Commissural and lemniscal synaptic input to the gerbil inferior colliculus

David R. Moore, Vibhakar C. Kotak, Dan Sanes

Research output: Contribution to journalArticle

Abstract

The central nucleus of the inferior colliculus (ICC) receives direct inputs, bilaterally, from all auditory brain stem nuclear groups. To evaluate the contribution made to gerbil ICC neuron physiology by two major afferent pathways, we examined the synaptic responses evoked by direct stimulation of the commissure of the inferior colliculus (CIC) and the ipsilateral lateral lemniscus (LL). Frontal midbrain slices were obtained from postnatal day (P) 9-p19 gerbils, and whole cell recordings were made under current- (n = 22) or voltage-clamp (n = 52) conditions. Excitatory and inhibitory synaptic responses were characterized by sequentially exposing the slice to ionotropic glutamate receptor antagonists [6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) + aminophosphonpentanoic acid (AP-5), or kynurenic acid)], a γ-aminobutryic acid type A receptor antagonist (bicuculline), and a glycine receptor antagonist (strychnine). In current clamp, LL stimulation typically produced a short latency depolarization followed by a longer duration hyperpolarization. The depolarization was abolished by AP-5 + CNQX, and the remaining inhibitory potential displayed either bicuculline or strychnine sensitivity. In voltage clamp, 79% of ICC neurons displayed synaptic currents after stimulation of each pathway. The synaptic currents were typically complex waveforms, and ionotropic glutamate receptor antagonists reduced inward currents at a holding potential of -80 mV in the majority of neurons. In addition, this treatment reduced outward synaptic currents at a holding potential of -20 mV, indicating that inhibitory interneuronal input was often activated by LL or CIC afferents. A minority of neurons had synaptic currents that were unaffected by glutamate receptor antagonists, but it was more common for CIC-evoked currents to be unaffected (38%) rather than LL-evoked currents (22%). The CIC provided a strong inhibitory input that was almost exclusively GABAergic, whereas the LL inhibition often included a glycinergic component. These experiments have shown that the CIC provides a major glutamatergic and GABAergic input to most ICC neurons. However, much of the inhibitory input from both the CIC and the LL appears to be mediated by interneuronal connections.

Original languageEnglish (US)
Pages (from-to)2229-2236
Number of pages8
JournalJournal of Neurophysiology
Volume80
Issue number5
StatePublished - Nov 1998

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Tectum Mesencephali
Inferior Colliculi
Gerbillinae
Excitatory Amino Acid Antagonists
Neurons
6-Cyano-7-nitroquinoxaline-2,3-dione
Ionotropic Glutamate Receptors
Strychnine
Bicuculline
Kynurenic Acid
Glycine Receptors
Afferent Pathways
Acids
Patch-Clamp Techniques
Mesencephalon
Brain Stem

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Commissural and lemniscal synaptic input to the gerbil inferior colliculus. / Moore, David R.; Kotak, Vibhakar C.; Sanes, Dan.

In: Journal of Neurophysiology, Vol. 80, No. 5, 11.1998, p. 2229-2236.

Research output: Contribution to journalArticle

Moore, David R. ; Kotak, Vibhakar C. ; Sanes, Dan. / Commissural and lemniscal synaptic input to the gerbil inferior colliculus. In: Journal of Neurophysiology. 1998 ; Vol. 80, No. 5. pp. 2229-2236.
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abstract = "The central nucleus of the inferior colliculus (ICC) receives direct inputs, bilaterally, from all auditory brain stem nuclear groups. To evaluate the contribution made to gerbil ICC neuron physiology by two major afferent pathways, we examined the synaptic responses evoked by direct stimulation of the commissure of the inferior colliculus (CIC) and the ipsilateral lateral lemniscus (LL). Frontal midbrain slices were obtained from postnatal day (P) 9-p19 gerbils, and whole cell recordings were made under current- (n = 22) or voltage-clamp (n = 52) conditions. Excitatory and inhibitory synaptic responses were characterized by sequentially exposing the slice to ionotropic glutamate receptor antagonists [6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) + aminophosphonpentanoic acid (AP-5), or kynurenic acid)], a γ-aminobutryic acid type A receptor antagonist (bicuculline), and a glycine receptor antagonist (strychnine). In current clamp, LL stimulation typically produced a short latency depolarization followed by a longer duration hyperpolarization. The depolarization was abolished by AP-5 + CNQX, and the remaining inhibitory potential displayed either bicuculline or strychnine sensitivity. In voltage clamp, 79{\%} of ICC neurons displayed synaptic currents after stimulation of each pathway. The synaptic currents were typically complex waveforms, and ionotropic glutamate receptor antagonists reduced inward currents at a holding potential of -80 mV in the majority of neurons. In addition, this treatment reduced outward synaptic currents at a holding potential of -20 mV, indicating that inhibitory interneuronal input was often activated by LL or CIC afferents. A minority of neurons had synaptic currents that were unaffected by glutamate receptor antagonists, but it was more common for CIC-evoked currents to be unaffected (38{\%}) rather than LL-evoked currents (22{\%}). The CIC provided a strong inhibitory input that was almost exclusively GABAergic, whereas the LL inhibition often included a glycinergic component. These experiments have shown that the CIC provides a major glutamatergic and GABAergic input to most ICC neurons. However, much of the inhibitory input from both the CIC and the LL appears to be mediated by interneuronal connections.",
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