Responses of neurons in the marmoset primary auditory cortex to interaural level differences: comparison of pure tones and vocalizations

Previous studies in anesthetized animals reported that the primary auditory cortex (A1) showed homogenous phasic responses to FM tones, namely a transient response to a particular instantaneous frequency when FM sweeps traversed a neuron's tone-evoked receptive field (TRF). Here, in awake cats, we report that A1 cells exhibit heterogeneous FM responses, consisting of three patterns. The first is continuous firing when a slow FM sweep traverses the receptive field of a cell with a sustained tonal response. The duration and amplitude of FM response decrease with increasing sweep speed. The second pattern is transient firing corresponding to the cell's phasic tonal response. This response could be evoked only by a fast FM sweep through the cell's TRF, suggesting a preference for fast FM. The third pattern was associated with the off response to pure tones and was composed of several discrete response peaks during slow FM stimulus. These peaks were not predictable from the cell's tonal response but reliably reflected the time when FM swept across specific frequencies. Our A1 samples often exhibited a complex response pattern, combining two or three of the basic patterns above, resulting in a heterogeneous response population. The diversity of FM responses suggests that A1 use multiple mechanisms to fully represent the whole range of FM parameters, including frequency extent, sweep speed, and direction.

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Functional Organization of Squirrel Monkey Primary Auditory Cortex: Responses to Pure Tones

Journal of Neurophysiology ◽

10.1152/jn.2001.85.4.1732 ◽

2001 ◽

Vol 85 (4) ◽

pp. 1732-1749 ◽

Cited By ~ 75

Author(s):

Steven W. Cheung ◽

Purvis H. Bedenbaugh ◽

Srikantan S. Nagarajan ◽

Christoph E. Schreiner

Keyword(s):

Receptive Field ◽

Auditory Cortex ◽

Squirrel Monkey ◽

Spatial Organization ◽

Functional Organization ◽

Primary Auditory Cortex ◽

Complex Sound ◽

Sound Coding ◽

Field Gradients ◽

Pure Tones

The spatial organization of response parameters in squirrel monkey primary auditory cortex (AI) accessible on the temporal gyrus was determined with the excitatory receptive field to pure tone stimuli. Dense, microelectrode mapping of the temporal gyrus in four animals revealed that characteristic frequency (CF) had a smooth, monotonic gradient that systematically changed from lower values (0.5 kHz) in the caudoventral quadrant to higher values (5–6 kHz) in the rostrodorsal quadrant. The extent of AI on the temporal gyrus was ∼4 mm in the rostrocaudal axis and 2–3 mm in the dorsoventral axis. The entire length of isofrequency contours below 6 kHz was accessible for study. Several independent, spatially organized functional response parameters were demonstrated for the squirrel monkey AI. Latency, the asymptotic minimum arrival time for spikes with increasing sound pressure levels at CF, was topographically organized as a monotonic gradient across AI nearly orthogonal to the CF gradient. Rostral AI had longer latencies (range = 4 ms). Threshold and bandwidth co-varied with the CF. Factoring out the contribution of the CF on threshold variance, residual threshold showed a monotonic gradient across AI that had higher values (range = 10 dB) caudally. The orientation of the threshold gradient was significantly different from the CF gradient. CF-corrected bandwidth, residual Q10, was spatially organized in local patches of coherent values whose loci were specific for each monkey. These data support the existence of multiple, overlying receptive field gradients within AI and form the basis to develop a conceptual framework to understand simple and complex sound coding in mammals.

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Phase-locked responses to pure tones in the primary auditory cortex

Hearing Research ◽

10.1016/s0378-5955(02)00580-4 ◽

2002 ◽

Vol 172 (1-2) ◽

pp. 160-171 ◽

Cited By ~ 40

Author(s):

Mark N Wallace ◽

Trevor M Shackleton ◽

Alan R Palmer

Keyword(s):

Auditory Cortex ◽

Primary Auditory Cortex ◽

Pure Tones

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A model of the primary auditory cortex response to sequences of pure tones

BMC Neuroscience ◽

10.1186/1471-2202-10-s1-p151 ◽

2009 ◽

Vol 10 (Suppl 1) ◽

pp. P151

Author(s):

Ernest Montbrió ◽

Johan P Larsson ◽

Rita Almeida ◽

Gustavo Deco

Keyword(s):

Auditory Cortex ◽

Primary Auditory Cortex ◽

Pure Tones

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Location of cells giving phase-locked responses to pure tones in the primary auditory cortex

Hearing Research ◽

10.1016/j.heares.2010.05.012 ◽

2011 ◽

Vol 274 (1-2) ◽

pp. 142-151 ◽

Cited By ~ 7

Author(s):

M.N. Wallace ◽

B. Coomber ◽

C.J. Sumner ◽

J.M.S. Grimsley ◽

T.M. Shackleton ◽

...

Keyword(s):

Auditory Cortex ◽

Primary Auditory Cortex ◽

Pure Tones

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Frequency and amplitude representations in anterior primary auditory cortex of the mustached bat

Journal of Neurophysiology ◽

10.1152/jn.1983.50.5.1182 ◽

1983 ◽

Vol 50 (5) ◽

pp. 1182-1196 ◽

Cited By ~ 24

Author(s):

A. Asanuma ◽

D. Wong ◽

N. Suga

Keyword(s):

Auditory Cortex ◽

Second Harmonic ◽

Free Field ◽

Primary Auditory Cortex ◽

Frequency Component ◽

Constant Frequency ◽

Mustached Bat ◽

Pteronotus Parnellii ◽

Frequency Representation ◽

Pure Tones

The orientation sound emitted by the Panamanian mustached bat, Pteronotus parnellii rubiginosus, consists of four harmonics. The third harmonic is 6-12 dB weaker than the predominant second harmonic and consists of a long constant-frequency component (CF3) at about 92 kHz and a short frequency-modulated component (FM3) sweeping from about 92 to 74 kHz. Our primary aim is to examine how CF3 and FM3 are represented in a region of the primary auditory cortex anterior to the Doppler-shifted constant-frequency (DSCF) area. Extracellular recordings of neuronal responses from the unanesthetized animal were obtained during free-field stimulation of the ears with pure tones. FM sounds, and signals simulating their orientation sounds and echoes. Response properties of neurons and tonotopic and amplitopic representations were examined in the primary and the anteroventral nonprimary auditory cortex. In the anterior primary auditory cortex, neurons responded strongly to single pure tones but showed no facilitative responses to paired stimuli. Neurons with best frequencies from 110 to 90 kHz were tonotopically organized rostrocaudally, with higher frequencies located more rostrally. Neurons tuned to 92-94 kHz were overpresented, whereas neurons tuned to sound between 64 and 91 kHz were rarely found. Consequently a striking discontinuity in frequency representation from 91 to 64 kHz was found across the anterior DSCF border. Most neurons exhibited monotonic impulse-count functions and responded maximally to sound pressure level (SPL). There were also neurons that responded best to weak sounds but unlike the DSCF area, amplitopic representation was not found. Thus, the DSCF area is quite unique not only in its extensive representation of frequencies in the second harmonic CF component but also in its amplitopic representation. The anteroventral nonprimary auditory cortex consisted of neurons broadly tuned to pure tones between 88 and 99 kHz. Neither tonotopic nor amplitopic representation was observed. Caudal to this area and near the anteroventral border of the DSCF area, a small cluster of FM-FM neurons sensitive to particular echo delays was identified. The responses of these neurons fluctuated significantly during repetitive stimulation.

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Response Patterns Along an Isofrequency Contour in Cat Primary Auditory Cortex (AI) to Stimuli Varying in Average and Interaural Levels

Journal of Neurophysiology ◽

10.1152/jn.00171.2003 ◽

2004 ◽

Vol 91 (1) ◽

pp. 118-135 ◽

Cited By ~ 30

Author(s):

Kyle T. Nakamoto ◽

Jiping Zhang ◽

Leonard M. Kitzes

Keyword(s):

Auditory Cortex ◽

Characteristic Frequency ◽

Primary Auditory Cortex ◽

Sound Level ◽

Response Patterns ◽

Single Neurons ◽

Sound Location ◽

Interaural Level Differences

The topographical response of a portion of an isofrequency contour in primary cat auditory cortex (AI) to a series of monaural and binaural stimuli was studied. Responses of single neurons to monaural and a matrix of binaural characteristic frequency tones, varying in average binaural level (ABL) and interaural level differences (ILD), were recorded. The topography of responses to monaural and binaural stimuli was appreciably different. Patches of cells that responded monotonically to increments in ABL alternated with patches that responded nonmonotonically to ABL. The patches were between 0.4 and 1 mm in length along an isofrequency contour. Differences were found among monotonic patches and among nonmonotonic patches. Topographically, activated and silent populations of neurons varied with both changes in ILD and changes in ABL, suggesting that the area of responsive units may underlie the coding of sound level and sound location.

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Magnetic fields evoked by amplitude modulated pure tones demonstrate enhanced activation of the primary auditory cortex in musicians

NeuroImage ◽

10.1016/s1053-8119(00)91616-1 ◽

2000 ◽

Vol 11 (5) ◽

pp. S686

Author(s):

Peter Schneider ◽

Andre Rupp ◽

Hans Günter Dosch ◽

Hans Joachim Specht ◽

Christoph Stippich ◽

...

Keyword(s):

Magnetic Fields ◽

Auditory Cortex ◽

Primary Auditory Cortex ◽

Pure Tones

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Binaural Interaction Revisited in the Cat Primary Auditory Cortex

Journal of Neurophysiology ◽

10.1152/jn.00166.2003 ◽

2004 ◽

Vol 91 (1) ◽

pp. 101-117 ◽

Cited By ~ 37

Author(s):

Jiping Zhang ◽

Kyle T. Nakamoto ◽

Leonard M. Kitzes

Keyword(s):

Auditory Cortex ◽

Large Population ◽

Primary Auditory Cortex ◽

Lower Proportion ◽

Response Functions ◽

Interaction Type ◽

Binaural Interaction ◽

The Matrix ◽

Interaural Level Differences ◽

Tonal Stimuli

The binaural interactions of neurons were studied in the primary auditory cortex (AI) of barbiturate-anesthetized cats with a matrix of binaural tonal stimuli varying in both interaural level differences (ILD) and average binaural level (ABL). The purpose of this study was to determine: 1) the distribution of preferred binaural combinations (PBCs) of a large population of neurons and its relationships with binaural interactions and binaural monotonicity; 2) whether monaural responses are predictive of binaural responses; and 3) whether there is a restricted set of representative binaural stimulus configurations that could effectively classify the binaural interactions. Binaural interactions were often diverse in the matrix and dependent on both ABL and ILD. Compared with previous studies, a higher proportion of mixed binaural interaction type and a lower proportion of EO/I type were found. No monaural neurons were found. Binaural responses often differed from monaural responses in the number of spikes and/or the form of the response functions. The PBCs of the majority of EO and PB neurons were in the contralateral field and midline, respectively. However, the PBCs of EE units were evenly distributed across the contralateral and ipsilateral fields. The majority of the nonmonotonic neurons responded most strongly to lower ABLs, whereas the majority of monotonic neurons responded most strongly to higher ABLs. This study demonstrated that in AI a restricted set of binaural stimulus configurations is not sufficient to reveal the binaural responses properties. Also, monaural responses are not predictive of binaural responses.

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Effects of ear plugging on single-unit azimuth sensitivity in cat primary auditory cortex. II. Azimuth tuning dependent upon binaural stimulation

Journal of Neurophysiology ◽

10.1152/jn.1994.71.6.2194 ◽

1994 ◽

Vol 71 (6) ◽

pp. 2194-2216 ◽

Cited By ~ 21

Author(s):

F. K. Samson ◽

P. Barone ◽

J. C. Clarey ◽

T. J. Imig

Keyword(s):

Auditory Cortex ◽

Single Unit ◽

Free Field ◽

Primary Auditory Cortex ◽

Excitatory Input ◽

Spectral Cues ◽

Binaural Stimulation ◽

Monaural Stimulation ◽

Monaural Spectral Cues ◽

Interaural Level Differences

1. Single-unit recordings were carried out in primary auditory cortex (AI) of barbiturate-anesthetized cats. Observations were based on a sample of 131 high-best-frequency (> 5 kHz), azimuth-sensitive neurons. These were identified by their responses to a set of noise bursts, presented in the free field, that varied in azimuth and sound-pressure level (SPL). Each azimuth-sensitive neuron responded well to some levels at certain azimuths, but did not respond well to any level at other azimuths. 2. Unilateral ear plugging was used to infer each neuron's response to monaural stimulation. Ear plugs, produced by injecting a plastic ear mold compound into the external ear, attenuated sound reaching the tympanic membrane by 25–70 dB. The azimuth tuning of a large proportion of the sample (62/131), referred to as binaural directional (BD), was completely dependent upon binaural stimulation because with one ear plugged, these cells were insensitive to azimuth (either responded well at all azimuths or failed to respond at any azimuth) or in a few cases exhibited striking changes in location of azimuth function peaks. This report describes patterns of monaural responses and binaural interactions exhibited by BD neurons and relates them to each cell's azimuth and level tuning. The response of BD cells to ear plugging is consistent with the hypothesis that they derive azimuth tuning from interaural level differences present in noise bursts. Another component of the sample consisted of monaural directional (27/131) cells that derived azimuth tuning in part or entirely from monaural spectral cues. Cells in the remaining portion of the sample (42/131) responded too unreliably to permit specific conclusions. 3. Binaural interactions were inferred by statistical comparison of a cell's responses to monaural (unilateral plug) and binaural (no plug) stimulation. A larger binaural response than either monaural response was taken as evidence for binaural facilitation. A smaller binaural than monaural response was taken as evidence for binaural inhibition. Binaural facilitation was exhibited by 65% (40/62) of the BD sample (facilitatory cells). Many of these exhibited mixed interactions, i.e., binaural facilitation occurred in response to some azimuth-level combinations, and binaural inhibition to others. Binaural inhibition in the absence of binaural facilitation occurred in 35% (22/62) of the BD sample, a majority of which were EI cells, so called because they received excitatory (E) input from one ear (excitatory ear) and inhibitory (I) input from the other (inhibitory ear). One cell that exhibited binaural inhibition received excitatory input from each ear.(ABSTRACT TRUNCATED AT 400 WORDS)

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