Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex

1991 ◽  
Vol 65 (5) ◽  
pp. 1207-1226 ◽  
Author(s):  
M. L. Sutter ◽  
C. E. Schreiner

1. The physiology and topography of single neuron responses along the isofrequency domain of the middle- and high-frequency portions [characteristic frequencies (CFs) greater than 4 kHz] of the primary auditory cortex (AI) were investigated in the barbiturate-anesthetized cat. Single neurons were recorded at several locations along the extent of isofrequency contours, defined from initial multiple-unit mapping. For each neuron a high-resolution excitatory tuning curve was determined, and for some neurons high-resolution two-tone tuning curves were recorded to measure inhibitory/suppressive areas. 2. A physiologically distinct population of neurons was found in the dorsal part of cat AI. These neurons exhibited two or three distinct excitatory frequency ranges, whereas most neurons in AI responded with excitation to a single narrow frequency range. These were called multipeaked neurons because of the shape of their tuning curves. At frequencies between the excitatory regions, the multipeaked neurons were inhibited or unresponsive. 3. Multipeaked neurons exhibited several distinct threshold minima in their frequency tuning curves. Most of the multipeaked neurons (88%) displayed two frequency minima, whereas the rest exhibited three minima. 4. The frequency separation between threshold minima was less than 1 octave in 71% of the double-peaked neurons recorded. Occasionally, the frequency peaks of these neurons closely corresponded to a response to second and third harmonics without a response to the fundamental frequency. 5. Multipeaked neurons exhibited a wide range of total bandwidths (highest excitatory frequency minus lowest excitatory frequency expressed in octaves). Bandwidths of the isolated peaks within the same neuron were also quite variable. 6. Response latencies to tones with frequencies within each peak of a multipeaked neuron could vary considerably. In 71% (17) of the neurons, tones corresponding to the high-frequency peak (CFh) elicited a longer response latency (greater than 4 ms) than those corresponding to the low-frequency peak (CF1). 7. Inhibitory/suppressive bands, as demonstrated with a two-tone paradigm, were often present between the peaks. Typically, neurons with excitatory peaks of similar response latencies showed an inhibitory band located between the peaks. 8. Ninety percent of the topographically localized multipeaked neurons were in the dorsal part of AI (greater than 1 mm dorsal to the maximum in the sharpness-of-tuning map). Although these neurons were restricted to dorsal AI, only 35% of neurons in this region were multipeaked. 9. Multipeaked neurons could show decreased response latencies and thresholds to two-tone combinations.(ABSTRACT TRUNCATED AT 400 WORDS)

2013 ◽  
Vol 25 (2) ◽  
pp. 175-187 ◽  
Author(s):  
Jihoon Oh ◽  
Jae Hyung Kwon ◽  
Po Song Yang ◽  
Jaeseung Jeong

Neural responses in early sensory areas are influenced by top–down processing. In the visual system, early visual areas have been shown to actively participate in top–down processing based on their topographical properties. Although it has been suggested that the auditory cortex is involved in top–down control, functional evidence of topographic modulation is still lacking. Here, we show that mental auditory imagery for familiar melodies induces significant activation in the frequency-responsive areas of the primary auditory cortex (PAC). This activation is related to the characteristics of the imagery: when subjects were asked to imagine high-frequency melodies, we observed increased activation in the high- versus low-frequency response area; when the subjects were asked to imagine low-frequency melodies, the opposite was observed. Furthermore, we found that A1 is more closely related to the observed frequency-related modulation than R in tonotopic subfields of the PAC. Our findings suggest that top–down processing in the auditory cortex relies on a mechanism similar to that used in the perception of external auditory stimuli, which is comparable to early visual systems.


1996 ◽  
Vol 75 (1) ◽  
pp. 75-96 ◽  
Author(s):  
D. R. Irvine ◽  
R. Rajan ◽  
L. M. Aitkin

1. Interaural intensity differences (IIDs) provide the major cue to the azimuthal location of high-frequency narrowband sounds. In recent studies of the azimuthal sensitivity of high-frequency neurons in the primary auditory cortex (field AI) of the cat, a number of different types of azimuthal sensitivity have been described and the azimuthal sensitivity of many neurons was found to vary as a function of changes in stimulus intensity. The extent to which the shape and the intensity dependence of the azimuthal sensitivity of AI neurons reflects features of their IID sensitivity was investigated by obtaining data on IID sensitivity from a large sample of neurons with a characteristic frequency (CF) > 5.5 kHz in AI of anesthetized cats. IID sensitivity functions were classified in a manner that facilitated comparison with previously obtained data on azimuthal sensitivity, and the effects of changes in the base intensity at which IIDs were introduced were examined. 2. IID sensitivity functions for CF tonal stimuli were obtained at one or more intensities for a total of 294 neurons, in most cases by a method of generating IIDs that kept the average binaural intensity (ABI) of the stimuli at the two ears constant. In the standard ABI range at which a function was obtained for each unit, five types of IID sensitivity were distinguished. Contra-max neurons (50% of the sample) had maximum response (a peak or a plateau) at IIDs corresponding to contralateral azimuths, whereas ipsi-max neurons (17%) had the mirror-image form of sensitivity. Near-zero-max neurons (18%) had a clearly defined maximum response (peak) in the range of +/- 10 dB IID, whereas a small group of tough neurons (2%) had a restricted range of minimal responsiveness with near-maximal responses at IIDs on either side. A final 18% of AI neurons were classified as insensitive to IIDs. The proportions of neurons exhibiting the various types of sensitivity corresponded closely to the proportions found to exhibit corresponding types of azimuthal sensitivity in a previous study. 3. There was a strong correlation between a neuron's binaural interaction characteristics and the form of its IID sensitivity function. Thus, neurons excited by monaural stimulation of only one ear but with either inhibitory, facilitatory, or mixed facilitatory-inhibitory effects of stimulation of the other ear had predominantly contra-max IID sensitivity (if contralateral monaural stimulation was excitatory) or ipsi-max sensitivity (if ipsilateral monaural stimulation was excitatory). Neurons driven weakly or not at all by monaural stimulation but facilitated binaurally almost all exhibited near-zero-max IID sensitivity. The exception to this tight association between binaural input and IID sensitivity was provided by neurons excited by monaural stimulation of either ear (EE neurons). Although EE neurons have frequently been considered to be insensitive to IIDs, our data were in agreement with two recent reports indicating that they can exhibit various forms of IID sensitivity: only 23 of 75 EE neurons were classified as insensitive and the remainder exhibited diverse types of sensitivity. 4. IID sensitivity was examined at two or more intensities (3-5 in most cases) for 84 neurons. The form of the IID sensitivity function (defined in terms of both shape and position along the IID axis) was invariant with changes in ABI for only a small proportion of IID-sensitive neurons (approximately 15% if a strict criterion of invariance was employed), and for many of these neurons the spike counts associated with a given IID varied with ABI, particularly at near-threshold levels. When the patterns of variation in the form of IID sensitivity produced by changes in ABI were classified in a manner equivalent to that used previously to classify the effects of intensity on azimuthal sensitivity, there was a close correspondence between the effects of intensity on corresponding types of azimuthal and IID sensitivity


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.


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.


1997 ◽  
Vol 77 (2) ◽  
pp. 923-943 ◽  
Author(s):  
Michael Brosch ◽  
Christoph E. Schreiner

Brosch, Michael and Christoph E. Schreiner. Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 77: 923–943, 1997. Nonsimultaneous two-tone interactions were studied in the primary auditory cortex of anesthetized cats. Poststimulatory effects of pure tone bursts (masker) on the evoked activity of a fixed tone burst (probe) were investigated. The temporal interval from masker onset to probe onset (stimulus onset asynchrony), masker frequency, and intensity were parametrically varied. For all of the 53 single units and 58 multiple-unit clusters, the neural activity of the probe signal was either inhibited, facilitated, and/or delayed by a limited set of masker stimuli. The stimulus range from which forward inhibition of the probe was induced typically was centered at and had approximately the size of the neuron's excitatory receptive field. This “masking tuning curve” was usually V shaped, i.e., the frequency range of inhibiting masker stimuli increased with the masker intensity. Forward inhibition was induced at the shortest stimulus onset asynchrony between masker and probe. With longer stimulus onset asynchronies, the frequency range of inhibiting maskers gradually became smaller. Recovery from forward inhibition occurred first at the lower- and higher-frequency borders of the masking tuning curve and lasted the longest for frequencies close to the neuron's characteristic frequency. The maximal duration of forward inhibition was measured as the longest period over which reduction of probe responses was observed. It was in the range of 53–430 ms, with an average of 143 ± 71 (SD) ms. Amount, duration and type of forward inhibition were weakly but significantly correlated with “static” neural receptive field properties like characteristic frequency, bandwidth, and latency. For the majority of neurons, the minimal inhibitory masker intensity increased when the stimulus onset asynchrony became longer. In most cases the highest masker intensities induced the longest forward inhibition. A significant number of neurons, however, exhibited longest periods of inhibition after maskers of intermediate intensity. The results show that the ability of cortical cells to respond with an excitatory activity depends on the temporal stimulus context. Neurons can follow higher repetition rates of stimulus sequences when successive stimuli differ in their spectral content. The differential sensitivity to temporal sound sequences within the receptive field of cortical cells as well as across different cells could contribute to the neural processing of temporally structured stimuli like speech and animal vocalizations.


1988 ◽  
Vol 59 (5) ◽  
pp. 1627-1638 ◽  
Author(s):  
S. L. Sally ◽  
J. B. Kelly

1. Responses of neurons in the auditory cortex of the albino rat were examined using microelectrode mapping techniques. Characteristic frequencies were determined for numerous electrode penetrations across the cortical surface in individual animals. A primary auditory area was identified in the posterolateral neocortex that was characterized by short latency responses to tone bursts and tonotopic organization with high frequencies represented rostrally and low frequencies, caudally. Within this area cells with similar characteristic frequencies were aligned in a dorsoventral orientation to form isofrequency contours. 2. Tuning curves obtained from primary auditory cortex were characteristically "V" shaped with Q10's ranging from 0.97 to 28.4. Maximum Q10 values increased monotonically with characteristic frequency (CF). The lowest thresholds at CF closely approximated the behavioral audiogram for the albino rat. Many neurons, however, had CF thresholds well above the behavioral limit. 3. Areas were found dorsal and ventral to the primary auditory cortex in which CF's were clearly discontinuous with the neighboring isofrequency contours. These data suggest the presence of other auditory fields, the detailed characteristics of which have yet to be examined.


2006 ◽  
Vol 96 (3) ◽  
pp. 1105-1115 ◽  
Author(s):  
Yonatan I. Fishman ◽  
Mitchell Steinschneider

An important function of the auditory nervous system is to analyze the frequency content of environmental sounds. The neural structures involved in determining psychophysical frequency resolution remain unclear. Using a two-noise masking paradigm, the present study investigates the spectral resolution of neural populations in primary auditory cortex (A1) of awake macaques and the degree to which it matches psychophysical frequency resolution. Neural ensemble responses (auditory evoked potentials, multiunit activity, and current source density) evoked by a pulsed 60-dB SPL pure-tone signal fixed at the best frequency (BF) of the recorded neural populations were examined as a function of the frequency separation (ΔF) between the tone and two symmetrically flanking continuous 80-dB SPL, 50-Hz-wide bands of noise. ΔFs ranged from 0 to 50% of the BF, encompassing the range typically examined in psychoacoustic experiments. Responses to the signal were minimal for ΔF = 0% and progressively increased with ΔF, reaching a maximum at ΔF = 50%. Rounded exponential functions, used to model auditory filter shapes in psychoacoustic studies of frequency resolution, provided excellent fits to neural masking functions. Goodness-of-fit was greatest for response components in lamina 4 and lower lamina 3 and least for components recorded in more superficial cortical laminae. Physiological equivalent rectangular bandwidths (ERBs) increased with BF, measuring nearly 15% of the BF. These findings parallel results of psychoacoustic studies in both monkeys and humans, and thus indicate that a representation of perceptual frequency resolution is available at the level of A1.


2021 ◽  
Author(s):  
Katherine C. M. Chew ◽  
Vineet Kumar ◽  
Andrew Y. Y. Tan

Tone-evoked synaptic excitation and inhibition are highly correlated in many neurons with V-shaped tuning curves in the primary auditory cortex of pentobarbital-anesthetized rats. In contrast, there is less correlation between spontaneous excitation and inhibition in visual cortex neurons under the same anesthetic conditions. However, it was not known whether the primary auditory cortex resembles visual cortex in having spontaneous excitation and inhibition that is less correlated than tone-evoked excitation and inhibition. Here we report whole-cell voltage-clamp measurements of spontaneous excitation and inhibition in primary auditory cortex neurons of pentobarbital-anesthetized rats. The larger excursions of both spontaneous excitatory and inhibitory currents appeared to consist of distinct events, with the inhibitory event rate typically lower than the excitatory event rate. We use the ratio of the excitatory event rate to the inhibitory event rate, and the assumption that the excitatory and inhibitory synaptic currents can each be reasonably described as a filtered Poisson process, to estimate the maximum spontaneous excitatory-inhibitory correlation for each neuron. In a subset of neurons, we also measured tone-evoked excitation and inhibition. In neurons with V-shaped tuning curves, although tone-evoked excitation and inhibition were highly correlated, the spontaneous inhibitory event rate was typically sufficiently lower than the spontaneous excitatory event rate to indicate a lower excitatory-inhibitory correlation for spontaneous activity than for tone-evoked responses.


2007 ◽  
Vol 98 (5) ◽  
pp. 2933-2942 ◽  
Author(s):  
Kazuo Imaizumi ◽  
Christoph E. Schreiner

Primary sensory cortical areas are characterized by orderly and largely independent representations of several receptive field properties. This is expressed in multiple, spatially overlaying parameter distributions, such as orientation preference, spatial frequency, and ocular dominance maps in the primary visual cortex. In the auditory cortex, two main and presumably independent representational parameters are the center frequency and the frequency extent of spectral tuning curves. Here we demonstrate interactions between cortical tonotopic gradient and spectral bandwidth modules in cat primary auditory cortex (AI). First, the spatial representation of spectral integration is not equally expressed across the whole frequency range in AI. Narrow-bandwidth modules are found only in the mid-frequency region (5–20 kHz). Thus spectral integration properties delineate three frequency regions (<5, 5–20, and >20 kHz) in cat AI. Second, the extent of spectral integration covaries with the local tonotopic gradient in the low- and mid-frequency ranges. Regions with a shallow frequency gradient tend to have narrower spectral integration than those with a steep gradient. These relationships between spectral selectivity and frequency gradient constrain forebrain models of thalamo- and corticocortical convergence and connectivity and may reflect the processing of behaviorally relevant stimulus constellations.


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