thanks A. Agmon, R. Kado, Y. Kubota, and T. Shindoh for comments and N. Wada for technical assistance.

  This work was supported by the Frontier Research Program, The Institute of Physical and Chemical Research (RIKEN).

	FOOTNOTES

  Address for reprint requests: Bio-Mimetic Control Research Center, RIKEN, 2271 Anagahora, Shimoshidami, Moriyama, Nagoya 463, Japan.

  Received 20 March 1997; accepted in final form 20 May 1997.

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