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J Neurophysiol 82: 2327-2345, 1999;
0022-3077/99 $5.00
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The Journal of Neurophysiology Vol. 82 No. 5 November 1999, pp. 2327-2345
Copyright ©1999 by the American Physiological Society

Facilitatory and Inhibitory Frequency Tuning of Combination-Sensitive Neurons in the Primary Auditory Cortex of Mustached Bats

Jagmeet S. Kanwal, Douglas C. Fitzpatrick, and Nobuo Suga

Department of Biology, Washington University, St. Louis, Missouri 63130

Kanwal, Jagmeet S., Douglas C. Fitzpatrick, and Nobuo Suga. Facilitatory and Inhibitory Frequency Tuning of Combination-Sensitive Neurons in the Primary Auditory Cortex of Mustached Bats. J. Neurophysiol. 82: 2327-2345, 1999. Mustached bats, Pteronotus parnellii parnellii, emit echolocation pulses that consist of four harmonics with a fundamental consisting of a constant frequency (CF1-4) component followed by a short, frequency-modulated (FM1-4) component. During flight, the pulse fundamental frequency is systematically lowered by an amount proportional to the velocity of the bat relative to the background so that the Doppler-shifted echo CF2 is maintained within a narrowband centered at ~61 kHz. In the primary auditory cortex, there is an expanded representation of 60.6- to 63.0-kHz frequencies in the "Doppler-shifted CF processing" (DSCF) area where neurons show sharp, level-tolerant frequency tuning. More than 80% of DSCF neurons are facilitated by specific frequency combinations of ~25 kHz (BFlow) and ~61 kHz (BFhigh). To examine the role of these neurons for fine frequency discrimination during echolocation, we measured the basic response parameters for facilitation to synthesized echolocation signals varied in frequency, intensity, and in their temporal structure. Excitatory response areas were determined by presenting single CF tones, facilitative curves were obtained by presenting paired CF tones. All neurons showing facilitation exhibit at least two facilitative response areas, one of broad spectral tuning to frequencies centered at BFlow corresponding to a frequency in the lower half of the echolocation pulse FM1 sweep and another of sharp tuning to frequencies centered at BFhigh corresponding to the CF2 in the echo. Facilitative response areas for BFhigh are broadened by ~0.38 kHz at both the best amplitude and 50 dB above threshold response and show lower thresholds compared with the single-tone excitatory BFhigh response areas. An increase in the sensitivity of DSCF neurons would lead to target detection from farther away and/or for smaller targets than previously estimated on the basis of single-tone responses to BFhigh. About 15% of DSCF neurons show oblique excitatory and facilitatory response areas at BFhigh so that the center frequency of the frequency-response function at any amplitude decreases with increasing stimulus amplitudes. DSCF neurons also have inhibitory response areas that either skirt or overlap both the excitatory and facilitatory response areas for BFhigh and sometimes for BFlow. Inhibition by a broad range of frequencies contributes to the observed sharpness of frequency tuning in these neurons. Recordings from orthogonal penetrations show that the best frequencies for facilitation as well as excitation do not change within a cortical column. There does not appear to be any systematic representation of facilitation ratios across the cortical surface of the DSCF area.




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