Frequency-specific corticofugal modulation of the dorsal cochlear nucleus in mice

Abstract

The primary auditory cortex (AI) modulates the sound information processing in the lemniscal subcortical nuclei, including the anteroventral cochlear nucleus (AVCN), in a frequency-specific manner. The dorsal cochlear nucleus (DCN) is a non-lemniscal subcortical nucleus but it is tonotopically organized like the AVCN. However, it remains unclear how the AI modulates the sound information processing in the DCN. This study examined the impact of focal electrical stimulation of AI on the auditory responses of the DCN neurons in mice. We found that the electrical stimulation induced significant changes in the best frequency (BF) of DCN neurons. The changes in the BFs were highly specific to the BF differences between the stimulated AI neurons and the recorded DCN neurons. The DCN BFs shifted higher when the AI BFs were higher than the DCN BFs and the DCN BFs shifted lower when the AI BFs were lower than the DCN BFs. The DCN BFs showed no change when the AI and DCN BFs were similar. Moreover, the BF shifts were linearly correlated to the BF differences. Thus, our data suggest that corticofugal modulation of the DCN is also highly specific to frequency information, similar to the corticofugal modulation of the AVCN. The frequency-specificity of corticofugal modulation does not appear limited to the lemniscal ascending pathway.

Keywords: corticofugal modulation; dorsal cochlear nucleus; frequency-specific modulation; lemniscal; neural plasticity; non-lemniscal; primary auditory cortex.

Figure 1

A schematic of the mouse brain with recording and electrical stimulation sites (adapted from Luo et al., 2008). The corticofugal projection to DCN is indicated by a solid dark line. Auditory cortex, AC; medial geniculate body, MGB; inferior colliculus, IC; cochlear nucleus, CN.

Figure 2

Three examples illustrating the effects of the ES_AI on the frequency tunings of DCN neurons (A–C). The ES_AI did not change the BF but increased the auditory responses of the matched DCN neurons (A1, A2), while the BFs of the unmatched DCN neurons shifted towards the cortical BF (B1, B2 and C1, C2). The ES_AI caused facilitation (A3, B3, C3) and inhibition (B3, C3) of DCN auditory responses. The gray bars in the top two rows of panels represent the BFs of the stimulated cortical neurons. In the bottom row of panels, the dark gray area represents facilitation, whereas the light gray area represents inhibition.

Figure 3

Frequency-specific changes in the auditory responses (spikes) of DCN neurons after contralateral cortical stimulation. (A) The degree of change was different between the matched and unmatched DCN neurons. Filled black circles indicate responses at pre-ES BFs (Control); filled gray circles indicate responses at post-ES BFs, open circles indicate responses of neurons with matched BF. (B) The averaged response change after cortical stimulation. Filled black bars show averaged responses at pre-ES BFs (control); filled gray bars show averaged responses at post-ES BFs, open bar shows averaged response of neurons with matched BF. The error bars represent the SEM.

Figure 4

Frequency-specific changes in the BF of DCN neurons after contralateral cortical stimulation. (A) The degree of change was systematically correlated to the BF difference between the AI and DCN neurons. Open circles, BF shift of neurons with matched BF; filled circles, BF shift of neurons with unmatched BF. (B) The averaged BF change after cortical stimulation. Open bar indicates the BF shift of neurons with matched BF; filled bars indicate the BF shift of neurons with unmatched BF. The error bars represent the SEM.