Elsevier

Neuroscience

Volume 91, Issue 4, July 1999, Pages 1445-1460
Neuroscience

Burst firing in identified rat geniculate interneurons

https://doi.org/10.1016/S0306-4522(98)00665-4Get rights and content

Abstract

We used whole-cell patch recording to study 102 local interneurons in the rat dorsal lateral geniculate nucleus in vitro. Input impedance with this technique (607.0±222.4 MΩ) was far larger than that measured with sharp electrode techniques, suggesting that interneurons may be more electrotonically compact than previously believed. Consistent and robust burst firing was observed in all interneurons when a slight depolarizing boost was given from a potential at, or slightly hyperpolarized from, resting membrane potential. These bursts had some similarities to the low-threshold spike described previously in other thalamic neuron types. The bursting responses were blocked by Ni+, suggesting that the low-threshold calcium current IT, responsible for the low-threshold spike, was also involved in interneuron burst firing. Compared to the low-threshold spike of thalamocortical cells, however, the interneuron bursts were of relatively long duration and low intraburst frequency. The requirement for a depolarizing boost to elicit the burst is consistent with previous reports of a depolarizing shift of the IT activation curve of interneurons relative to thalamocortical cells, a finding we confirmed using voltage-clamp. Voltage-clamp study also revealed an additional long-lasting current that could be tentatively identified as the calcium activated non-selective cation current, ICAN, based on reversal potential and on pharmacological characteristics. Computer simulation of the interneuron burst demonstrated that its particular morphology is likely due to the interaction of IT and ICAN. In the slice, bursts could also be elicited by stimulation of the optic tract, suggesting that they may occur in response to natural stimulation. Synaptically triggered bursts were only partially blocked by Ni+, but could then be completely blocked by further addition of (±)-2-amino-5-phosphonopentanoic acid. The existence of robust bursts in this cell type suggests an additional role for interneurons in sculpting sensory responses by feedforward inhibition of thalamocortical cells.

The low-threshold spike is a mechanism whereby activity in a neuron is dependent on a prior lack of activity in that same neuron. Understanding of the low-threshold spike in the other major neuron types of the thalamus has brought many new insights into how thalamic oscillations might be involved in sleep and epilepsy. Our description of this phenomenon in the interneurons of the thalamus suggests that these network oscillations might be even more complicated than previously believed.

Section snippets

Slice preparation

Sprague–Dawley rats (Harlan, Indianapolis, IN; four to 10 weeks old; 100–300 g) were deeply anesthetized using halothane. A minimum number of animals were used to obtain the necessary results and the animals were not allowed to suffer in any way. After decapitation, the brain was quickly removed into cold (6–8°C) physiological solution containing (in mM): NaCl 126, KCl 2.5, NaH2PO4 1.25, NaHCO3 26, MgSO4 1, dextrose 20, CaCl2 2 (pH 7.35). The solution was continuously bubbled with 95% O2/5% CO2.

Neuronal identification

We recorded from 102 interneurons in the rat LGN using whole-cell patch recording technique. Of these, 40 were assessed for the burst firing reported in this study. Thalamic interneurons were identified physiologically and morphologically. Physiological identification was based on previously described criteria,52., 59., 84. with some modification resulting from our use of the whole-cell technique. All cells were successfully labeled with biocytin, so that their identity could be confirmed

Discussion

In this study, all geniculate interneurons recorded produced burst firing. The bursts were generally of prolonged duration and low frequency, distinct from the bursts found in TC cells, but somewhat similar to those of RE cells. The pattern of bursting seen was also similar to that seen in previous recordings of thalamic interneurons both in vivo and in vitro.1., 4., 11., 13., 15., 21., 59., 63., 77., 84. However, in previous in vitro studies, bursts were not elicited consistently.

Conclusion

Inhibitory mechanisms play an important role in thalamic function, due in part to the existence of low-threshold bursting mechanisms in the other major cell types of the thalamus. The presence of similar bursting mechanisms in the inhibitory interneurons suggests additional complexity for the functional thalamic circuit. Although the depolarized shift in the threshold for activation of low-threshold bursts in interneurons makes them somewhat less dependent on hyperpolarization preceding a

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