Effects of Adaptation on Discrimination of Whisker Deflection Velocity and Angular Direction in a Model of the Barrel Cortex.

Mainak J Patel

doi:10.3389/fncom.2018.00045

Abstract

Two important stimulus features represented within the rodent barrel cortex are velocity and angular direction of whisker deflection. Each cortical barrel receives information from thalamocortical (TC) cells that relay information from a single whisker, and TC input is decoded by barrel regular-spiking (RS) cells through a feedforward inhibitory architecture (with inhibition delivered by cortical fast-spiking or FS cells). TC cells encode deflection velocity through population synchrony, while deflection direction is encoded through the distribution of spike counts across the TC population. Barrel RS cells encode both deflection direction and velocity with spike rate, and are divided into functional domains by direction preference. Following repetitive whisker stimulation, system adaptation causes a weakening of synaptic inputs to RS cells and diminishes RS cell spike responses, though evidence suggests that stimulus discrimination may improve following adaptation. In this work, I construct a model of the TC, FS, and RS cells comprising a single barrel system—the model incorporates realistic synaptic connectivity and dynamics and simulates both angular direction (through the spatial pattern of TC activation) and velocity (through synchrony of the TC population spikes) of a deflection of the primary whisker, and I use the model to examine direction and velocity selectivity of barrel RS cells before and after adaptation. I find that velocity and direction selectivity of individual RS cells (measured over multiple trials) sharpens following adaptation, but stimulus discrimination using a simple linear classifier by the RS population response during a single trial (a more biologically meaningful measure than single cell discrimination over multiple trials) exhibits strikingly different behavior—velocity discrimination is similar both before and after adaptation, while direction classification improves substantially following adaptation. This is the first model, to my knowledge, that simulates both whisker deflection velocity and angular direction and examines the ability of the RS population response to pinpoint both stimulus features within the context of adaptation.

Highlights

Whisker bending moment provides the major drive for primary mechanosensory cells (Peron et al, 2015; Campagner et al, 2016), and passive experiments employing whisker deflections in anesthetized animals show that two important features of primary whisker stimulation encoded within the corresponding barrel system are the velocity and angular direction of deflection (Bale and Maravall, 2018), which arises as a consequence of the encoding of bending moment and the temporal derivative of the bending moment in barreloid afferents (Campagner et al, 2018)
Thalamocortical cells encode a diverse array of stimulus features (Petersen et al, 2008), and a barreloid tends to encode deflection direction through the distribution of spiking activity across TC cells—barreloid TC cells are functionally divided into groups by direction preference (Timofeeva et al, 2003), and the magnitude of the spike response of a TC direction group diminishes as the angular direction of whisker deflection deviates from the preferred direction of the group toward the opposite direction 180◦ away (Pinto et al, 2000; Bruno and Simons, 2002; Temereanca and Simons, 2003)
To simulate a whisker deflection of a particular angular direction, TC cells within the corresponding direction group spike with high probability, while spike probability progressively diminishes in TC direction groups whose preferred directions deviate from the stimulus direction, with the lowest spike probability in the TC group with a preferred direction 180◦ away; the temporal distribution of TC cell spikes is fixed across direction groups (Pinto et al, 2000; Temereanca and Simons, 2003)

Summary

Introduction

Synchronous spiking activity is a strategy commonly used by neuronal populations to encode and process information (Marthy and Fetz, 1992; Eckhorn, 1994; Gray, 1994; Laurent and Davidowitz, 1994; Friedrich et al, 2004; Patel et al, 2009, 2013; Patel and Joshi, 2015), and feedforward (or phase-delayed) inhibition is often employed to decode information encoded by population synchrony (Leitch et al, 1996; Deng and Rogers, 1998; Fricker and Miles, 2000; Pouille and Scanziani, 2001; Perez-Orive et al, 2002; Wehr and Zador, 2003; Benowitz and Karten, 2004; Blitz and Regehr, 2005; Mittmann et al, 2005; Jortner et al, 2007; Sridharan et al, 2011; Patel and Reed, 2013), due to its ability to robustly detect temporally coherent input (Bruno, 2011; Joshi and Patel, 2013; Patel and Joshi, 2013). A barreloid encodes deflection velocity, on the other hand, through population synchrony; experiments show that different whisker deflection velocities lead to similar net spiking activity of the barreloid (as measured over the entire stimulus interval), while the spikes of TC cells within the barreloid become more temporally coherent with rising deflection velocity, leading to larger spike counts during the “ramp” phase of the stimulus (Pinto et al, 2000; Bruno and Sakmann, 2006; Temereanca et al, 2008). The net barreloid spike count is similar across deflection directions and velocities, with deflection direction encoded by the distribution of spikes across TC direction groups and deflection velocity encoded by the synchrony of TC spikes across the barreloid

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Results

Conclusion