Information Transmission in Primary Afferent Neurons of the Vestibular System

The semicircular canals of the vertebrate inner ear encode information about dynamical head rotational stimuli and convey it to the central nervous system in real-time via thousands of primary afferent neurons. One of the most striking characteristics of this afferent population is the broad diversity in spontaneous discharge regularity. Afferent spontaneous discharge represents a potential source of noise that could make it more difficult for central vestibular neurons to discern discharge components associated with the stimulus, and the amount of potential noise at frequencies present in the stimulus increases as the regularity of discharge decreases. This latter fact suggests that the lower potential noise levels in the spontaneous activity of regularly firing afferents means that they transmit more information to the brain than do irregularly firing afferents, as quantified by mutual information rates (I). Some support for this understanding of the effect of spontaneous discharge regularity on I comes from data from macaque vestibular afferents, in which regular afferents exhibited higher mutual information per spike (Ispike) than irregular afferents (Sadeghi et al. 2007).;In Chapter 2 we examined whether, as a general rule among primary vestibular afferents among all vertebrate species, regular afferents always transmit more information than irregular afferents by using repeated presentations of broadband Gaussian-distributed rotational stimuli to assess stimulus-response coherence ( g2sr ), response-response coherence ( g2rr ), signal-to-noise ratio (SNR), I, and I spike in horizontal semicircular canal (HC) afferents in bullfrogs. In this species, irregular afferents have much higher response gains than regular afferents, and their responses are highly nonlinear due to their relatively low spontaneous discharge rates, which allow them to be driven to silence during sufficiently intense inhibitory portions of stimuli. In contrast with the macaque, it was found that regular bullfrog afferents had low g2sr and g2rr across the stimulus frequency band, which translated to low SNR, I, and Ispike. Conversely, irregular bullfrog afferents had high g2sr and g2rr across the stimulus frequency band, which translated to high SNR, I, and Ispike. Decomposing the responses into signal and noise components revealed that: 1) in some irregular afferents the power spectral density (PSD) of perstimulus noise was much lower than the PSD of spontaneous discharge; and 2) SNR was highly correlated with signal levels and uncorrelated with noise levels. The first result highlighted the point that spontaneous activity does not necessarily completely carry over to perstimulus noise, and the second result suggested that response gain—rather than spontaneous activity—is the main factor determining information transmission rates in bullfrogs.;Because we found that signal levels are the main determinant of SNR and information rates in bullfrogs, we recorded from vestibular afferents in chinchillas to see whether this might also be true in mammals (Chapter 3). As in other mammals, irregular chinchilla afferents generally have higher response gains than regular afferents, though there is a subpopulation of low-gain irregulars that have dendritic terminals consisting exclusively of calyces. We found that in chinchillas both regular and irregular afferents can have either low or high SNR, I, and Ispike. Decomposing responses into signal and noise revealed that: 1) spontaneous activity is a bigger determinant of noise in irregular afferents in the chinchilla than in the bullfrog indicating that in the bullfrog; and 2) SNR is not determined by either signal or noise alone in the chinchilla. Together, these two findings suggest that for chinchilla vestibular afferents perstimulus noise levels are largely set by spontaneous discharge regularity and then information transmission rates may be either low or high, depending on whether an afferent's response gain is high enough to impart signal levels that can compensate for the noise levels. Comparing Ispike with gains of responses to a low frequency (1.6 Hz) sinusoidal stimulus allowed us to classify the low-Ispike irregular afferents as putative calyx-only afferents.;In Chapter 4 we applied information theoretic measures and multineuronal optimal linear decoding to test the hypothesis that the primary afferent neurons projecting from the anterior semicircular canal (AC) could be providing a substantial amount of information to the brain regarding rotations in the horizontal plane. We found that AC afferents transmitted as much information as HC afferents and multineuronal optimal linear decoders performed best when they included irregular afferents from both the AC and HC. These findings suggest that the central nervous system could be using the responses of AC afferents to help with coding of head rotations in the horizontal plane.;Overall, our studies of information transmission properties in primary vestibular afferents promise to provide a fruitful basis for beginning to integrate the known primary afferent heterogeneity into existing models of vestibular function (e.g., control systems models or probabilistic optimal Bayesian estimation models) in order to gain new insights into how the organizational principles of central vestibular circuits in each individual species are specifically tailored for their ethological needs.