scholarly journals Sex-dependent hemispheric asymmetries for processing frequency-modulated sounds in the primary auditory cortex of the mustached bat

2012 ◽  
Vol 108 (6) ◽  
pp. 1548-1566 ◽  
Author(s):  
Stuart D. Washington ◽  
Jagmeet S. Kanwal

Species-specific vocalizations of mammals, including humans, contain slow and fast frequency modulations (FMs) as well as tone and noise bursts. In this study, we established sex-specific hemispheric differences in the tonal and FM response characteristics of neurons in the Doppler-shifted constant-frequency processing area in the mustached bat's primary auditory cortex (A1). We recorded single-unit cortical activity from the right and left A1 in awake bats in response to the presentation of tone bursts and linear FM sweeps that are contained within their echolocation and/or communication sounds. Peak response latencies to neurons' preferred or best FMs were significantly longer on the right compared with the left in both sexes, and in males this right-left difference was also present for the most excitatory tone burst. Based on peak response magnitudes, right hemispheric A1 neurons in males preferred low-rate, narrowband FMs, whereas those on the left were less selective, responding to FMs with a variety of rates and bandwidths. The distributions of parameters for best FMs in females were similar on the two sides. Together, our data provide the first strong physiological support of a sex-specific, spectrotemporal hemispheric asymmetry for the representation of tones and FMs in a nonhuman mammal. Specifically, our results demonstrate a left hemispheric bias in males for the representation of a diverse array of FMs differing in rate and bandwidth. We propose that these asymmetries underlie lateralized processing of communication sounds and are common to species as divergent as bats and humans.

1992 ◽  
Vol 68 (5) ◽  
pp. 1613-1623 ◽  
Author(s):  
H. Riquimaroux ◽  
S. J. Gaioni ◽  
N. Suga

1. The Jamaican mustached bat uses a biosonar signal (pulse) with eight major components: four harmonics each consisting of a long constant frequency (CF1-4) component followed by a short frequency-modulated (FM1-4) component. While flying, the bat adjusts the frequency of its pulse so as to maintain the CF2 of the Doppler-shifted echo at a frequency to which its cochlea is very sharply tuned. This Doppler shift (DS) compensation likely is mediated or influenced by the Doppler-shifted CF (DSCF) processing area of the primary auditory cortex, which only represents frequencies in the range of echo CF2s (60.6 to 62.3 kHz when the "resting" frequency of the CF2 is 61.0 kHz). 2. We trained four bats to discriminate between different trains of paired tone bursts that mimicked a bat's pulse CF2 and the accompanying echo CF2. The frequency of these CF2s ranged between 61.0 and 64.0 kHz. A discriminated shock avoidance procedure response was employed using a leg flexion. For one stimulus, the S+, the pulse and echo CF2s were the same frequency (delta f = 0, i.e., no Doppler shift). A leg flexion during the S+ turned off both the S+ and the scheduled shock. For a second stimulus, the S-, the echo CF2 was 0.05, 0.1, 0.3, 0.5, or 2.0 kHz higher than the pulse CF2. A delta f of 0.05 kHz was a frequency difference of 0.08%. No shock followed the S-, and leg flexions had no consequences. Correct responses consisted of a leg flexion during the S+ and no flexion during the S-; these responses were added together to compute the percentage of correct responses. When a bat correctly responded at better than 75% for all the delta f s, muscimol, a potent agonist of gamma-aminobutyric acid, was bilaterally applied to inactivate the DSCF area. Performance on each delta f discrimination was then measured. 3. Initial attempts to condition the bats to flex their legs to the CF tones mimicking part of the natural pulses and echoes failed. When broad-band noise bursts were substituted, however, the conditioned response was rapidly established. The noise band-width was gradually reduced and then replaced with the CF tones. Discrimination training with the tone burst trains then commenced. Throughout this procedure, the bats maintained their responding to the stimuli. The bats typically required approximately 20-30 sessions to perform consistently (> or = 75% correct responses) a discrimination involving a 2 kHz delta f.(ABSTRACT TRUNCATED AT 400 WORDS)


Symmetry ◽  
2021 ◽  
Vol 13 (6) ◽  
pp. 1037
Author(s):  
Stuart D. Washington ◽  
Dominique L. Pritchett ◽  
Georgios A. Keliris ◽  
Jagmeet S. Kanwal

The mustached bat (Pteronotus parnellii) is a mammalian model of cortical hemispheric asymmetry. In this species, complex social vocalizations are processed preferentially in the left Doppler-shifted constant frequency (DSCF) subregion of primary auditory cortex. Like hemispheric specializations for speech and music, this bat brain asymmetry differs between sexes (i.e., males>females) and is linked to spectrotemporal processing based on selectivities to frequency modulations (FMs) with rapid rates (>0.5 kHz/ms). Analyzing responses to the long-duration (>10 ms), slow-rate (<0.5 kHz/ms) FMs to which most DSCF neurons respond may reveal additional neural substrates underlying this asymmetry. Here, we bilaterally recorded responses from 176 DSCF neurons in male and female bats that were elicited by upward and downward FMs fixed at 0.04 kHz/ms and presented at 0–90 dB SPL. In females, we found inter-hemispheric latency differences consistent with applying different temporal windows to precisely integrate spectrotemporal information. In males, we found a substrate for asymmetry less related to spectrotemporal processing than to acoustic energy (i.e., amplitude). These results suggest that in the DSCF area, (1) hemispheric differences in spectrotemporal processing manifest differently between sexes, and (2) cortical asymmetry for social communication is driven by spectrotemporal processing differences and neural selectivities for amplitude.


1990 ◽  
Vol 64 (3) ◽  
pp. 888-902 ◽  
Author(s):  
R. Rajan ◽  
L. M. Aitkin ◽  
D. R. Irvine

1. The organization of azimuthal sensitivity of units across the dorsoventral extent of primary auditory cortex (AI) was studied in electrode penetrations made along frequency-band strips of AI. Azimuthal sensitivity for each unit was represented by a mean azimuth function (MF) calculated from all azimuth functions obtained to characteristic frequency (CF) stimuli at intensities 20 dB or more greater than threshold. MFs were classified as contrafield, ipsi-field, central-field, omnidirectional, or multipeaked, according to the criteria established in the companion paper (Rajan et al. 1990). 2. The spatial distribution of three types of MFs was not random across frequency-band strips: for contra-field, ipsi-field, and central-field MFs there was a significant tendency for clustering of functions of the same type in sequentially encountered units. Occasionally, repeated clusters of a particular MF type could be found along a frequency-band strip. In contrast, the spatial distribution of omnidirectional MFs along frequency-band strips appeared to be random. 3. Apart from the clustering of MF types, there were also regions along a frequency-band strip in which there were rapid changes in the type of MF encountered in units isolated over short distances. Most often such changes took the form of irregular, rapid juxtapositions of MF types. Less frequently such changes appeared to show more systematic changes from one type of MF to another type. In contrast to these changes in azimuthal sensitivity seen in electrode penetrations oblique to the cortical surface, much less change in azimuthal sensitivity was seen in the form of azimuthal sensitivity displayed by successively isolated units in penetrations made normal to the cortical surface. 4. To determine whether some significant feature or features of azimuthal sensitivity shifted in a more continuous and/or systematic manner along frequency-band strips, azimuthal sensitivity was quantified in terms of the peak-response azimuth (PRA) of the MFs of successive units and of the azimuthal range over which the peaks occurred in the individual azimuth functions contributing to each MF (the peak-response range). In different experiments shifts in these measures of the peaks in successively isolated units along a frequency-band strip were found generally to fall into one of four categories: 1) shifts across the entire frontal hemifield; 2) clustering in the contralateral quadrant; 3) clustering in the ipsilateral quadrant; and 4) clustering about the midline. In two cases more than one of these four patterns were found along a frequency-band strip.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 82 (5) ◽  
pp. 2327-2345 ◽  
Author(s):  
Jagmeet S. Kanwal ◽  
Douglas C. Fitzpatrick ◽  
Nobuo Suga

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 BFlowcorresponding 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.


2010 ◽  
Vol 103 (5) ◽  
pp. 2339-2354 ◽  
Author(s):  
M. Vater ◽  
E. Foeller ◽  
E. C. Mora ◽  
F. Coro ◽  
I. J. Russell ◽  
...  

The primary auditory cortex (AI) of adult Pteronotus parnellii features a foveal representation of the second harmonic constant frequency (CF2) echolocation call component. In the corresponding Doppler-shifted constant frequency (DSCF) area, the 61 kHz range is over-represented for extraction of frequency-shift information in CF2 echoes. To assess to which degree AI postnatal maturation depends on active echolocation or/and reflects ongoing cochlear maturation, cortical neurons were recorded in juveniles up to postnatal day P29, before the bats are capable of active foraging. At P1-2, neurons in posterior AI are tuned sensitively to low frequencies (22–45 dB SPL, 28–35 kHz). Within the prospective DSCF area, neurons had insensitive responses (>60 dB SPL) to frequencies <40 kHz and lacked sensitive tuning curve tips. Up to P10, when bats do not yet actively echolocate, tonotopy is further developed and DSCF neurons respond to frequencies of 51–57 kHz with maximum tuning sharpness ( Q10dB) of 57. Between P11 and 20, the frequency representation in AI includes higher frequencies anterior and dorsal to the DSCF area. More multipeaked neurons (33%) are found than at older age. In the oldest group, DSCF neurons are tuned to frequencies close to 61 kHz with Q10dB values ≤212, and threshold sensitivity, tuning sharpness and cortical latencies are adult-like. The data show that basic aspects of cortical tonotopy are established before the bats actively echolocate. Maturation of tonotopy, increase of tuning sharpness, and upward shift in the characteristic frequency of DSCF neurons appear to strongly reflect cochlear maturation.


1998 ◽  
Vol 80 (5) ◽  
pp. 2743-2764 ◽  
Author(s):  
Jos J. Eggermont

Eggermont, Jos J. Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. J. Neurophysiol. 80: 2743–2764, 1998. This study investigates the degree of similarity of three different auditory cortical areas with respect to the coding of periodic stimuli. Simultaneous single- and multiunit recordings in response to periodic stimuli were made from primary auditory cortex (AI), anterior auditory field (AAF), and secondary auditory cortex (AII) in the cat to addresses the following questions: is there, within each cortical area, a difference in the temporal coding of periodic click trains, amplitude-modulated (AM) noise bursts, and AM tone bursts? Is there a difference in this coding between the three cortical fields? Is the coding based on the temporal modulation transfer function (tMTF) and on the all-order interspike-interval (ISI) histogram the same? Is the perceptual distinction between rhythm and roughness for AM stimuli related to a temporal versus spatial representation of AM frequency in auditory cortex? Are interarea differences in temporal response properties related to differences in frequency tuning? The results showed that: 1) AM stimuli produce much higher best modulation frequencies (BMFs) and limiting rates than periodic click trains. 2) For periodic click trains and AM noise, the BMFs and limiting rates were not significantly different for the three areas. However, for AM tones the BMF and limiting rates were about a factor 2 lower in AAF compared with the other areas. 3) The representation of stimulus periodicity in ISIs resulted in significantly lower mean BMFs and limiting rates compared with those estimated from the tMTFs. The difference was relatively small for periodic click trains but quite large for both AM stimuli, especially in AI and AII. 4) Modulation frequencies <20 Hz were represented in the ISIs, suggesting that rhythm is coded in auditory cortex in temporal fashion. 5) In general only a modest interdependence of spectral- and temporal-response properties in AI and AII was found. The BMFs were correlated positively with characteristic frequency in AAF. The limiting rate was positively correlated with the frequency-tuning curve bandwidth in AI and AII but not in AAF. Only in AAF was a correlation between BMF and minimum latency was found. Thus whereas differences were found in the frequency-tuning curve bandwidth and minimum response latencies among the three areas, the coding of periodic stimuli in these areas was fairly similar with the exception of the very poor representation of AM tones in AII. This suggests a strong parallel processing organization in auditory cortex.


2014 ◽  
Vol 315 ◽  
pp. 1-9 ◽  
Author(s):  
James B. Fallon ◽  
Robert K. Shepherd ◽  
David A.X. Nayagam ◽  
Andrew K. Wise ◽  
Leon F. Heffer ◽  
...  

1997 ◽  
Vol 181 (6) ◽  
pp. 615-633 ◽  
Author(s):  
J. R. Mendelson ◽  
C. E. Schreiner ◽  
M. L. Sutter

2003 ◽  
Vol 90 (4) ◽  
pp. 2660-2675 ◽  
Author(s):  
Jennifer F. Linden ◽  
Robert C. Liu ◽  
Maneesh Sahani ◽  
Christoph E. Schreiner ◽  
Michael M. Merzenich

The mouse is a promising model system for auditory cortex research because of the powerful genetic tools available for manipulating its neural circuitry. Previous studies have identified two tonotopic auditory areas in the mouse—primary auditory cortex (AI) and anterior auditory field (AAF)— but auditory receptive fields in these areas have not yet been described. To establish a foundation for investigating auditory cortical circuitry and plasticity in the mouse, we characterized receptive-field structure in AI and AAF of anesthetized mice using spectrally complex and temporally dynamic stimuli as well as simple tonal stimuli. Spectrotemporal receptive fields (STRFs) were derived from extracellularly recorded responses to complex stimuli, and frequency-intensity tuning curves were constructed from responses to simple tonal stimuli. Both analyses revealed temporal differences between AI and AAF responses: peak latencies and receptive-field durations for STRFs and first-spike latencies for responses to tone bursts were significantly longer in AI than in AAF. Spectral properties of AI and AAF receptive fields were more similar, although STRF bandwidths were slightly broader in AI than in AAF. Finally, in both AI and AAF, a substantial minority of STRFs were spectrotemporally inseparable. The spectrotemporal interaction typically appeared in the form of clearly disjoint excitatory and inhibitory subfields or an obvious spectrotemporal slant in the STRF. These data provide the first detailed description of auditory receptive fields in the mouse and suggest that although neurons in areas AI and AAF share many response characteristics, area AAF may be specialized for faster temporal processing.


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