Neuronal Responses to Lemniscal Stimulation in Laminar Brain Slices of the Inferior Colliculus

Abstract

The central nucleus of the inferior colliculus (ICC) receives inputs from all parts of the auditory brainstem and transmits the information to the forebrain. Fibrodendritic laminae of the ICC provide a structural basis for a tonotopic organization, and the interaction of inputs within a single layer is important for ICC processing. Transverse slice planes of the ICC sever the layers and many of the ascending axons that enter through the lateral lemniscus. Consequently, the activity initiated within a lamina by a pure lemniscal stimulus is not well characterized. Here, we use a slice plane that maintains the integrity of the laminae in ICC and allows the axons in the lateral lemniscus to be stimulated at a distance from the ICC. We examined both the postsynaptic currents and potentials of the same neurons to lemniscal stimuli in this laminar brain slice. Our main finding is that lemniscal stimulation evokes prolonged synaptic potentials in ICC neurons. Synaptic potential amplitudes and durations increase with lemniscal shock strength. In õ50% of ICC neurons, the postsynaptic potential is equal in duration to the postsynaptic current, whereas in the remaining neurons it is three to four times longer. Synaptic responses to single shocks or shock trains exhibit plateau potentials that enable sustained firing in ICC neurons. Plateau potentials are evoked by N-methyl-D-aspartate (NMDA) receptor activation, and their amplitudes and durations are regulated by both NMDA-R and gamma-aminobutyric acid A (GABA A )-R activation. These data suggest that in the intact laminae of the ICC, lemniscal inputs initiate sustained firing through monosynaptic and polysynaptic NMDA-mediated synapses regulated by GABA A synapses.

Contribution of NMDA and AMPA Receptors to Temporal Patterning of Auditory Responses in the Inferior Colliculus

“…This agrees closely with conclusions of previous in vivo iontophoretic studies in IC (Feldman and Knudsen, 1994;Zhang and Kelly, 2001). Furthermore, it supports in vitro IC studies showing that NMDARs conduct current at resting membrane potentials when AMPARs are blocked Sivaramakrishnan and Oliver, 2005). Evidence for the independent action of NMDARs has also been reported previously [e.g., in the spinal cord (Davies and Watkins, 1983), lateral geniculate nucleus (Sillito et al, 1990), and mouse barrel cortex (Fleidervish et al, 1998)].…”

High concentrations of divalent cations isolate monosynaptic inputs from local circuits in the auditory midbrain

“…Complete recovery from strychnine was rapid (5–10 min); recovery from gabazine was slower (>30 min). These recovery times are similar to those in IC brain slices (Sivaramakrishnan and Oliver, 2006). In experiments not reported here, we also tested recovery from bicuculline.…”

“…In other experiments we used concentric electrodes with smaller active diameters, but these electrodes did not give us the full range of synaptic activity, suggesting inadequate effective current spread, which would selectively eliminate axons with smaller diameters from our data. With the 100 μm tip diameter, responses at minimal stimulation, which was defined as a 50% failure rate, evoked synaptic currents between 30 and 60 pA, which we estimate to be three to four times the amplitude of a spontaneous miniature synaptic current in IC neurons (Sivaramakrishnan and Oliver, 2006). Thus we think that we were able to isolate a few synapses with minimal stimulation.…”

Processing Temporal Modulations in Binaural and Monaural Auditory Stimuli by Neurons in the Inferior Colliculus and Auditory Cortex

“…5 and 10). In contrast, neurons in the brain slice of the IC show discrete EPSPs that precisely follow pulse rates of 100 Hz (and potentially to even higher rates) (Sivaramakrishnan and Oliver 2006). This is in line with the higher cutoff frequencies in the IC (Figs.…”