Fine Control of Sound Frequency Tuning and Frequency Discrimination Acuity by Synaptic Zinc Signaling in Mouse Auditory Cortex

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.

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Frequency preference and attention effects across cortical depths in the human primary auditory cortex

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1507552112 ◽

2015 ◽

Vol 112 (52) ◽

pp. 16036-16041 ◽

Cited By ~ 106

Author(s):

Federico De Martino ◽

Michelle Moerel ◽

Kamil Ugurbil ◽

Rainer Goebel ◽

Essa Yacoub ◽

...

Keyword(s):

Auditory Cortex ◽

Frequency Tuning ◽

Primary Auditory Cortex ◽

Task Demands ◽

Sound Frequency ◽

7 Tesla ◽

Cortical Layers ◽

Functional Responses ◽

Feed Forward ◽

Deep Layers

Columnar arrangements of neurons with similar preference have been suggested as the fundamental processing units of the cerebral cortex. Within these columnar arrangements, feed-forward information enters at middle cortical layers whereas feedback information arrives at superficial and deep layers. This interplay of feed-forward and feedback processing is at the core of perception and behavior. Here we provide in vivo evidence consistent with a columnar organization of the processing of sound frequency in the human auditory cortex. We measure submillimeter functional responses to sound frequency sweeps at high magnetic fields (7 tesla) and show that frequency preference is stable through cortical depth in primary auditory cortex. Furthermore, we demonstrate that—in this highly columnar cortex—task demands sharpen the frequency tuning in superficial cortical layers more than in middle or deep layers. These findings are pivotal to understanding mechanisms of neural information processing and flow during the active perception of sounds.

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Arousal regulates frequency tuning in primary auditory cortex

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1911383116 ◽

2019 ◽

Vol 116 (50) ◽

pp. 25304-25310 ◽

Cited By ~ 7

Author(s):

Pei-Ann Lin ◽

Samuel K. Asinof ◽

Nicholas J. Edwards ◽

Jeffry S. Isaacson

Keyword(s):

Auditory Cortex ◽

Frequency Tuning ◽

Primary Auditory Cortex ◽

Pyramidal Cells ◽

Frequency Discrimination ◽

Recurrent Network ◽

Excitatory Input ◽

Network Activity ◽

Shape Tuning

Changes in arousal influence cortical sensory representations, but the synaptic mechanisms underlying arousal-dependent modulation of cortical processing are unclear. Here, we use 2-photon Ca2+ imaging in the auditory cortex of awake mice to show that heightened arousal, as indexed by pupil diameter, broadens frequency-tuned activity of layer 2/3 (L2/3) pyramidal cells. Sensory representations are less sparse, and the tuning of nearby cells more similar when arousal increases. Despite the reduction in selectivity, frequency discrimination by cell ensembles improves due to a decrease in shared trial-to-trial variability. In vivo whole-cell recordings reveal that mechanisms contributing to the effects of arousal on sensory representations include state-dependent modulation of membrane potential dynamics, spontaneous firing, and tone-evoked synaptic potentials. Surprisingly, changes in short-latency tone-evoked excitatory input cannot explain the effects of arousal on the broadness of frequency-tuned output. However, we show that arousal strongly modulates a slow tone-evoked suppression of recurrent excitation underlying lateral inhibition [H. K. Kato, S. K. Asinof, J. S. Isaacson, Neuron, 95, 412–423, (2017)]. This arousal-dependent “network suppression” gates the duration of tone-evoked responses and regulates the broadness of frequency tuning. Thus, arousal can shape tuning via modulation of indirect changes in recurrent network activity.

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Tuning to Sound Frequency in Auditory Field Potentials

Journal of Neurophysiology ◽

10.1152/jn.00358.2007 ◽

2007 ◽

Vol 98 (3) ◽

pp. 1806-1809 ◽

Cited By ~ 33

Author(s):

Christoph Kayser ◽

Christopher I. Petkov ◽

Nikos K. Logothetis

Keyword(s):

Auditory Cortex ◽

Functional Imaging ◽

High Frequency ◽

Auditory Evoked Potentials ◽

Frequency Tuning ◽

Sound Frequency ◽

Mass Action ◽

Oscillatory Activity ◽

Field Potentials ◽

Frequency Bands

Neurons in auditory cortex are selective for the frequency content of acoustical stimuli. Classically, this response selectivity is studied at the single-neuron level. However, current research often employs functional imaging techniques to investigate the organization of auditory cortex. The signals underlying the imaging data arise from neural mass action and reflect the properties of populations of neurons. For example, the signal used for functional magnetic resonance imaging (fMRI-BOLD) was shown to correlate with the oscillatory activity quantified by local field potentials (LFPs). This raises the questions of how the frequency selectivity in neuronal population signals compares with the tuning of spiking responses. To address this, we quantified tuning properties of auditory-evoked potentials (AEP), different frequency bands of the LFP, analog multi-unit (AMUA), and spike-sorted single- and multiunit activity in auditory cortex. The AMUA showed a close correspondence in frequency tuning to the spike-sorted activity. In contrast, for the LFP, we found a clear dissociation of high- and low-frequency bands: there was a gradual increase of tuning-curve similarity, tuning specificity, and information about the stimulus with increasing LFP frequency. Although properties of the high-frequency LFP matched those of spiking activity, the lower-frequency bands differed considerably as did the AEP. These results demonstrate that electrophysiological population responses exhibit varying degrees of frequency tuning and suggest that those functional imaging methods that are related to high-frequency oscillatory activity should well reflect the neuronal processing of sound frequency.

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Blocking c-Fos Expression Reveals the Role of Auditory Cortex Plasticity in Sound Frequency Discrimination Learning

Cerebral Cortex ◽

10.1093/cercor/bhx060 ◽

2017 ◽

Vol 28 (5) ◽

pp. 1645-1655 ◽

Cited By ~ 7

Author(s):

Livia de Hoz ◽

Dorota Gierej ◽

Victoria Lioudyno ◽

Jacek Jaworski ◽

Magda Blazejczyk ◽

...

Keyword(s):

Auditory Cortex ◽

Discrimination Learning ◽

Frequency Discrimination ◽

Sound Frequency ◽

Fos Expression

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The Effect of Weak Background Noise on The Frequency Tuning of Neurons in The Rat Auditory Cortex*

PROGRESS IN BIOCHEMISTRY AND BIOPHYSICS ◽

10.3724/sp.j.1206.2012.00114 ◽

2012 ◽

Vol 39 (11) ◽

pp. 1082-1088

Author(s):

Yin-Ting PENG ◽

Qing PU ◽

Xin-De SUN ◽

Ji-Ping ZHANG

Keyword(s):

Auditory Cortex ◽

Background Noise ◽

Frequency Tuning

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The effects of contrast on visual orientation and spatial frequency discrimination: a comparison of single cells and behavior

Journal of Neurophysiology ◽

10.1152/jn.1987.57.3.773 ◽

1987 ◽

Vol 57 (3) ◽

pp. 773-786 ◽

Cited By ~ 186

Author(s):

B. C. Skottun ◽

A. Bradley ◽

G. Sclar ◽

I. Ohzawa ◽

R. D. Freeman

Keyword(s):

Spatial Frequency ◽

Striate Cortex ◽

Frequency Tuning ◽

Single Cells ◽

Frequency Discrimination ◽

Frequency Selectivity ◽

Response Amplitude ◽

Visual Orientation ◽

Characteristic Analysis ◽

Response Variance

We have compared the effects of contrast on human psychophysical orientation and spatial frequency discrimination thresholds and on the responses of individual neurons in the cat's striate cortex. Contrast has similar effects on orientation and spatial frequency discrimination: as contrast is increased above detection threshold, orientation and spatial frequency discrimination performance improves but reaches maximum levels at quite low contrasts. Further increases in contrast produce no further improvements in discrimination. We measured the effects of contrast on response amplitude, orientation and spatial frequency selectivity, and response variance of neurons in the cat's striate cortex. Orientation and spatial frequency selectivity vary little with contrast. Also, the ratio of response variance to response mean is unaffected by contrast. Although, in many cells, response amplitude increases approximately linearly with log contrast over most of the visible range, some cells show complete or partial saturation of response amplitude at medium contrasts. Therefore, some cells show a clear increase in slope of the orientation and spatial frequency tuning functions with increasing contrast, whereas in others the slopes reach maximum values at medium contrasts. Using receiver operating characteristic analysis, we estimated the minimum orientation and spatial frequency differences that can be signaled reliably as a response change by an individual cell. This analysis shows that, on average, the discrimination of orientation or spatial frequency improves with contrast at low contrasts more than at higher contrasts. Using the optimal stimulus for each cell, we estimated the contrast threshold of 48 neurons. Most cells had contrast thresholds below 5%. Thresholds were only slightly higher for nonoptimal stimuli. Therefore, increasing the contrast of sinusoidal gratings above approximately 10% will not produce large increases in the number of responding cells. The observed effects of contrast on the response characteristics of nonsaturating cortical cells do not appear consistent with the psychophysical results. Cells that reach their maximum response at low-to-medium contrasts may account for the contrast independence of psychophysical orientation and spatial frequency discrimination thresholds at medium and high contrasts.

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Broadened Population-Level Frequency Tuning in Human Auditory Cortex of Portable Music Player Users

PLoS ONE ◽

10.1371/journal.pone.0017022 ◽

2011 ◽

Vol 6 (3) ◽

pp. e17022 ◽

Cited By ~ 5

Author(s):

Hidehiko Okamoto ◽

Henning Teismann ◽

Ryusuke Kakigi ◽

Christo Pantev

Keyword(s):

Auditory Cortex ◽

Frequency Tuning ◽

Population Level ◽

Human Auditory Cortex ◽

Music Player

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Monaural inhibition in cat auditory cortex

Journal of Neurophysiology ◽

10.1152/jn.1995.73.5.1876 ◽

1995 ◽

Vol 73 (5) ◽

pp. 1876-1891 ◽

Cited By ~ 187

Author(s):

M. B. Calford ◽

M. N. Semple

Keyword(s):

Auditory Cortex ◽

Lateral Inhibition ◽

Cortical Neurons ◽

Frequency Tuning ◽

Inhibitory Response ◽

Forward Masking ◽

Excitatory Response ◽

Rate Level ◽

Wide Range ◽

Response Area

1. Several studies of auditory cortex have examined the competitive inhibition that can occur when appropriate sounds are presented to each ear. However, most cortical neurons also show both excitation and inhibition in response to presentation of stimuli at one ear alone. The extent of such inhibition has not been described. Forward masking, in which a variable masking stimulus was followed by a fixed probe stimulus (within the excitatory response area), was used to examine the extent of monaural inhibition for neurons in primary auditory cortex of anesthetized cats (barbiturate or barbiturate-ketamine). Both the masking and probe stimuli were 50-ms tone pips presented to the contralateral ear. Most cortical neurons showed significant forward masking at delays beyond which masking effects in the auditory nerve are relatively small compared with those seen in cortical neurons. Analysis was primarily concerned with such components. Standard rate-level functions were also obtained and were examined for nonmonotonicity, an indication of level-dependent monaural inhibition. 2. Consistent with previous reports, a wide range of frequency tuning properties (excitatory response area shapes) was found in cortical neurons. This was matched by a wide range of forward-masking-derived inhibitory response areas. At the most basic level of analysis, these were classified according to the presence of lateral inhibition, i.e., where a probe tone at a neuron's characteristic frequency was masked by tones outside the limits of the excitatory response area. Lateral inhibition was a property of 38% of the sampled neurons. Such neurons represented 77% of those with nonmonotonic rate-level functions, indicating a strong correlation between the two indexes of monaural inhibition; however, the shapes of forward masking inhibitory response areas did not usually correspond with those required to account for the "tuning" of a neuron. In addition, it was found that level-dependent inhibition was not added to by forward masking inhibition. 3. Analysis of the discharges to individual stimulus pair presentations, under conditions of partial masking, revealed that discharges to the probe occurred independently of discharges to the preceding masker. This indicates that even when the masker is within a neuron's excitatory response area, forward masking is not a postdischarge habituation phenomenon. However, for most neurons the degree of masking summed over multiple stimulus presentations appears determined by the same stimulus parameters that determine the probability of response to the masker.(ABSTRACT TRUNCATED AT 400 WORDS)

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Functional Role of Auditory Cortex in Frequency Processing and Pitch Perception

Journal of Neurophysiology ◽

10.1152/jn.00104.1999 ◽

2002 ◽

Vol 87 (1) ◽

pp. 122-139 ◽

Cited By ~ 70

Author(s):

Mark Jude Tramo ◽

Gaurav D. Shah ◽

Louis D. Braida

Keyword(s):

Auditory Cortex ◽

Pure Tone ◽

Current Knowledge ◽

Frequency Discrimination ◽

Frequency Selectivity ◽

Frequency Resolution ◽

Frequency Change ◽

Fine Grained ◽

Difference Thresholds ◽

Frequency Processing

Microelectrode studies in nonhuman primates and other mammals have demonstrated that many neurons in auditory cortex are excited by pure tone stimulation only when the tone's frequency lies within a narrow range of the audible spectrum. However, the effects of auditory cortex lesions in animals and humans have been interpreted as evidence against the notion that neuronal frequency selectivity is functionally relevant to frequency discrimination. Here we report psychophysical and anatomical evidence in favor of the hypothesis that fine-grained frequency resolution at the perceptual level relies on neuronal frequency selectivity in auditory cortex. An adaptive procedure was used to measure difference thresholds for pure tone frequency discrimination in five humans with focal brain lesions and eight normal controls. Only the patient with bilateral lesions of primary auditory cortex and surrounding areas showed markedly elevated frequency difference thresholds: Weber fractions for frequency direction discrimination (“higher”—“lower” pitch judgments) were about eightfold higher than Weber fractions measured in patients with unilateral lesions of auditory cortex, auditory midbrain, or dorsolateral frontal cortex; Weber fractions for frequency change discrimination (“same”—“different” pitch judgments) were about seven times higher. In contrast, pure-tone detection thresholds, difference thresholds for pure tone duration discrimination centered at 500 ms, difference thresholds for vibrotactile intensity discrimination, and judgments of visual line orientation were within normal limits or only mildly impaired following bilateral auditory cortex lesions. In light of current knowledge about the physiology and anatomy of primate auditory cortex and a review of previous lesion studies, we interpret the present results as evidence that fine-grained frequency processing at the perceptual level relies on the integrity of finely tuned neurons in auditory cortex.

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