Decoding stimulus duration from neural responses in the auditory midbrain

Abstract

(DTNs). Temporal specificity in their spiking suggests that one function of DTNs is to encode stimulus duration; however, the efficacy of duration encoding by DTNs has yet to be investigated. Herein, we characterize the information content of individual cells and a population of DTNs from the mammalian inferior colliculus (IC) by measuring the stimulus-specific information (SSI) and estimated Fisher information (FI) of spike count responses. We found that SSI was typically greatest for those stimulus durations that evoked maximum spike counts, defined as best duration (BD) stimuli, and that FI was maximal for stimulus durations off BD where sensitivity to a change in duration was greatest. Using population data, we demonstrate that a maximum likelihood estimator (MLE) can accurately decode stimulus duration from evoked spike counts. We also simulated a two-alternative forced choice task by having MLE models decide whether two durations were the same or different. With this task we measured the just-noticeable difference threshold for stimulus duration and calculated the corresponding Weber fractions across the stimulus domain. Altogether, these results demonstrate that the spiking responses of DTNs from the mammalian IC contain sufficient information for the CNS to encode, decode, and discriminate behaviorally relevant auditory signal durations. big brown bat; Eptesicus fuscus; Fisher information, inferior colliculus; just-noticeable difference; stimulus-specific information, temporal processing; Weber fraction DURATION-TUNED NEURONS (DTNs) are ideal candidates for encoding spectral, intensity, and temporal information about an auditory stimulus because they respond selectively to the frequency, amplitude, and duration of acoustic signals. First reported in the torus semicircularis of frogs and subsequently the inferior colliculus (IC) of bats, DTNs have now been recorded from the auditory midbrain, thalamus, and cortex in a variety of vertebrates, and from the mammalian visual cortex (see Sayegh et al. 2011, for review). To date, the electrophysiological properties and underlying synaptic inputs responsible for creating the temporally selective responses of DTNs have been a major research focus, but a quantitative analysis of the information content and encoding efficiency of any neural system is important for linking neurophysiology to behavior and perception because it can suggest limits on the efficacy of information representation. Information theoretic measurements have previously been used to characterize the spiking responses of visual (Strong et al. 1998;Tolhurst et al. 2009 Sensory neurons in general, and auditory neurons in particular, are often viewed as feature detectors that have a preferred value in stimulus domains such as frequency or amplitude, and they encode the domain with spike counts (or rates) and latencies that vary as a function of the stimulus. We measured spike counts and latencies from auditory DTNs in the mammalian IC to characterize the information content of duration-selective ne...

Slow NMDA-Mediated Excitation Accelerates Offset-Response Latencies Generated via a Post-Inhibitory Rebound Mechanism

“…Behaviorally, sound offsets are an important cue for sound-duration encoding. Neurons in the auditory midbrain that are sensitive to sound duration act as coincidence detectors that only fire action potentials if excitatory postsynaptic responses evoked by the onset of sound temporally coincide with excitatory postsynaptic responses evoked by the offset of sound (Casseday et al, 1994; Aubie et al, 2009, 2012, 2014; Sayegh et al, 2011; ). Duration sensitive neurons have been classified according to their ability to preferably encode sounds of different durations and are referred to as short-pass, bandpass and long-pass duration tuned neurons.…”

Diverse cortical codes for scene segmentation in primate auditory cortex

“…For example, Aubie et al (2014) decoded spike counts recorded from bat midbrain neurons responding to tones with durations ranging from 1 to 25 ms. The much longer tone durations we presented (50 -400 ms) are the inverses of the range of modulation frequencies essential for speech signals (2.5-20 Hz) and known to be robustly represented by cortical neurons in this species ).…”

“…Neurons exhibiting duration-selective responses have been characterized in multiple vertebrate species (Aubie et al 2012;Sayegh et al 2011), chiefly frogs (Gooler and Feng 1992;Hall and Feng 1986;Narins and Capranica 1980;Potter 1965;Rose 2014) and bats (Aubie et al 2014;Casseday et al 1994;Ehrlich et al 1997;Faure et al 2003;Fuzessery 1994; Fuzessery and Hall 1999; Galazyuk and Feng 1997; Macías et al . Contextual modulation of cortical responses permits the discrimination of tone duration from the "spontaneous" rates and onset responses.…”

Neural Resolution of Formant Frequencies in the Primary Auditory Cortex of Rats

“…While the neural resolution measure we developed here is sensitive to the noise inherent in trial-to-trial variability of discharges, it contributes nothing to our understanding of such informational redundancy in neural population codes. Furthermore, there are other measures which are in widespread use in central auditory physiology which quantify neural coding in the light of response variability, such as Shannon information [ 6 , 17 , 37 , 38 ] or Fisher information [ 39 , 40 ]. So why, or when, is the use of a neural resolution estimate through kernel-smoothing of the type developed here more appropriate than the use of alternative, already well established methods for the quantification of neural tuning or coding?…”