Potassium conductance dynamics confer robust spike-time precision in a neuromorphic model of the auditory brain stem

Abstract

Wittig JH Jr, Boahen K. Potassium conductance dynamics confer robust spike-time precision in a neuromorphic model of the auditory brain stem. J Neurophysiol 110: 307-321, 2013. First published April 3, 2013 doi:10.1152/jn.00433.2012.-A fundamental question in neuroscience is how neurons perform precise operations despite inherent variability. This question also applies to neuromorphic engineering, where low-power microchips emulate the brain using large populations of diverse silicon neurons. Biological neurons in the auditory pathway display precise spike timing, critical for sound localization and interpretation of complex waveforms such as speech, even though they are a heterogeneous population. Silicon neurons are also heterogeneous, due to a key design constraint in neuromorphic engineering: smaller transistors offer lower power consumption and more neurons per unit area of silicon, but also more variability between transistors and thus between silicon neurons. Utilizing this variability in a neuromorphic model of the auditory brain stem with 1,080 silicon neurons, we found that a low-voltage-activated potassium conductance (g KL ) enables precise spike timing via two mechanisms: statically reducing the resting membrane time constant and dynamically suppressing late synaptic inputs. The relative contribution of these two mechanisms is unknown because blocking g KL in vitro eliminates dynamic adaptation but also lengthens the membrane time constant. We replaced g KL with a static leak in silico to recover the short membrane time constant and found that silicon neurons could mimic the spike-time precision of their biological counterparts, but only over a narrow range of stimulus intensities and biophysical parameters. The dynamics of g KL were required for precise spike timing robust to stimulus variation across a heterogeneous population of silicon neurons, thus explaining how neural and neuromorphic systems may perform precise operations despite inherent variability. silicon neuron; phase locking; bushy cells; g KL ; heterogeneity AUDITORY NERVE AXONS DIVERGE in the cochlear nuclei to excite multiple cell types that integrate and process different aspects of sound (Young and Oertel 2004). Nerve fiber spikes encode both the intensity and phase of acoustic energy in a narrow band of spectrum, whereas spikes in their targets are skewed toward encoding either intensity or phase (reviewed in Oertel et al. 2011). A phenomenal example of the latter comes from bushy cells, whose spikes encode the phase of low-frequency tones with greater temporal precision than their inputs (Joris et al. 1994a). Bushy cells contribute to the neural circuits for localizing sound sources based on differences of sound pressure level and phase (Yin 2002). At elevated sound levels these cells eschew information about stimulus intensity: they fire exactly one precisely timed spike each stimulus cycle over more than a 20-decibel range of sound pressure level (dB SPL). This intensity-invariant spike-time precision and spike-count reliabil...

Differential contributions of voltage-gated potassium channel subunits in enhancing temporal coding in the bushy cells of the ventral cochlear nucleus

“…The Kv1.1, 1.2, and 1.6 subunits regulated AP kinetics and ensured a single firing pattern and shortened rise time in this study. A single precise AP generated in response to normal suprathreshold depolarization resulted in the activation of elaborate presynaptic endbulb of Held release machinery (77), fast AMPA receptors (78), and specific postsynaptic potassium channels (79). Several studies have suggested that the inhibition of Kv1.1 subunits results in multiple AP firing patterns (14,34).…”

A review of mechanical and synaptic processes in otolith transduction of sound and vibration for clinical VEMP testing

“…1) The hair bundles of vestibular type I striolar hair cells may be stiffer; 2) The tenuously attached striola hair cells may have a steeper response curve; 3) The unique type I-calyx system of striolar type I hair cells may act to confer this higher precision. With respect to 3), there is now evidence for a transient increase in the concentration of K ϩ in the thin synaptic cleft between type I hair cells and calyx afferents (Contini et al 2017;Lim et al 2011;Wittig and Boahen 2013). In contrast to the extracellular endolymph fluid bathing the stereocilia, the extracellular space surrounding hair cells and afferent terminals is perilymph.…”