Response Selectivity for Species-Specific Calls in the Inferior Colliculus of Mexican Free-Tailed Bats is Generated by Inhibition

Abstract

Here we show that inhibition shapes diverse responses to species-specific calls in the inferior colliculus (IC) of Mexican free-tailed bats. We presented 10 calls to each neuron of which 8 were social communication and 2 were echolocation calls. We also measured excitatory response regions: the range of tone burst frequencies that evoked discharges at a fixed intensity. The calls evoked highly selective responses in that IC neurons responded to some calls but not others even though those calls swept through their excitatory response regions. By convolving activity in the response regions with the spectrogram of each call, we evaluated whether responses to tone bursts could predict discharge patterns evoked by species-specific calls. The convolutions often predicted responses to calls that evoked no responses and thus were inaccurate. Blocking inhibition at the IC reduced or eliminated selectivity and greatly improved the predictive accuracy of the convolutions. By comparing the responses evoked by two calls with similar spectra, we show that each call evoked a unique spatiotemporal pattern of activity distributed across and within isofrequency contours and that the disparity in the population response was greatly reduced by blocking inhibition. Thus the inhibition evoked by each call can shape a unique pattern of activity in the IC population and that pattern may be important for both the identification of a particular call and for discriminating it from other calls and other signals.

Spectrotemporal Receptive Fields in the Inferior Colliculus Revealing Selectivity for Spectral Motion in Conspecific Vocalizations

“…The remaining 8% were tuned to frequencies above 30 kHz. Although most of the neurons in our sample were tuned to a narrow range of frequencies, between 21 and 25 kHz, this frequency range is overrepresented in the cochlea as well as in other auditory brainstem nuclei of Mexican free-tailed bats (Vater and Siefer, 1995;Bauer et al, 2002;Klug et al, 2002;Xie et al, 2005). A representative STRF is shown in Figure 2 A and illustrates many of the features common to the STRFs we obtained from the other 58 neurons.…”

“…One explanation for this difference in the effects of inhibition on direction selectivity and inseparability is that blocking inhibition frequently causes an expansion of the excitatory receptive field, in which the expansion is not uniform along the spectrotemporal axis (Yang et al, 1992;Palombi and Caspary, 1996;LeBeau et al, 2001;Klug et al, 2002). Such a nonuniform expan- 6.…”

Efficient Encoding of Vocalizations in the Auditory Midbrain

“…We used the pure tone response model as our reference because previous studies show that the IC is the first site in the ascending auditory pathway in which neural responses to vocalizations cannot be predicted by neural responses to pure tones alone Klug et al, 2002;Pollak et al, 2003). Our results showed that the mouse IC encodes vocalizations more efficiently than an encoding predicted by the pure tone model.…”

Experience is required for the maintenance and refinement of FM sweep selectivity in the developing auditory cortex

“…development ͉ response selectivity N eural selectivity for species-specific vocalizations is present in several vertebrate groups (1)(2)(3)(4)(5)(6)(7)(8). In songbirds, experience shapes the development of vocalization selectivity (9)(10)(11).…”