scholarly journals The specificity of stimulus-specific adaptation in human auditory cortex increases with repeated exposure to the adapting stimulus

2013 ◽  
Vol 110 (12) ◽  
pp. 2679-2688 ◽  
Author(s):  
Paul M. Briley ◽  
Katrin Krumbholz

The neural response to a sensory stimulus tends to be more strongly reduced when the stimulus is preceded by the same, rather than a different, stimulus. This stimulus-specific adaptation (SSA) is ubiquitous across the senses. In hearing, SSA has been suggested to play a role in change detection as indexed by the mismatch negativity. This study sought to test whether SSA, measured in human auditory cortex, is caused by neural fatigue (reduction in neural responsiveness) or by sharpening of neural tuning to the adapting stimulus. For that, we measured event-related cortical potentials to pairs of pure tones with varying frequency separation and stimulus onset asynchrony (SOA). This enabled us to examine the relationship between the degree of specificity of adaptation as a function of frequency separation and the rate of decay of adaptation with increasing SOA. Using simulations of tonotopic neuron populations, we demonstrate that the fatigue model predicts independence of adaptation specificity and decay rate, whereas the sharpening model predicts interdependence. The data showed independence and thus supported the fatigue model. In a second experiment, we measured adaptation specificity after multiple presentations of the adapting stimulus. The multiple adapters produced more adaptation overall, but the effect was more specific to the adapting frequency. Within the context of the fatigue model, the observed increase in adaptation specificity could be explained by assuming a 2.5-fold increase in neural frequency selectivity. We discuss possible bottom-up and top-down mechanisms of this effect.

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.


1999 ◽  
Vol 82 (3) ◽  
pp. 1542-1559 ◽  
Author(s):  
Michael Brosch ◽  
Andreas Schulz ◽  
Henning Scheich

It is well established that the tone-evoked response of neurons in auditory cortex can be attenuated if another tone is presented several hundred milliseconds before. The present study explores in detail a complementary phenomenon in which the tone-evoked response is enhanced by a preceding tone. Action potentials from multiunit groups and single units were recorded from primary and caudomedial auditory cortical fields in lightly anesthetized macaque monkeys. Stimuli were two suprathreshold tones of 100-ms duration, presented in succession. The frequency of the first tone and the stimulus onset asynchrony (SOA) between the two tones were varied systematically, whereas the second tone was fixed. Compared with presenting the second tone in isolation, the response to the second tone was enhanced significantly when it was preceded by the first tone. This was observed in 87 of 130 multiunit groups and in 29 of 69 single units with no obvious difference between different auditory fields. Response enhancement occurred for a wide range of SOA (110–329 ms) and for a wide range of frequencies of the first tone. Most of the first tones that enhanced the response to the second tone evoked responses themselves. The stimulus, which on average produced maximal enhancement, was a pair with a SOA of 120 ms and with a frequency separation of about one octave. The frequency/SOA combinations that induced response enhancement were mostly different from the ones that induced response attenuation. Results suggest that response enhancement, in addition to response attenuation, provides a basic neural mechanism involved in the cortical processing of the temporal structure of sounds.


2015 ◽  
Vol 113 (7) ◽  
pp. 2582-2591 ◽  
Author(s):  
Björn Herrmann ◽  
Molly J. Henry ◽  
Elisa Kim Fromboluti ◽  
J. Devin McAuley ◽  
Jonas Obleser

Stimulus-specific adaptation is the phenomenon whereby neural response magnitude decreases with repeated stimulation. Inconsistencies between recent nonhuman animal recordings and computational modeling suggest dynamic influences on stimulus-specific adaptation. The present human electroencephalography (EEG) study investigates the potential role of statistical context in dynamically modulating stimulus-specific adaptation by examining the auditory cortex-generated N1 and P2 components. As in previous studies of stimulus-specific adaptation, listeners were presented with oddball sequences in which the presentation of a repeated tone was infrequently interrupted by rare spectral changes taking on three different magnitudes. Critically, the statistical context varied with respect to the probability of small versus large spectral changes within oddball sequences (half of the time a small change was most probable; in the other half a large change was most probable). We observed larger N1 and P2 amplitudes (i.e., release from adaptation) for all spectral changes in the small-change compared with the large-change statistical context. The increase in response magnitude also held for responses to tones presented with high probability, indicating that statistical adaptation can overrule stimulus probability per se in its influence on neural responses. Computational modeling showed that the degree of coadaptation in auditory cortex changed depending on the statistical context, which in turn affected stimulus-specific adaptation. Thus the present data demonstrate that stimulus-specific adaptation in human auditory cortex critically depends on statistical context. Finally, the present results challenge the implicit assumption of stationarity of neural response magnitudes that governs the practice of isolating established deviant-detection responses such as the mismatch negativity.


2022 ◽  
Author(s):  
Julien Besle ◽  
Rosa-Maria Sánchez-Panchuelo ◽  
Susan Francis ◽  
Katrin Krumbholz

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.


2013 ◽  
Vol 110 (4) ◽  
pp. 973-983 ◽  
Author(s):  
Cornelis P. Lanting ◽  
Paul M. Briley ◽  
Christian J. Sumner ◽  
Katrin Krumbholz

This study investigates the temporal properties of adaptation in the late auditory-evoked potentials in humans. The results are used to make inferences about the mechanisms of adaptation in human auditory cortex. The first experiment measured adaptation by single adapters as a combined function of the adapter duration and the stimulus onset asynchrony (SOA) and interstimulus interval (ISI) between the adapter and the adapted sound (“probe”). The results showed recovery from adaptation with increasing ISI, as would be expected, but buildup of adaptation with increasing adapter duration and thus SOA. This suggests that adaptation in auditory cortex is caused by the ongoing, rather than the onset, response to the adapter. Quantitative modeling indicated that the rate of buildup of adaptation is almost an order of magnitude faster than the recovery rate of adaptation. The recovery rate suggests that cortical adaptation is caused by synaptic depression and slow afterhyperpolarization. The P2 was more strongly affected by adaptation than the N1, suggesting that the two deflections originate from different cortical generators. In the second experiment, the single adapters were replaced by trains of two or four identical adapters. The results indicated that adaptation decays faster after repeated presentation of the adapter. This increase in the recovery rate of adaptation might contribute to the elicitation of the auditory mismatch negativity response. It may be caused by top-down feedback or by local processes such as the buildup of residual Ca2+ within presynaptic neurons.


2003 ◽  
Vol 18 (2) ◽  
pp. 432-440 ◽  
Author(s):  
Takako Fujioka ◽  
Bernhard Ross ◽  
Hidehiko Okamoto ◽  
Yasuyuki Takeshima ◽  
Ryusuke Kakigi ◽  
...  

2013 ◽  
Vol 110 (8) ◽  
pp. 1892-1902 ◽  
Author(s):  
Ben D. Richardson ◽  
Kenneth E. Hancock ◽  
Donald M. Caspary

Novel stimulus detection by single neurons in the auditory system, known as stimulus-specific adaptation (SSA), appears to function as a real-time filtering/gating mechanism in processing acoustic information. Particular stimulus paradigms allowing for quantification of a neuron's ability to detect novel or deviant stimuli have been used to examine SSA in the inferior colliculus, medial geniculate body (MGB), and auditory cortex of anesthetized rodents. However, the study of SSA in awake animals is limited to auditory cortex. The present study used individually advanceable tetrodes to record single-unit responses from auditory thalamus (MGB) of awake young adult and aged Fischer Brown Norway (FBN) rats to 1) examine the presence of SSA in the MGB of awake rats and 2) determine whether SSA is altered by aging in MGB. MGB single units in awake FBN rats displayed SSA in response to two stimulus paradigms: the oddball paradigm and a random blocked/interleaved presentation of a set of frequencies. SSA levels were modestly, but nonsignificantly, increased in the nonlemniscal regions of the MGB and at lower stimulus intensities, where 27 of 57 (47%) young adult MGB units displayed SSA. The present findings provide the initial description of SSA in the MGB of awake rats and support SSA as being qualitatively independent of arousal level or anesthetized state. Finally, contrary to previous studies in auditory cortex of anesthetized rats, MGB units in aged rats showed SSA levels indistinguishable from SSA levels in young adult rats, suggesting that SSA in MGB was not impacted by aging in an awake preparation.


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