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Frequency-modulated (FM) sweeps are common components of vocalizations, including human speech. Both sweep direction and rate influence discrimination of vocalizations. Across species, relatively less is known about FM rate selectivity compared with direction selectivity. In this study, FM rate selectivity was studied in the auditory cortex of anesthetized 1- to 3-mo-old C57bl/6 mice. Neurons were classified as fast pass, band pass, slow pass, or all pass depending on their selectivity for rates between 0.08 and 20 kHz/ms. Multiunit recordings were used to map FM rate selectivity at depths between 250 and 450 μm across both primary auditory cortex (A1) and the anterior auditory field (AAF). In terms of functional organization of rate selectivity, three patterns were found. First, in both A1 and AAF, neurons clustered according to rate selectivity. Second, most (∼60%) AAF neurons were either fast-pass or band-pass selective. Most A1 neurons (∼72%) were slow-pass selective. This distribution supports the hypothesis that AAF is specialized for faster temporal processing than A1. Single-unit recordings (n = 223) from A1 and AAF show that the mouse auditory cortex is best poised to detect and discriminate a narrow range of sweep rates between 0.5 and 3 kHz/ms. Third, based on recordings obtained at different depths, neurons in the infragranular layers were less rate selective than neurons in the granular layers, suggesting FM processing undergoes changes within the cortical column. On average, there was very little direction selectivity in the mouse auditory cortex. There was also no correlation between characteristic frequency and direction selectivity. The narrow range of rate selectivity in the mouse cortex indicates that FM rate processing is a useful physiological marker for studying contributions of genetic and environmental factors in auditory system development, aging, and disease.

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In active sensing, animals make motor adjustments to match sensory inputs to specialized neural circuitry. Here, we describe an active sensing system for sound level processing. The pallid bat uses downward frequency-modulated (FM) sweeps as echolocation calls for general orientation and obstacle avoidance. The bat’s auditory cortex contains a region selective for these FM sweeps (FM sweep-selective region, FMSR). We show that the vast majority of FMSR neurons are sensitive and strongly selective for relatively low levels (30-60 dB SPL). Behavioral testing shows that when a flying bat approaches a target, it reduces output call levels to keep echo levels between ∼30 and 55 dB SPL. Thus, the pallid bat behaviorally matches echo levels to an optimized neural representation of sound levels. FMSR neurons are more selective for sound levels of FM sweeps than tones, suggesting that across-frequency integration enhances level tuning. Level-dependent timing of high-frequency sideband inhibition in the receptive field shapes increased level selectivity for FM sweeps. Together with previous studies, these data indicate that the same receptive field properties shape multiple filters (sweep direction, rate, and level) for FM sweeps, a sound common in multiple vocalizations, including human speech. The matched behavioral and neural adaptations for low-intensity echolocation in the pallid bat will facilitate foraging with reduced probability of acoustic detection by prey.

The pallid bat (Antrozous pallidus) listens to prey-generated noise to localize and hunt terrestrial prey while reserving echolocation to avoid obstacles. The thalamocortical connections in the pallid bat are organized as parallel pathways that may serve echolocation and prey localization behaviors. Thalamic inputs to the cortical echolocation call- and noise-selective regions originate primarily in the suprageniculate nucleus (SG) and ventral division of medial geniculate body (MGBv), respectively. Here we examined the distribution of Parvalbumin (PV) and Calbindin (CB) expression in cortical regions and thalamic nuclei of these pathways. Electrophysiology was used to identify cortical regions selective for echolocation calls and noise. Immunohistochemistry was used to stain for PV and CB in the auditory cortex and MGB. A higher percentage (relative to Nissl-stained cells) of PV+ cells compared to CB+ cells was found in both echolocation call- and noise-selective regions. This was due to differences in cortical layers V-VI, but not layers I-IV. In the MGB, CB+ cells were present across all divisions of the MGB with a higher percentage in the MGBv than the SG. Perhaps the most surprising result was the virtual absence of PV staining in the MGBv. PV staining was present only in the SG. Even in the SG, the staining was mostly diffuse in the neuropil. These data are supportive of the notion that calcium binding proteins are differentially distributed in different processing streams. Our comparative data, however, do not support a general mammalian pattern of PV/CB staining that distinguishes lemniscal and non-lemniscal pathways.