Signatures of somatic inhibition and dendritic excitation in auditory brainstem field potentials

Joshua H. Goldwyn, Myles McLaughlin, Eric Verschooten, Philip X. Joris, John Rinzel

Research output: Contribution to journalArticle

Abstract

Extracellular voltage recordings (Ve; field potentials) provide an accessible view of in vivo neural activity, but proper interpretation of field potentials is a long-standing challenge. Computational modeling can aid in identifying neural generators of field potentials. In the auditory brainstem of cats, spatial patterns of sound-evoked Ve can resemble, strikingly, Ve generated by current dipoles. Previously, we developed a biophysically-based model of a binaural brainstem nucleus, the medial superior olive (MSO), that accounts qualitatively for observed dipole-like Ve patterns in sustained responses to monaural tones with frequencies >~1000 Hz (Goldwyn et al., 2014). We have observed, however, that Ve patterns in cats of both sexes appear more monopole-like for lower-frequency tones. Here, we enhance our theory to accurately reproduce dipole and non-dipole features of Ve responses to monaural tones with frequencies ranging from 600 to 1800 Hz. By applying our model to data, we estimate time courses of paired input currents to MSO neurons. We interpret these inputs as dendrite-targeting excitation and soma-targeting inhibition (the latter contributes non-dipole-like features to Ve responses). Aspects of inferred inputs are consistent with synaptic inputs to MSO neurons including the tendencies of inhibitory inputs to attenuate in response to high-frequency tones and to precede excitatory inputs. Importantly, our updated theory can be tested experimentally by blocking synaptic inputs. MSO neurons perform a critical role in sound localization and binaural hearing. By solving an inverse problem to uncover synaptic inputs from Ve patterns we provide a new perspective on MSO physiology.

Original languageEnglish (US)
Pages (from-to)10451-10467
Number of pages17
JournalJournal of Neuroscience
Volume37
Issue number43
DOIs
StatePublished - Oct 25 2017

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Brain Stem
Neurons
Cats
Sound Localization
Carisoprodol
Dendrites
Hearing
Superior Olivary Complex

Keywords

  • Auditory brainstem
  • Field potentials
  • Inhibition
  • Mathematical model
  • Medial superior olive
  • Neurophonic

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Signatures of somatic inhibition and dendritic excitation in auditory brainstem field potentials. / Goldwyn, Joshua H.; McLaughlin, Myles; Verschooten, Eric; Joris, Philip X.; Rinzel, John.

In: Journal of Neuroscience, Vol. 37, No. 43, 25.10.2017, p. 10451-10467.

Research output: Contribution to journalArticle

Goldwyn, Joshua H. ; McLaughlin, Myles ; Verschooten, Eric ; Joris, Philip X. ; Rinzel, John. / Signatures of somatic inhibition and dendritic excitation in auditory brainstem field potentials. In: Journal of Neuroscience. 2017 ; Vol. 37, No. 43. pp. 10451-10467.
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