Three GABA receptor-mediated postsynaptic potentials in interneurons in the rat lateral geniculate nucleus

Abstract

Inhibition is crucial for the thalamus to relay sensory information from the periphery to the cortex and to participate in thalamocortical oscillations. However, the properties of inhibitory synaptic events in interneurons are poorly defined because in part of the technical difficulty of obtaining stable recording from these small cells. With the whole-cell recording technique, we obtained stable recordings from local interneurons in the lateral geniculate nucleus and studied their inhibitory synaptic properties. We found that interneurons expressed three different types of GABA receptors: bicuculline-sensitive GABA(A) receptors, bicuculline-insensitive GABA(A) receptors, and GABA(B) receptors. The reversal potentials of GABA responses were estimated by polarizing the membrane potential. The GABA(A) receptor-mediated responses had a reversal potential of approximately -82 mV, consistent with mediation via Cl(-) channels. The reversal potential for the GABA(B) response was -97 mV, consistent with it being a K(+) conductance. The roles of these GABA receptors in postsynaptic responses were also examined in interneurons. Optic tract stimulation evoked a disynaptic IPSP that was mediated by all three types of GABA receptors and depended on activation of geniculate interneurons. Stimulation of the thalamic reticular nucleus evoked an IPSP, which appeared to be mediated exclusively by bicuculline-sensitive GABA(A) receptors and depended on the activation of reticular cells. The results indicate that geniculate interneurons form a complex neuronal circuitry with thalamocortical and reticular cells via feed-forward and feedback circuits, suggesting that they play a more important role in thalamic function than thought previously.

Fig. 1.

A geniculate interneuron.A, Morphology of a reconstructed geniculate interneuron.B, Location of the cell in the LGN. Note that the coronal section contains no TRN. vLGN, Ventral LGN;LP, lateral posterior nucleus; OT, optic tract.C, Responses of the same interneuron to depolarizing and hyperpolarizing current pulses. The resting potential of this cell was −76 mV.

Fig. 2.

Responses of a rat geniculate interneuron to a brief bath application of GABA. A, GABA (500 μm; horizontal bar) induced a prolonged response in a geniculate interneuron, which appeared to consist of two components. B, Plotting the peak amplitudes of the early response against the membrane potential revealed its reversal potential to be −82.5 mV. C, Plotting the amplitudes of the response at 50 sec after the GABA application against the membrane potential revealed its reversal potential to be −99.0 mV. The data points in B and C were fitted by linear lines. The resting potential of this cell was −64 mV.

Fig. 3.

Responses of a rat geniculate interneuron to a brief bath application of GABA. A, A brief bath application of 500 μm GABA induced a depolarization and a hyperpolarization in an interneuron.B, The depolarization was suppressed by bath application of 20 μm bicuculline. C, Increasing bicuculline to 200 μm had little additional effect on the residual depolarization. D, Adding 1 mmsaclofen in the bath solution completely blocked the hyperpolarization.E, The response recovered after washing in the normal bath solution. The resting membrane potential of this cell was −61 mV, and the cell was held at −90 mV during the experiment.

Fig. 4.

Responses of a rat geniculate interneuron to a brief bath application of GABA. A, A brief bath application of 500 μm GABA induced a hyperpolarization in an interneuron. B, The hyperpolarization was partially blocked by bath application of 20 μm bicuculline and 2 mm saclofen.C, The residual response was completely blocked by adding 10 μm PTX in the bath solution. D, The response partially recovered after washing in the normal bath solution. The resting membrane potential of this cell was −63 mV.

Fig. 5.

Responses of a rat geniculate interneuron to a brief bath application of CACA. A, A brief bath application of 250 μm CACA induced a hyperpolarization in an interneuron. B, The hyperpolarization was partially blocked by bath application of 20 μm bicuculline.C, The residual response was completely blocked by adding 10 μm PTX in the bath solution. D, The response recovered after washing in the normal bath solution. The resting membrane potential of this cell was −69 mV.

Fig. 6.

Responses of a rat geniculate interneuron to stimulation of the optic tract. A, Single electric shock induced a prolonged EPSP in an interneuron, which could reach threshold and elicit action potentials. B, Depolarizing the cell to −5 mV revealed a prominent IPSP.C, A substantial part of the IPSP was blocked by the bath application of 20 μm bicuculline. D, The bicuculline-resistant IPSP was partially blocked by adding 1 mm saclofen to the bath solution. E, The residual IPSP was blocked by 10 μm PTX. F, The response recovered after washing in the normal bath solution. The resting membrane potential of this cell was −74 mV.

Fig. 7.

Responses of a rat geniculate interneuron to stimulation of the optic tract. A, Single electric shock induced a prolonged EPSP in an interneuron, which could reach threshold and elicit action potentials. B, Depolarizing the cell to −5 mV revealed a prominent IPSP.C, The IPSP was completely blocked by the bath application of 20 μm DNQX and 50 μmd-AP-5. D, The response recovered after washing in the normal bath solution. The resting membrane potential of this cell was −74 mV.

Fig. 8.

A geniculate interneuron.A, Morphology of a reconstructed geniculate interneuron.B, Location of the cell in the LGN. Note that the parasagittal section contains both the LGN and TRN. MG, Medial geniculate nucleus. C, Responses of the same interneuron to depolarizing and hyperpolarizing current pulses. The resting potential of this cell was −67 mV.

Fig. 9.

Responses of a rat geniculate interneuron to stimulation of the TRN. A, Single electric shock in the TRN induced a small IPSP in an interneuron.B, A train of three shocks at 250 Hz induced a larger IPSP in the same interneuron. C, The IPSP was completely blocked by the bath application of 20 μm bicuculline.D, The response recovered after washing in the normal bath solution. Note that 20 μm DNQX and 50 μmd-AP-5 were included in the bath solution during the experiment. The resting membrane potential of this cell was −66 mV.

Fig. 10.

Responses of a rat geniculate interneuron to local application of glutamate in the TRN. A, Local application of 250 μm glutamate in the TRN induced a small hyperpolarization in an interneuron. B, The hyperpolarization was completely blocked by the bath application of 20 μm bicuculline. C, The response recovered after washing in the normal bath solution. The resting membrane potential of this cell was −64 mV.

Fig. 11.

Inhibitory circuits in the thalamus.