Central auditory neurons have composite receptive fields

High-level neurons processing complex, behaviorally relevant signals are sensitive to conjunctions of features. Characterizing the receptive fields of such neurons is difficult with standard statistical tools, however, and the principles governing their organization remain poorly understood. Here, we demonstrate multiple distinct receptive-field features in individual high-level auditory neurons in a songbird, European starling, in response to natural vocal signals (songs). We then show that receptive fields with similar characteristics can be reproduced by an unsupervised neural network trained to represent starling songs with a single learning rule that enforces sparseness and divisive normalization. We conclude that central auditory neurons have composite receptive fields that can arise through a combination of sparseness and normalization in neural circuits. Our results, along with descriptions of random, discontinuous receptive fields in the central olfactory neurons in mammals and insects, suggest general principles of neural computation across sensory systems and animal classes

Biomechanics of hearing in katydids

Animals have evolved a vast diversity of mechanisms to detect sounds. Auditory organs are used to detect intraspecific communicative signals and environmental sounds relevant to survival. To hear, terrestrial animals must convert the acoustic energy contained in the airborne sound pressure waves into neural signals. In mammals, spectral quality is assessed by the decomposition of incoming sound waves into elementary frequency components using a sophisticated cochlear system. Some neotropical insects like katydids (bushcrickets) have evolved biophysical mechanisms for auditory processing that are remarkably equivalent to those of mammals. Located on their front legs, katydid ears are small, yet are capable of performing several of the tasks usually associated with mammalian hearing. These tasks include air-to-liquid impedance conversion, signal amplification, and frequency analysis. Impedance conversion is achieved by a lever system, a mechanism functionally analogous to the mammalian middle ear ossicles, yet morphologically distinct. In katydids, the exact mechanisms supporting frequency analysis seem diverse, yet are seen to result in dispersive wave propagation phenomenologically similar to that of cochlear systems. Phylogenetically unrelated, katydids and tetrapods have evolved remarkably different structural solutions to common biophysical problems. Here, we discuss the biophysics of hearing in katydids and the variations observed across different species

Disproportionate Frequency Representation in the Inferior Colliculus of Doppler-Compensating Greater Horseshoe Bats. Evidence for an Acoustic Fovea

1. The inferior colliculus of 8 Greater Horseshoe bats (Rhinolophus ferrumequinun) was systematically sampled with electrode penetrations covering the entire volume of the nucleus. The best frequencies and intensity thresholds for pure tones (Fig. 2) were determined for 591 neurons. The locations of the electrode penetrations within the inferior colliculus were histologically verified. 2. About 50% of all neurons encountered had best frequencies (BF) in the frequency range between 78 and 88 kHz (Table 1, Fig. 1A). Within this frequency range the BFs between 83.0 and 84.5 kHz were overrepresented with 16.3% of the total population of neurons (Fig. 1B). The frequencies of the constant frequency components of the echoes fall into this frequency range. 3. The representation of BFs expressed as number of neurons per octave shows a striking correspondence to the nonuniform innervation density in the afferent innervation of the basilar membrane (Bruns and Schmieszek, in press). The high innervation density of the basilar membrane in the frequency band between 83 and 84.5 kHz coincides with the maximum of the distribution of number of neurons per octave across frequency in the inferior colliculus (Fig. 1 C). 4. The disproportionate representation of frequencies in the auditory system of the greater horseshoe bat is described as an acoustical fovea functioning in analogy to the fovea in the visual system. The functional importance of the Doppler-shift compensation for such a foveal mechanism in the auditory system of horseshoe bats is related to that of tracking eye movements in the visual system

Mammalian cochlea as a physics guided evolution-optimized hearing sensor

Nonlinear physics plays an essential role in hearing, from sound signal generation to sound sensing to the processing of complex sound environments. We demonstrate that the evolution of the biological hearing sensors demonstrates a dramatic reduction in the solution space available for hearing sensors due to nonlinear physics principles. More specifically, our analysis hints at that the differences between amniotic lineages hearing, could be recast into a scaleable and a non-scaleable arrangement of nonlinear sound detectors. The scalable solution employed in mammals, as the most advanced design, provides a natural context that demands the ultimate characterization of complex sounds through pitch

Timescale-invariant representation of acoustic communication signals by a bursting neuron

Acoustic communication often involves complex sound motifs in which the relative durations of individual elements, but not their absolute durations, convey meaning. Decoding such signals requires an explicit or implicit calculation of the ratios between time intervals. Using grasshopper communication as a model, we demonstrate how this seemingly difficult computation can be solved in real time by a small set of auditory neurons. One of these cells, an ascending interneuron, generates bursts of action potentials in response to the rhythmic syllable-pause structure of grasshopper calls. Our data show that these bursts are preferentially triggered at syllable onset; the number of spikes within the burst is linearly correlated with the duration of the preceding pause. Integrating the number of spikes over a fixed time window therefore leads to a total spike count that reflects the characteristic syllable-to-pause ratio of the species while being invariant to playing back the call faster or slower. Such a timescale-invariant recognition is essential under natural conditions, because grasshoppers do not thermoregulate; the call of a sender sitting in the shade will be slower than that of a grasshopper in the sun. Our results show that timescale-invariant stimulus recognition can be implemented at the single-cell level without directly calculating the ratio between pulse and interpulse durations

Spectral and temporal gating mechanisms enhance the clutter rejection in the echolocating bat, Rhinolophus rouxi

Doppler shift compensation behaviour in horseshoe bats, Rhinolophus rouxi, was used to test the interference of pure tones and narrow band noise with compensation performance. The distortions in Doppler shift compensation to sinusoidally frequency shifted echoes (modulation frequency: 0.1 Hz, maximum frequency shift: 3 kHz) consisted of a reduced compensation amplitude and/or a shift of the emitted frequency to lower frequencies (Fig. 1). Pure tones at frequencies between 200 and 900 Hz above the bat's resting frequency (RF) disturbed the Doppler shift compensation, with a maximum of intererence between 400 and 550 Hz (Fig. 2). Minimum duration of pure tones for interference was 20 ms and durations above 40 ms were most effective (Fig. 3). Interfering pure tones arriving later than about 10 ms after the onset of the echolocation call showed markedly reduced interference (Fig. 4). Doppler shift compensation was affected by pure tones at the optimum interfering frequency with sound pressure levels down to –48 dB rel the intensity level of the emitted call (Figs. 5, 6). Narrow bandwidth noise (bandwidth from ± 100 Hz to ± 800 Hz) disturbed Doppler shift compensation at carrier frequencies between –250 Hz below and 800 Hz above RF with a maximum of interference between 250 and 500 Hz above resting frequency (Fig. 7). The duration and delay of the noise had similar influences on interference with Doppler shift compensation as did pure tones (Figs. 8, 9). Intensity dependence for noise interference was more variable than for pure tones (-32 dB to -45 dB rel emitted sound pressure level, Fig. 10). The temporal and spectral gating in Doppler shift compensation behaviour is discussed as an effective mechanism for clutter rejection by improving the processing of frequency and amplitude transients in the echoes of horseshoe bats