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

Jagmeet S. Kanwal, Douglas C. Fitzpatrick, Nobuo Suga
1999 Journal of Neurophysiology  
Kanwal, J. S., D. C. Fitzpatrick, and N. Suga. Facilitatory and inhibitory frequency tuning of combination-sensitive neurons in the primary auditory cortex of mustached bats. J. Neurophysiol. 82: 2327Neurophysiol. 82: -2345Neurophysiol. 82: , 1999. Mustached bats, Pteronotus parnellii parnellii, emit echolocation pulses that consist of four harmonics with a fundamental consisting of a constant frequency (CF 1-4 ) component followed by a short, frequency-modulated (FM 1-4 ) component. During
more » ... ht, 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 CF 2 is maintained within a narrowband centered at ϳ61 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 ϳ25 kHz (BF low ) and ϳ61 kHz (BF high ). 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 BF low corresponding to a frequency in the lower half of the echolocation pulse FM 1 sweep and another of sharp tuning to frequencies centered at BF high corresponding to the CF 2 in the echo. Facilitative response areas for BF high are broadened by ϳ0.38 kHz at both the best amplitude and 50 dB above threshold response and show lower thresholds compared with the single-tone excitatory BF high 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 BF high . About 15% of DSCF neurons show oblique excitatory and facilitatory response areas at BF high 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 BF high and sometimes for BF low . 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. I N T R O D U C T I O N To understand how acoustic stimuli are processed in the mammalian auditory cortex, several studies have focused on the basic response properties of cortical neurons, such as the sharpness of frequency tuning, response thresholds, dynamic response range, amplitude-response functions, etc., and how they are spatially and temporally organized (deCharms and These studies provide important clues to the functional organization of the auditory cortex in mammals without necessarily attributing single-cell response properties to species-specific behaviors. A few recent studies, however, have made a special attempt to link neural responses and mechanisms with the specific auditory functions such as communication (Ehret and Schreiner 1997; Rauschecker 1998; Rauschecker et al. 1995; Wang et al. 1995) . In mustached bats, the functional organization of the auditory cortex has been explored with great success using speciesspecific stimuli relevant to their echolocation behavior (Fitzpatrick et al
doi:10.1152/jn.1999.82.5.2327 pmid:10561409 fatcat:cikoptgurfh2no7cegotlhay2u