Compensation for Traveling Wave Delay Through Selection of Dendritic Delays Using Spike-Timing-Dependent Plasticity in a Model of the Auditory Brainstem

Abstract

Asynchrony among synaptic inputs may prevent a neuron from responding to behaviorally relevant sensory stimuli. For example, “octopus cells” are monaural neurons in the auditory brainstem of mammals that receive input from auditory nerve fibers (ANFs) representing a broad band of sound frequencies. Octopus cells are known to respond with finely timed action potentials at the onset of sounds despite the fact that due to the traveling wave delay in the cochlea, synaptic input from the auditory nerve is temporally diffuse. This paper provides a proof of principle that the octopus cells' dendritic delay may provide compensation for this input asynchrony, and that synaptic weights may be adjusted by a spike-timing dependent plasticity (STDP) learning rule. This paper used a leaky integrate and fire model of an octopus cell modified to include a “rate threshold,” a property that is known to create the appropriate onset response in octopus cells. Repeated audio click stimuli were passed to a realistic auditory nerve model which provided the synaptic input to the octopus cell model. A genetic algorithm was used to find the parameters of the STDP learning rule that reproduced the microscopically observed synaptic connectivity. With these selected parameter values it was shown that the STDP learning rule was capable of adjusting the values of a large number of input synaptic weights, creating a configuration that compensated the traveling wave delay of the cochlea.

Periodicity Pitch Perception

“…Octopus cells are topologically arranged in frequency-ordered laminae and locally wired to bundles of ANFs. The wiring patterns' scheme constitutes their temporal receptive fields (TRFs) (Oertel et al, 2017;Spencer et al, 2018). Octopus cells latency-phase rectify space-time trajectories in their TRFs (Golding and Oertel, 2012;McGinley et al, 2012).…”

General neural mechanisms can account for rising slope preference in localization of ambiguous sounds

“…We model onset behaviour abstractly as the weighted difference of two low-pass filtered signals (with different time constants). This can be interpreted either as two precisely timed excitatory/inhibitory pathways, or in a similar way to the octopus cell model of Spencer et al (2012Spencer et al ( , 2018 and Ferragamo and Oertel (2002). Their model uses a spike threshold on the rate of change of the membrane potential Brette, 2010, 2011), which we reformulated in terms of firing rates (see Methods and Appendix).…”

“…The compression and gain mechanisms did not contribute substantially ( Figure 3A). We investigated the octopus cell model discussed earlier (Ferragamo and Oertel, 2002;Spencer et al, 2012Spencer et al, , 2018 and found that it could provide a good fit only if adaptation was present alongside the onset mechanism ( Figure 3AD). For model variants including the onset mechanism, the positive or excitatory time constant τ e must be small (Figures 2A and 4B), and the negative or inhibitory time constant τ i must be larger than τ e ( Figure 3CD, τ e versus τ i ).…”

“…However, if β = 1 and τ e τ i the same equations can also be interpreted as a single onset neuron. The equations are approximately equal to a rate-based version of the octopus cell model of Spencer et al (2018), which is itself a simplification of the models of Spencer et al (2012) and Ferragamo and Oertel (2002). In their spiking model,…”

“…Proposed models of peripheral adaptation range from simulating the ringing of the basilar membrane (Tollin, 1998) to adaptation occurring at the synapse between the inner hair cells and the auditory nerve fibers (Hartung and Trahiotis, 2001;Xia and Shinn-Cunningham, 2011). Similarly, onset cells located in the cochlear nucleus (Rothman and Manis, 2003;Spencer et al, 2012Spencer et al, , 2018 are likely to play a role in discarding counfounding localization cues. On the other hand, models of the auditory system including lateral inhibitory circuits in the medial superior olive (MSO) or inferior colliculus (IC) were also able to account for some aspects of the precedence effect.…”