Efficient Encoding of Vocalizations in the Auditory Midbrain

Abstract

An important question in sensory neuroscience is what coding strategies and mechanisms are used by the brain to detect and discriminate among behaviorally relevant stimuli. There is evidence that sensory systems migrate from a distributed and redundant encoding strategy at the periphery to a more heterogeneous encoding in cortical structures. It has been hypothesized that heterogeneity is an efficient encoding strategy that minimizes the redundancy of the neural code and maximizes information throughput. Evidence of this mechanism has been documented in cortical structures. In this study, we examined whether heterogeneous encoding of complex sounds contributes to efficient encoding in the auditory midbrain by characterizing neural responses to behaviorally relevant vocalizations in the mouse inferior colliculus (IC). We independently manipulated the frequency, amplitude, duration, and harmonic structure of the vocalizations to create a suite of modified vocalizations. Based on measures of both spike rate and timing, we characterized the heterogeneity of neural responses to the natural vocalizations and their perturbed variants. Using information theoretic measures, we found that heterogeneous response properties of IC neurons contribute to efficient encoding of behaviorally relevant vocalizations.

Discrimination of partial from whole ultrasonic vocalizations using a go/no-go task in mice

“…The 30 kHz Harm, 40 kHz Harm, and 2HarmD USVs were recorded for Holmstrom et al (2010). The Chevron USV was recorded in our own lab (using an Avisoft UltraSoundGate recorder, model 416H).…”

Impaired Auditory Temporal Selectivity in the Inferior Colliculus of Aged Mongolian Gerbils

“…Heterogeneous receptive fields can increase the information encoded in population activity (Shamir and Sompolinsky, 2006;Chelaru and Dragoi, 2008). A recent study in the IC reports that heterogeneity of neuronal responses lead, relative to lower auditory nuclei, to a decrease in signal correlations over the IC population, which could increase the encoding efficiency for natural stimuli (Holmstrom et al, 2010).…”

Behavioral and Single-Neuron Sensitivity to Millisecond Variations in Temporally Patterned Communication Signals

“…The individually stereotyped EOD waveform contains identifying information such as species, sex, and dominance status, and can even be used to identify individuals in some species (Graff and Kramer, 1992;Friedman and Hopkins, 1996;Carlson, 2002;Hanika and Kramer, 2005). Combining the stereotyped EOD waveform with individually characteristic scallop patterns could facilitate individual recognition.…”

“…For instance, the time intervals between successive sound or light pulses are species-specific in certain frogs and insects (Lloyd, 1966;Ewing and Bennet-Clark, 1968;Loftus-Hills and Littlejohn, 1971;Pollack, 2000). Previous studies have shown that circuits process these types of temporal patterns with central neurons that are selective for particular timing intervals (Rose and Capranica, 1983;Grothe, 1994;Fortune and Rose, 1997a;Edwards et al, 2002;Sakai et al, 2009;Pluta and Kawasaki, 2010;Goel and Buonomano, 2014). These response properties arise from synaptic mechanisms such as temporal summation and short-term synaptic plasticity (Fortune and Rose, 2000;George et al, 2011;Rose et al, 2011;Baker and Carlson, 2014), as well as from intrinsic postsynaptic membrane properties (Fortune and Rose, 1997b;Trussell, 1999;Fortune and Rose, 2003;Carlson and Kawasaki, 2006;Kohashi and Carlson, 2014).…”