Strong Correlations between Sensitivity and Variability Give Rise to Constant Discrimination Thresholds across the Otolith Afferent Population

Abstract

The vestibular system is vital for our sense of linear self-motion. At the earliest processing stages, the otolith afferents of the vestibular nerve encode linear motion. Their resting discharge regularity has long been known to span a wide range, suggesting an important role in sensory coding, yet to date, the question of how this regularity alters the coding of translational motion is not fully understood. Here, we recorded from single otolith afferents in macaque monkeys during linear motion along the preferred directional axis of each afferent over a wide range of frequencies (0.5-16 Hz) corresponding to physiologically relevant stimulation. We used signal-detection theory to directly measure neuronal thresholds and found that values for single afferents were substantially higher than those observed for human perception even when a Kaiser filter was used to provide an estimate of firing rate. Surprisingly, we further found that neuronal thresholds were independent of both stimulus frequency and resting discharge regularity. This was because increases in trial-to-trial variability were matched by increases in sensitivity such that their ratio remains constant: a coding strategy that markedly differs from that used by semicircular canal vestibular afferents to encode rotations. Finally, using Fisher information, we show that pooling the activities of multiple otolith afferents gives rise to neural thresholds comparable with those measured for perception. Together, our results strongly suggest that higher-order structures integrate inputs across afferent populations to provide our sense of linear motion and provide unexpected insight into the influence of variability on sensory encoding. IntroductionAs we navigate through the world, our brain integrates information originating from the vestibular, visual, and proprioceptive systems to compute an estimate of self-motion. However, vestibular contributions to motion perception have been difficult to study because the pathways are inherently multisensory. Numerous studies have attempted to quantify perceptual vestibular thresholds for linear motion in humans (Walsh, 1961(Walsh, , 1962 Young and Meiry, 1968;Jones and Young, 1978; Benson et al., 1986; Zupan and Merfeld, 2008; MacNeilage et al., 2010a,b;Naseri and Grant, 2012). Notably, recent results show that vestibular cues play a central role in determining perceptual thresholds and further suggest that they can be as low as ϳ1.5 cm/s 2 (Valko et al., 2012). To date, the neural mechanisms that give rise to our sense of linear self-motion are essentially unknown. At the earliest stages of vestibular processing, otolith afferents detect linear acceleration. Studies performed in other systems show that central pathways must integrate information transmitted by peripheral sensory neuron populations to explain perceptual thresholds as peripheral sensory neurons display much higher values (visual: Pelli, 1985;Amano et al., 2006; Shadlen et al., 1996; auditory: Pfingst and Xu, 2004;Bizley et al., 2010; cross modal: ...

Neuronal thresholds and choice-related activity of otolith afferent fibers during heading perception

“…3C), such that they largely counteract each other. Similar results have also been reported previously during sinusoidal stimulation in the absence of a perceptual task for both otolith (25,26) and semicircular canal (27) afferents.…”

“…Specifically, the fact that some sensory fibers are nearly as sensitive as behavior would imply either information-limiting correlations or massively suboptimal decoding to account for behavior (42,45,46). We consider it more likely that the total information encoded by the otolith afferent population is constrained by information-limiting correlations (40), in which case it is inappropriate to use the square root law to predict behavioral thresholds as previous studies have done (26,37). Unfortunately, it is unlikely that measurements of correlated noise from pairs of neurons provide a good estimate of the informationlimiting correlations (40).…”

“…Otolith afferent thresholds have been measured previously using sinusoidal stimuli (25,26), but behavioral data were not collected simultaneously. Thus, neuronal thresholds were instead compared with human perceptual thresholds (36).…”

“…An important question is how combining the responses of many sensory neurons determines the overall sensitivity of the population code. Some previous studies have attempted to determine the number of neurons (pool size) necessary to predict human perceptual thresholds from neuronal thresholds measured in macaques, assuming that neuronal population thresholds decrease as a function of the square root of pool size (26,37). We believe that this approach has major flaws because strong assumptions must be made regarding the shared variability among neurons (correlated noise) and the efficiency of population decoding, both of which remain largely unknown.…”

Statistics of the Vestibular Input Experienced during Natural Self-Motion: Implications for Neural Processing

“…There are two distinct types of sensors: the otolith organs, which sense translation, and the semicircular canals, which sense rotation. The self-motion responses of afferents from both types of sensors have been typically characterized using artificial stimuli (e.g., sinusoids, bandpass noise) that were constrained to one dimension (e.g., a rotation about the vertical axis or fore-aft translation) (Goldberg, 2000;Cullen and Roy, 2004;Sadeghi et al, 2007;Massot et al, 2011;Jamali et al, 2013). Over the physiologically relevant frequency range, peripheral semicircular canal and otolith afferents encode angular velocity and linear acceleration, respectively, and their response sensitivity increases with increasing frequency Fernández et al, 1988;Goldberg, 2000).…”