Abstract
Corticofugal modulation of auditory responses in subcortical nuclei has been extensively studied whereas corticofugal synaptic transmission must still be characterized. This study examined postsynaptic potentials of the corticocollicular system, i.e., the projections from the primary auditory cortex (AI) to the central nucleus of the inferior colliculus (ICc) of the midbrain, in anesthetized C57 mice. We used focal electrical stimulation at the microampere level to activate the AI (ESAI) and in vivo whole-cell current-clamp to record the membrane potentials of ICc neurons. Following the whole-cell patch-clamp recording of 88 ICc neurons, 42 ICc neurons showed ESAI-evoked changes in the membrane potentials. We found that the ESAI induced inhibitory postsynaptic potentials in 6 out of 42 ICc neurons but only when the stimulus current was 96 μA or higher. In the remaining 36 ICc neurons, excitatory postsynaptic potentials (EPSPs) were induced at a much lower stimulus current. The 36 ICc neurons exhibiting EPSPs were categorized into physiologically matched neurons (n = 12) when the characteristic frequencies of the stimulated AI and recorded ICc neurons were similar (≤1 kHz) and unmatched neurons (n = 24) when they were different (>1 kHz). Compared to unmatched neurons, matched neurons exhibited a significantly lower threshold of evoking noticeable EPSP, greater EPSP amplitude, and shorter EPSP latency. Our data allow us to propose that corticocollicular synaptic transmission is primarily excitatory and that synaptic efficacy is dependent on the relationship of the frequency tunings between AI and ICc neurons.
Highlights
The auditory cortex sends large numbers of descending projections to most auditory nuclei in the thalamus, midbrain, and low brainstem (Weedman and Ryugo, 1996; Druga et al, 1997; Winer et al, 1998, 2001; Rouiller and Welker, 2000; Schofield and Coomes, 2005)
The resting membrane potentials (RMPs) of these inferior colliculus (ICc) neurons are shown in Supplementary Table 1 and the characteristic frequencies (CFs) and minimum threshold (MT) of sampled ICc neurons and corresponding auditory cortex (AI) neurons are shown in Supplementary Table 2
Our study suggests that corticofugal modulation of postsynaptic excitability through N-methyl-Daspartate receptor (NMDAR)/metabotropic glutamate receptor (mGluR) must have a significant impact on the responses of postsynaptic neurons to ascending inputs; greater corticofugal excitatory postsynaptic potentials (EPSPs) translates to a greater impact on the auditory responses of postsynaptic neurons (i.e., ICc neurons)
Summary
The auditory cortex sends large numbers of descending projections to most auditory nuclei in the thalamus, midbrain, and low brainstem (Weedman and Ryugo, 1996; Druga et al, 1997; Winer et al, 1998, 2001; Rouiller and Welker, 2000; Schofield and Coomes, 2005). Cortical neurons implement differential modulation of the auditory responses of subcortical neurons depending on the functional relationship of cortical and subcortical neurons, facilitation when cortical and subcortical neurons have similar tunings, and suppression when they have different ones (Suga, 2020) This cortex-oriented modulation is seen across various domains i.e., frequency, amplitude, and time (Yan and Suga, 1996; Ma and Suga, 2001; Yan and Ehret, 2002; Zhou and Jen, 2007), various processing centers i.e., thalamus, midbrain, and cochlear nucleus (Zhang and Suga, 2000; Zhou and Jen, 2000; Luo et al, 2008; Liu et al, 2010) and various species i.e., bats, gerbils and mice (Zhang et al, 1997; Zhou and Jen, 2000; Sakai and Suga, 2002; Yan and Ehret, 2002). Little is known about the synaptic mechanism underlying the corticofugal system and its highly specific modulation
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