Transcutaneous induction of stimulus-timing-dependent plasticity in dorsal cochlear nucleus.

Calvin Wu,Susan E. Shore,David T. Martel

doi:10.3389/fnsys.2015.00116

Calvin Wu, Susan E. Shore + Show 1 more

Open Access

https://doi.org/10.3389/fnsys.2015.00116

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Abstract

The cochlear nucleus (CN) is the first site of multisensory integration in the ascending auditory pathway. The principal output neurons of the dorsal cochlear nucleus (DCN), fusiform cells, receive somatosensory information relayed by the CN granule cells from the trigeminal and dorsal column pathways. Integration of somatosensory and auditory inputs results in long-term enhancement or suppression in a stimulus-timing-dependent manner. Here, we demonstrate that stimulus-timing-dependent plasticity (STDP) can be induced in DCN fusiform cells using paired auditory and transcutaneous electrical stimulation of the face and neck to activate trigeminal and dorsal column pathways to the CN, respectively. Long-lasting changes in fusiform cell firing rates persisted for up to 2 h after this bimodal stimulation, and followed Hebbian or anti-Hebbian rules, depending on tone duration, but not somatosensory stimulation location: 50 ms paired tones evoked predominantly Hebbian, while 10 ms paired tones evoked predominantly anti-Hebbian plasticity. The tone-duration-dependent STDP was strongly correlated with first inter-spike intervals, implicating intrinsic cellular properties as determinants of STDP. This study demonstrates that transcutaneous stimulation with precise auditory–somatosensory timing parameters can non-invasively induce fusiform cell long-term modulation, which could be harnessed in the future to moderate tinnitus-related hyperactivity in DCN.

Highlights

The cochlear nucleus (CN) receives auditory nerve fiber (ANF) inputs from the cochlea, as well as projections from somatosensory afferents
Whether enhancement or suppression occurs is determined by the temporal order and interval of the combined auditory and somatosensory stimuli (Koehler and Shore, 2013a,b), which is mediated by spike-timing-dependent plasticity of the parallel fiber–fusiform cell synapse in vitro (Tzounopoulos et al, 2004, 2007)
Maladaptive stimulustiming-dependent plasticity (STDP) in dorsal cochlear nucleus (DCN) occurs in tinnitus (Koehler and Shore, 2013a), the phantom perception of sound, which is characterized by fusiform cell hyperactivity (Brozoski et al, 2002; Kaltenbach et al, 2004, 2005; Dehmel et al, 2012; Koehler and Shore, 2013a)

Summary

Introduction

The cochlear nucleus (CN) receives auditory nerve fiber (ANF) inputs from the cochlea, as well as projections from somatosensory afferents. Stimulating the trigeminal ganglion or the spinal trigeminal nucleus (Sp5), cervical nerve or dorsal column brainstem nuclei can suppress or enhance fusiform cell responses to auditory stimuli (Kanold and Young, 2001; Shore, 2005; Kanold et al, 2011; Koehler et al, 2011; Dehmel et al, 2012). Whether enhancement or suppression occurs is determined by the temporal order and interval of the combined auditory and somatosensory stimuli (Koehler and Shore, 2013a,b), which is mediated by spike-timing-dependent plasticity (sTDP) of the parallel fiber–fusiform cell synapse in vitro (Tzounopoulos et al, 2004, 2007). Maladaptive STDP in DCN occurs in tinnitus (Koehler and Shore, 2013a), the phantom perception of sound, which is characterized by fusiform cell hyperactivity (Brozoski et al, 2002; Kaltenbach et al, 2004, 2005; Dehmel et al, 2012; Koehler and Shore, 2013a)

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