Retuning of Inferior Colliculus Neurons Following Spiral Ganglion Lesions: A Single-Neuron Model of Converging Inputs

Abstract

Lesions of spiral ganglion cells, representing a restricted sector of the auditory nerve array, produce immediate changes in the frequency tuning of inferior colliculus (IC) neurons. There is a loss of excitation at the lesion frequencies, yet responses to adjacent frequencies remain intact and new regions of activity appear. This leads to immediate changes in tuning and in tonotopic progression. Similar effects are seen after different methods of peripheral damage and in auditory neurons in other nuclei. The mechanisms that underlie these postlesion changes are unknown, but the acute effects seen in IC strongly suggest the “unmasking” of latent inputs by the removal of inhibition. In this study, we explore computational models of single neurons with a convergence of excitatory and inhibitory inputs from a range of characteristic frequencies (CFs), which can simulate the narrow prelesion tuning of IC neurons, and account for the changes in CF tuning after a lesion. The models can reproduce the data if inputs are aligned relative to one another in a precise order along the dendrites of model IC neurons. Frequency tuning in these neurons approximates that seen physiologically. Removal of inputs representing a narrow range of frequencies leads to unmasking of previously subthreshold excitatory inputs, which causes changes in CF. Conversely, if all of the inputs converge at the same point on the cell body, receptive fields are broad and unmasking rarely results in CF changes. However, if the inhibition is tonic with no stimulus-driven component, then unmasking can still produce changes in CF.

Acute changes in frequency responses of inferior colliculus central nucleus (ICC) neurons following progressively enlarged restricted spiral ganglion lesions

“…Although tuning curves in auditory nerve fibers often have notches between their “tips” and “tails” after acoustic trauma similar to the notches seen in ICC after SG-lesions, the frequency locations of auditory nerve notches are unrelated to LCF, whereas the notches in ICC FRAs after SG-lesions are centered at LCF. These differences, which are summarized diagrammatically in Figure 15, have also been observed in models of post-lesion responses in central auditory neurons (Scholes et al, 2006; Sumner et al, 2008; Sinex unpublished observations).…”

“…Type 2 & 3 changes, i.e., excitation increases inside (Type 2) and outside (Type 3) the pre-lesion response area without concomitant excitatory losses or changes in CF, occurred in 23% of response areas which showed a post-lesion change. It is worth noting that these percentages approximate the proportion of lesion induced receptive field changes observed by Sumner et al (2008) in their “basic multi-compartmental” computational model of ICC neuron receptive fields.…”

“…As described by Sumner et al (2008), Type 1 changes were those that showed simple excitatory losses at frequencies corresponding to the lesion frequencies. These excitatory losses could be either above or below CF (Type 1a and1b, respectively), and sometimes produced notched FRAs.…”

“…Sumner et al, 2008 categorized the lesion-induced receptive field changes into 4 types. As described by Sumner et al (2008), Type 1 changes were those that showed simple excitatory losses at frequencies corresponding to the lesion frequencies.…”

Midbrain local circuits shape sound intensity codes

“…These afferent contacts, if made through large glutamatergic terminals or dense terminal arbors (Winer, 2005; Nakamoto et al, 2013) on proximal dendrites, would have the properties of driving inputs (Sherman and Guillery, 1998). Our results suggest that these driving inputs include those that create tuning curves, which are frequency specific channels that persist through the auditory pathway (Liu et al, 2007; Kandler et al, 2009; Sumner et al, 2009). A primary role of narrow dynamic range peripheral afferents may therefore be to ensure throughput of the rate-level code through proximal monosynaptic inputs.…”