Spectral Integration in A1 of Awake Primates: Neurons With Single- and Multipeaked Tuning Characteristics

Siddhartha C. Kadia; Xiaoqin Wang

doi:10.1152/jn.00271.2001

Spectral Integration in A1 of Awake Primates: Neurons With Single- and Multipeaked Tuning Characteristics

Journal of Neurophysiology ◽

10.1152/jn.00271.2001 ◽

2003 ◽

Vol 89 (3) ◽

pp. 1603-1622 ◽

Cited By ~ 95

Author(s):

Siddhartha C. Kadia ◽

Xiaoqin Wang

Keyword(s):

Frequency Tuning ◽

Primary Auditory Cortex ◽

Complex Sounds ◽

Spectral Integration ◽

Sound Levels ◽

Classical Receptive Field ◽

Wide Range ◽

Spectral Peaks ◽

A1 Neurons ◽

Processing Properties

We investigated modulations by stimulus components placed outside of the classical receptive field in the primary auditory cortex (A1) of awake marmosets. Two classes of neurons were identified using single tone stimuli: neurons with single-peaked frequency tuning characteristics (147/185, 80%) and neurons with multipeaked frequency tuning characteristics (38/185, 20%), referred to as single- and multipeaked units, respectively. Each class of neurons was further studied using two-tone paradigms in which the frequency, intensity, and timing of the second tone were systematically varied while a unit was driven by the first tone placed at a unit's characteristic frequency (CF) if it was single-peaked or at one of multiple spectral peaks if it was multipeaked. The main findings were: 1) excitatory spectral peaks in the frequency tuning of the multipeaked units were often harmonically related. 2) Multipeaked units showed facilitation in their responses to combinations of two harmonically related tones placed at the spectral peaks of their frequency tuning. The two-tone facilitation was strongest for the simultaneously presented tones. 3) In 76 of 113 single-peaked units studied using the two-tone paradigm, facilitatory and/or inhibitory modulations by distant off-CF tones were observed. This distant inhibition differed from flanking (or side-band) inhibitions near CF. 4) In single-peaked units, the distant off-CF inhibitions were dominated by tones at frequencies that were harmonically related to the CF of a unit, whereas the facilitation by off-CF tones was observed for a wide range of frequencies. And 5) in both single- and multipeaked units, sound levels of two interacting tones determined whether the two tones produced excitation or inhibition. The largest facilitation was achieved by using two tones at their corresponding preferred sound levels. Together, these findings suggest that extracting or rejecting harmonically related components embedded in complex sounds may represent fundamental signal processing properties in different classes of A1 neurons.

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Local Homogeneity of Tonotopic Organization in the Primary Auditory Cortex of Marmosets

10.1101/398677 ◽

2018 ◽

Author(s):

Huan-huan Zeng ◽

Jun-feng Huang ◽

Ming Chen ◽

Yun-qing Wen ◽

Zhi-ming Shen ◽

...

Keyword(s):

Auditory Cortex ◽

Large Scale ◽

Frequency Tuning ◽

Primary Auditory Cortex ◽

Primate Species ◽

Tonotopic Organization ◽

Brain Structure And Function ◽

A1 Neurons ◽

Cortical Regions

AbstractMarmoset has emerged as a useful non-human primate species for studying the brain structure and function. Previous studies on the mouse primary auditory cortex (A1) showed that neurons with preferential frequency tuning responses are mixed within local cortical regions, despite a large-scale tonotopic organization. Here we found that frequency tuning properties of marmoset A1 neurons are highly uniform within local cortical regions. We first defined tonotopic map of A1 using intrinsic optical imaging, and then used in vivo two-photon calcium imaging of large neuronal populations to examine the tonotopic preference at the single-cell level. We found that tuning preferences of layer 2/3 neurons were highly homogeneous over hundreds of micrometers in both horizontal and vertical directions. Thus, marmoset A1 neurons are distributed in a tonotopic manner at both macro- and microscopic levels. Such organization is likely to be important for the organization of auditory circuits in the primate brain.

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Neural representation of spectral and temporal information in speech

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2007.2151 ◽

2007 ◽

Vol 363 (1493) ◽

pp. 923-945 ◽

Cited By ~ 55

Author(s):

Eric D Young

Keyword(s):

Neural Coding ◽

Frequency Tuning ◽

Neural Representation ◽

Complex Sounds ◽

Sound Levels ◽

Language Communication ◽

Frequency Components ◽

The Central Nervous System ◽

Stimulus Features ◽

Central Auditory Neurons

Speech is the most interesting and one of the most complex sounds dealt with by the auditory system. The neural representation of speech needs to capture those features of the signal on which the brain depends in language communication. Here we describe the representation of speech in the auditory nerve and in a few sites in the central nervous system from the perspective of the neural coding of important aspects of the signal. The representation is tonotopic, meaning that the speech signal is decomposed by frequency and different frequency components are represented in different populations of neurons. Essential to the representation are the properties of frequency tuning and nonlinear suppression. Tuning creates the decomposition of the signal by frequency, and nonlinear suppression is essential for maintaining the representation across sound levels. The representation changes in central auditory neurons by becoming more robust against changes in stimulus intensity and more transient. However, it is probable that the form of the representation at the auditory cortex is fundamentally different from that at lower levels, in that stimulus features other than the distribution of energy across frequency are analysed.

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Temporally precise population coding of dynamic sounds by auditory cortex

Journal of Neurophysiology ◽

10.1152/jn.00709.2020 ◽

2021 ◽

Author(s):

Joshua D Downer ◽

James Bigelow ◽

Melissa Runfeldt ◽

Brian James Malone

Keyword(s):

Auditory Cortex ◽

Cortical Neurons ◽

Frequency Tuning ◽

Average Rate ◽

Relative Effectiveness ◽

Primary Auditory Cortex ◽

Population Based ◽

Population Coding ◽

Complex Sounds ◽

Animal Vocalizations

Fluctuations in the amplitude envelope of complex sounds provide critical cues for hearing, particularly for speech and animal vocalizations. Responses to amplitude modulation (AM) in the ascending auditory pathway have chiefly been described for single neurons. How neural populations might collectively encode and represent information about AM remains poorly characterized, even in primary auditory cortex (A1). We modeled population responses to AM based on data recorded from A1 neurons in awake squirrel monkeys and evaluated how accurately single trial responses to modulation frequencies from 4 to 512 Hz could be decoded as functions of population size, composition, and correlation structure. We found that a population-based decoding model that simulated convergent, equally weighted inputs was highly accurate and remarkably robust to the inclusion of neurons that were individually poor decoders. By contrast, average rate codes based on convergence performed poorly; effective decoding using average rates was only possible when the responses of individual neurons were segregated, as in classical population decoding models using labeled lines. The relative effectiveness of dynamic rate coding in auditory cortex was explained by shared modulation phase preferences among cortical neurons, despite heterogeneity in rate-based modulation frequency tuning. Our results indicate significant population-based synchrony in primary auditory cortex and suggest that robust population coding of the sound envelope information present in animal vocalizations and speech can be reliably achieved even with indiscriminate pooling of cortical responses. These findings highlight the importance of firing rate dynamics in population-based sensory coding.

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Shapes and Level Tolerances of Frequency Tuning Curves in Primary Auditory Cortex: Quantitative Measures and Population Codes

Journal of Neurophysiology ◽

10.1152/jn.2000.84.2.1012 ◽

2000 ◽

Vol 84 (2) ◽

pp. 1012-1025 ◽

Cited By ~ 57

Author(s):

Mitchell L. Sutter

Keyword(s):

High Frequency ◽

Frequency Tuning ◽

Low Frequency ◽

Primary Auditory Cortex ◽

Inverse Slope ◽

Lower Tail ◽

Tuning Curves ◽

Population Codes ◽

Auditory Systems ◽

A1 Neurons

The shape and level tolerance of the excitatory frequency/intensity tuning curves (eFTCs) of 160 cat primary auditory cortical (A1) neurons were investigated. Overall, A1 cells were characterized by tremendous variety in eFTC shapes and symmetries; eFTCs were U-shaped (∼20%), V-shaped (∼20%), lower-tail-upper-sharp (∼15%), upper-tail-lower-sharp (<2%), slant-lower (∼10%), slant-upper (<3%), multipeaked (∼10%), and circumscribed (∼20%). Quantitative analysis suggests that eFTC are best thought of as forming a continuum of shapes, rather than falling into discrete categories. A1 eFTCs tended to be more level tolerant than eFTCs from earlier stations in the ascending auditory system as inferred from other studies. While individual peaks of multipeaked eFTCs were similar to single peaked eFTCs, the overall eFTC of multipeaked neurons (spanning the range of all peaks) tended to have high-frequency tails. Measurements of shape and symmetry indicate that A1 eFTCs, on average, tended to have greater area on the low-frequency side of characteristic frequency (CF) than on the high-frequency side. A1 cells showed a relationship between CF and the inverse slope of low-frequency edges of eFTCs, but not for high-frequency edges. These data demonstrate that frequency tuning, particularly along the eFTC low-frequency border, sharpens along the lemniscal pathway to A1. The results are consistent with studies in mustached bats ( Suga 1997 ) and support the idea that spectral decomposition along the ascending lemniscal pathway up to A1 is a general organizing principle of mammalian auditory systems. Altogether, these data suggest that A1 neurons' eFTCs are shaped by complex patterns of inhibition and excitation accumulating along the auditory pathways, implying that central rather than peripheral filtering properties are responsible for certain psychophysical phenomena.

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Processing of Modulated Sounds in the Zebra Finch Auditory Midbrain: Responses to Noise, Frequency Sweeps, and Sinusoidal Amplitude Modulations

Journal of Neurophysiology ◽

10.1152/jn.01064.2004 ◽

2005 ◽

Vol 94 (2) ◽

pp. 1143-1157 ◽

Cited By ~ 33

Author(s):

Sarah M. N. Woolley ◽

John H. Casseday

Keyword(s):

Zebra Finch ◽

Auditory Processing ◽

Frequency Tuning ◽

Spike Rate ◽

Auditory Midbrain ◽

Complex Sounds ◽

Tuning Curves ◽

Wide Range ◽

Band Limited ◽

Frequency Sweeps

The avian auditory midbrain nucleus, the mesencephalicus lateralis, dorsalis (MLd), is the first auditory processing stage in which multiple parallel inputs converge, and it provides the input to the auditory thalamus. We studied the responses of single MLd neurons to four types of modulated sounds: 1) white noise; 2) band-limited noise; 3) frequency modulated (FM) sweeps, and 4) sinusoidally amplitude-modulated tones (SAM) in adult male zebra finches. Responses were compared with the responses of the same neurons to pure tones in terms of temporal response patterns, thresholds, characteristic frequencies, frequency tuning bandwidths, tuning sharpness, and spike rate/intensity relationships. Most neurons responded well to noise. More than one-half of the neurons responded selectively to particular portions of the noise, suggesting that, unlike forebrain neurons, many MLd neurons can encode specific acoustic components of highly modulated sounds such as noise. Selectivity for FM sweep direction was found in only 13% of cells that responded to sweeps. Those cells also showed asymmetric tuning curves, suggesting that asymmetric inhibition plays a role in FM directional selectivity. Responses to SAM showed that MLd neurons code temporal modulation rates using both spike rate and synchronization. Nearly all cells showed low-pass or band-pass filtering properties for SAM. Best modulation frequencies matched the temporal modulations in zebra finch song. Results suggest that auditory midbrain neurons are well suited for encoding a wide range of complex sounds with a high degree of temporal accuracy rather than selectively responding to only some sounds.

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Responses of Neurons in Primary Auditory Cortex (A1) to Pure Tones in the Halothane-Anesthetized Cat

Journal of Neurophysiology ◽

10.1152/jn.00822.2005 ◽

2006 ◽

Vol 95 (6) ◽

pp. 3756-3769 ◽

Cited By ~ 57

Author(s):

Dina Moshitch ◽

Liora Las ◽

Nachum Ulanovsky ◽

Omer Bar-Yosef ◽

Israel Nelken

Keyword(s):

Auditory Cortex ◽

Frequency Tuning ◽

Sensory Information ◽

Primary Auditory Cortex ◽

Response Patterns ◽

Neural Responses ◽

Standard Classification ◽

A1 Neurons ◽

Pure Tones ◽

Stimulus Offset

The responses of primary auditory cortex (A1) neurons to pure tones in anesthetized animals are usually described as having mostly narrow, unimodal frequency tuning and phasic responses. Thus A1 neurons are believed not to carry much information about pure tones beyond sound onset. In awake cats, however, tuning may be wider and responses may have substantially longer duration. Here we analyze frequency-response areas (FRAs) and temporal-response patterns of 1,828 units in A1 of halothane-anesthetized cats. Tuning was generally wide: the total bandwidth at 40 dB above threshold was 4 octaves on average. FRA shapes were highly variable and many were diffuse, not fitting into standard classification schemes. Analyzing the temporal patterns of the largest responses of each unit revealed that only 9% of the units had pure onset responses. About 40% of the units had sustained responses throughout stimulus duration (115 ms) and 13% of the units had significant and informative responses lasting 300 ms and more after stimulus offset. We conclude that under halothane anesthesia, neural responses show many of the characteristics of awake responses. Furthermore, A1 units maintain sensory information in their activity not only throughout sound presentation but also for hundreds of milliseconds after stimulus offset, thus possibly playing a role in sensory memory.

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Distinct Manifestations of Cooperative, Multidimensional Stimulus Representations in Different Auditory Forebrain Stations

Cerebral Cortex ◽

10.1093/cercor/bhz299 ◽

2020 ◽

Vol 30 (5) ◽

pp. 3130-3147

Author(s):

Jonathan Y Shih ◽

Kexin Yuan ◽

Craig A Atencio ◽

Christoph E Schreiner

Keyword(s):

Receptive Fields ◽

Medial Geniculate Body ◽

Primary Auditory Cortex ◽

Linear Filter ◽

Auditory Information ◽

Stimulus Response ◽

Spectral Integration ◽

Medial Geniculate ◽

A1 Neurons ◽

Stimulus Features

Abstract Classic spectrotemporal receptive fields (STRFs) for auditory neurons are usually expressed as a single linear filter representing a single encoded stimulus feature. Multifilter STRF models represent the stimulus-response relationship of primary auditory cortex (A1) neurons more accurately because they can capture multiple stimulus features. To determine whether multifilter processing is unique to A1, we compared the utility of single-filter versus multifilter STRF models in the medial geniculate body (MGB), anterior auditory field (AAF), and A1 of ketamine-anesthetized cats. We estimated STRFs using both spike-triggered average (STA) and maximally informative dimension (MID) methods. Comparison of basic filter properties of first maximally informative dimension (MID1) and second maximally informative dimension (MID2) in the 3 stations revealed broader spectral integration of MID2s in MGBv and A1 as opposed to AAF. MID2 peak latency was substantially longer than for STAs and MID1s in all 3 stations. The 2-filter MID model captured more information and yielded better predictions in many neurons from all 3 areas but disproportionately more so in AAF and A1 compared with MGBv. Significantly, information-enhancing cooperation between the 2 MIDs was largely restricted to A1 neurons. This demonstrates significant differences in how these 3 forebrain stations process auditory information, as expressed in effective and synergistic multifilter processing.

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Local homogeneity of tonotopic organization in the primary auditory cortex of marmosets

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1816653116 ◽

2019 ◽

Vol 116 (8) ◽

pp. 3239-3244 ◽

Cited By ~ 8

Author(s):

Huan-huan Zeng ◽

Jun-feng Huang ◽

Ming Chen ◽

Yun-qing Wen ◽

Zhi-ming Shen ◽

...

Keyword(s):

Auditory Cortex ◽

Large Scale ◽

Frequency Tuning ◽

Primary Auditory Cortex ◽

Primate Species ◽

Tonotopic Organization ◽

Brain Structure And Function ◽

A1 Neurons ◽

Cortical Regions

Marmoset has emerged as a useful nonhuman primate species for studying brain structure and function. Previous studies on the mouse primary auditory cortex (A1) showed that neurons with preferential frequency-tuning responses are mixed within local cortical regions, despite a large-scale tonotopic organization. Here we found that frequency-tuning properties of marmoset A1 neurons are highly uniform within local cortical regions. We first defined the tonotopic map of A1 using intrinsic optical imaging and then used in vivo two-photon calcium imaging of large neuronal populations to examine the tonotopic preference at the single-cell level. We found that tuning preferences of layer 2/3 neurons were highly homogeneous over hundreds of micrometers in both horizontal and vertical directions. Thus, marmoset A1 neurons are distributed in a tonotopic manner at both macro- and microscopic levels. Such organization is likely to be important for the organization of auditory circuits in the primate brain.

Download Full-text