Combining ultra-high-field fMRI adaptation and computational modelling to estimate neuronal frequency selectivity in human auditory cortex

Frequency selectivity is a ubiquitous property of auditory neurons. Measuring it in human auditory cortex may be crucial for understanding common auditory deficits, but current non-invasive neuroimaging techniques can only measure the aggregate response of large populations of cells, thereby overestimating tuning width. Here we attempted to estimate neuronal frequency tuning in human auditory cortex using a combination of fMRI-adaptation paradigm at 7T and computational modelling. We measured the BOLD response in the auditory cortex of eleven participants to a high frequency (3.8 kHz) probe presented alone or preceded by adaptors at different frequencies (0.5 to 3.8 kHz). From these data, we derived both the response tuning curves (the BOLD response to adaptors alone as a function of adaptor frequency) and adaptation tuning curves (the degree of response suppression to the probe as a function of adaptor frequency, assumed to reflect neuronal tuning) in primary and secondary auditory cortical areas, delineated in each participant. Results suggested the existence of both frequency-independent and frequency-specific adaptation components, with the latter being more frequency-tuned than response tuning curves. Using a computational model of neuronal adaptation and BOLD non-linearity in topographically-organized cortex, we demonstrate both that the frequency-specific adaptation component overestimates the underlying neuronal frequency tuning and that frequency-specific and frequency-independent adaptation component cannot easily be disentangled from the adaptation tuning curve. By fitting our model directly to the response and adaptation tuning curves, we derive a range of plausible values for neuronal frequency tuning. Our results suggest that fMRI adaptation is suitable for measuring neuronal frequency tuning properties in human auditory cortex, provided population effects and the non-linearity of BOLD response are taken into account.

Download Full-text

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

Download Full-text

Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustached bat

Journal of Neurophysiology ◽

10.1152/jn.1985.53.4.1109 ◽

1985 ◽

Vol 53 (4) ◽

pp. 1109-1145 ◽

Cited By ~ 70

Author(s):

N. Suga ◽

K. Tsuzuki

Keyword(s):

Auditory Cortex ◽

Frequency Analysis ◽

Frequency Tuning ◽

Neural Basis ◽

Single Tone ◽

Tuning Curves ◽

Mustached Bat ◽

Essential Components ◽

High Stimulus ◽

Pulse Echo

For echolocation the mustached bat, Pteronotus parnellii, emits complex orientation sounds (pulses), each consisting of four harmonics with long constant-frequency components (CF1-4) followed by short frequency-modulated components (FM1-4). The CF signals are best suited for target detection and measurement of target velocity. The CF/CF area of the auditory cortex of this species contains neurons sensitive to pulse-echo pairs. These CF/CF combination-sensitive neurons extract velocity information from Doppler-shifted echoes. In this study we electrophysiologically investigated the frequency tuning of CF/CF neurons for excitation, facilitation, and inhibition. CF1/CF2 and CF1/CF3 combination-sensitive neurons responded poorly to individual signal elements in pulse-echo pairs but showed strong facilitation of responses to pulse-echo pairs. The essential components in the pairs were CF1 of the pulse and CF2 or CF3 of the echo. In 68% of CF/CF neurons, the frequency-tuning curves for facilitation were extremely sharp for CF2 or CF3 and were "level-tolerant" so that the bandwidths of the tuning curves were less than 5.0% of best frequencies even at high stimulus levels. Facilitative tuning curves for CF1 were level tolerant only in 6% of the neurons studied. CF/CF neurons were specialized for fine analysis of the frequency relationship between two CF sounds regardless of sound pressure levels. Some CF/CF neurons responded to single-tone stimuli. Frequency-tuning curves for excitation (responses to single-tone stimuli) were extremely sharp and level tolerant for CF2 or CF3 in 59% of CF1/CF2 neurons and 70% of CF1/CF3 neurons. Tuning to CF1 was level tolerant in only 9% of these neurons. Sharp level-tolerant tuning may be the neural basis for small difference limens in frequency at high stimulus levels. Sharp level-tolerant tuning curves were sandwiched between broad inhibitory areas. Best frequencies for inhibition were slightly higher or lower than the best frequencies for facilitation and excitation. We thus conclude that sharp level-tolerant tuning curves are produced by inhibition. The extent to which neural sharpening occurred differed among groups of neurons tuned to different frequencies. The more important the frequency analysis of a particular component in biosonar signals, the more pronounced the neural sharpening. This was in addition to the peripheral specialization for fine frequency analysis of that component. The difference in bandwidth or quality factor between the excitatory tuning curves of peripheral neurons and the facilitative and excitatory tuning curves of CF/CF neurons was larger at higher stimulus levels.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

Evidence of sharp frequency tuning in the human auditory cortex

Hearing Research ◽

10.1016/0378-5955(94)90057-4 ◽

1994 ◽

Vol 75 (1-2) ◽

pp. 67-74 ◽

Cited By ~ 34

Author(s):

Mikko Sams ◽

Riitta Salmelin

Keyword(s):

Auditory Cortex ◽

Frequency Tuning ◽

Human Auditory Cortex

Download Full-text

S4-3. Population-level frequency tuning in human auditory cortex

Clinical Neurophysiology ◽

10.1016/j.clinph.2018.02.039 ◽

2018 ◽

Vol 129 (5) ◽

pp. e24

Author(s):

Hidehiko Okamoto

Keyword(s):

Auditory Cortex ◽

Frequency Tuning ◽

Population Level ◽

Human Auditory Cortex

Download Full-text

Noradrenergic Induction of Selective Plasticity in the Frequency Tuning of Auditory Cortex Neurons

Journal of Neurophysiology ◽

10.1152/jn.00079.2004 ◽

2004 ◽

Vol 92 (3) ◽

pp. 1445-1463 ◽

Cited By ~ 64

Author(s):

Yves Manunta ◽

Jean-Marc Edeline

Keyword(s):

Auditory Cortex ◽

Cortical Neurons ◽

Cortical Plasticity ◽

Frequency Tuning ◽

Tone Frequency ◽

Cortical Cells ◽

Tuning Curves ◽

Alpha Receptors ◽

Frequency Changes ◽

Selective Effects

Neuromodulators have long been viewed as permissive factors in experience-induced cortical plasticity, both during development and in adulthood. Experiments performed over the last two decades have reported the potency of acetylcholine to promote changes in functional properties of cortical cells in the auditory, visual, and somatosensory modality. In contrast, very few attempts were made with the monoaminergic systems. The present study evaluates how repeated presentation of brief pulses of noradrenaline (NA) concomitant with presentation of a particular tone frequency changes the frequency tuning curves of auditory cortex neurons determined at 20 dB above threshold. After 100 trials of NA-tone pairing, 28% of the cells (19/67) exhibited selective tuning modifications for the frequency paired with NA. All the selective effects were obtained when the paired frequency was within 1/4 of an octave from the initial best frequency. For these cells, selective decreases were prominent (15/19 cases), and these effects lasted ≥15 min after pairing. No selective effects were observed under various control conditions: tone alone ( n = 10 cells), NA alone ( n = 11 cells), pairing with ascorbic acid ( n = 6 cells), or with GABA ( n = 20 cells). Selective effects were observed when the NA-tone pairing was performed in the presence of propranolol (4/10 cells) but not when it was performed in the presence phentolamine (0/13 cells), suggesting that the effects were mediated by alpha receptors. These results indicate that brief increases in noradrenaline concentration can trigger selective modifications in the tuning curves of cortical neurons that, in most of the cases, go in opposite direction compared with those usually reported with acetylcholine.

Download Full-text

Fine frequency tuning in monkey auditory cortex and thalamus

Journal of Neurophysiology ◽

10.1152/jn.00559.2010 ◽

2011 ◽

Vol 106 (2) ◽

pp. 849-859 ◽

Cited By ~ 28

Author(s):

Edward L. Bartlett ◽

Srivatsun Sadagopan ◽

Xiaoqin Wang

Keyword(s):

Auditory Cortex ◽

Auditory Nerve ◽

Animal Studies ◽

De Novo ◽

Frequency Tuning ◽

Primary Auditory Cortex ◽

Auditory Pathway ◽

Nerve Fibers ◽

Frequency Resolution ◽

Human Auditory Cortex

The frequency resolution of neurons throughout the ascending auditory pathway is important for understanding how sounds are processed. In many animal studies, the frequency tuning widths are about 1/5th octave wide in auditory nerve fibers and much wider in auditory cortex neurons. Psychophysical studies show that humans are capable of discriminating far finer frequency differences. A recent study suggested that this is perhaps attributable to fine frequency tuning of neurons in human auditory cortex (Bitterman Y, Mukamel R, Malach R, Fried I, Nelken I. Nature 451: 197–201, 2008). We investigated whether such fine frequency tuning was restricted to human auditory cortex by examining the frequency tuning width in the awake common marmoset monkey. We show that 27% of neurons in the primary auditory cortex exhibit frequency tuning that is finer than the typical frequency tuning of the auditory nerve and substantially finer than previously reported cortical data obtained from anesthetized animals. Fine frequency tuning is also present in 76% of neurons of the auditory thalamus in awake marmosets. Frequency tuning was narrower during the sustained response compared to the onset response in auditory cortex neurons but not in thalamic neurons, suggesting that thalamocortical or intracortical dynamics shape time-dependent frequency tuning in cortex. These findings challenge the notion that the fine frequency tuning of auditory cortex is unique to human auditory cortex and that it is a de novo cortical property, suggesting that the broader tuning observed in previous animal studies may arise from the use of anesthesia during physiological recordings or from species differences.

Download Full-text

Development of Cochlear Amplification, Frequency Tuning, and Two-Tone Suppression in the Mouse

Journal of Neurophysiology ◽

10.1152/jn.00983.2007 ◽

2008 ◽

Vol 99 (1) ◽

pp. 344-355 ◽

Cited By ~ 15

Author(s):

Lei Song ◽

JoAnn McGee ◽

Edward J. Walsh

Keyword(s):

Time Course ◽

Frequency Tuning ◽

Tuning Curve ◽

Frequency Region ◽

Frequency Selectivity ◽

Tuning Curves ◽

Equivalent Time ◽

Cochlear Amplification ◽

Narrow Frequency Band ◽

Dynamic Operating

It is generally believed that the micromechanics of active cochlear transduction mature later than passive elements among altricial mammals. One consequence of this developmental order is the loss of transduction linearity, because an active, physiologically vulnerable process is superimposed on the passive elements of transduction. A triad of sensory advantage is gained as a consequence of acquiring active mechanics; sensitivity and frequency selectivity (frequency tuning) are enhanced and dynamic operating range increases. Evidence supporting this view is provided in this study by tracking the development of tuning curves in BALB/c mice. Active transduction, commonly known as cochlear amplification, enhances sensitivity in a narrow frequency band associated with the “tip” of the tuning curve. Passive aspects of transduction were assessed by considering the thresholds of responses elicited from the tuning curve “tail,” a frequency region that lies below the active transduction zone. The magnitude of cochlear amplification was considered by computing tuning curve tip-to-tail ratios, a commonly used index of active transduction gain. Tuning curve tip thresholds, frequency selectivity and tip-to-tail ratios, all indices of the functional status of active biomechanics, matured between 2 and 7 days after tail thresholds achieved adultlike values. Additionally, two-tone suppression, another product of active cochlear transduction, was first observed in association with the earliest appearance of tuning curve tips and matured along an equivalent time course. These findings support a traditional view of development in which the maturation of passive transduction precedes the maturation of active mechanics in the most sensitive region of the mouse cochlea.

Download Full-text