Detection of Natural Complex Sounds by Cells in the Primary Auditory Cortex of the Cat

1975 ◽  
Vol 93 (3) ◽  
pp. 318-335 ◽  
Author(s):  
Anssi R. A. Sovijärvi
2011 ◽  
Vol 106 (2) ◽  
pp. 1016-1027 ◽  
Author(s):  
Martin Pienkowski ◽  
Jos J. Eggermont

The distribution of neuronal characteristic frequencies over the area of primary auditory cortex (AI) roughly reflects the tonotopic organization of the cochlea. However, because the area of AI activated by any given sound frequency increases erratically with sound level, it has generally been proposed that frequency is represented in AI not with a rate-place code but with some more complex, distributed code. Here, on the basis of both spike and local field potential (LFP) recordings in the anesthetized cat, we show that the tonotopic representation in AI is much more level tolerant when mapped with spectrotemporally dense tone pip ensembles rather than with individually presented tone pips. That is, we show that the tuning properties of individual unit and LFP responses are less variable with sound level under dense compared with sparse stimulation, and that the spatial frequency resolution achieved by the AI neural population at moderate stimulus levels (65 dB SPL) is better with densely than with sparsely presented sounds. This implies that nonlinear processing in the central auditory system can compensate (in part) for the level-dependent coding of sound frequency in the cochlea, and suggests that there may be a functional role for the cortical tonotopic map in the representation of complex sounds.


2009 ◽  
Vol 102 (6) ◽  
pp. 3329-3339 ◽  
Author(s):  
Nima Mesgarani ◽  
Stephen V. David ◽  
Jonathan B. Fritz ◽  
Shihab A. Shamma

Population responses of cortical neurons encode considerable details about sensory stimuli, and the encoded information is likely to change with stimulus context and behavioral conditions. The details of encoding are difficult to discern across large sets of single neuron data because of the complexity of naturally occurring stimulus features and cortical receptive fields. To overcome this problem, we used the method of stimulus reconstruction to study how complex sounds are encoded in primary auditory cortex (AI). This method uses a linear spectro-temporal model to map neural population responses to an estimate of the stimulus spectrogram, thereby enabling a direct comparison between the original stimulus and its reconstruction. By assessing the fidelity of such reconstructions from responses to modulated noise stimuli, we estimated the range over which AI neurons can faithfully encode spectro-temporal features. For stimuli containing statistical regularities (typical of those found in complex natural sounds), we found that knowledge of these regularities substantially improves reconstruction accuracy over reconstructions that do not take advantage of this prior knowledge. Finally, contrasting stimulus reconstructions under different behavioral states showed a novel view of the rapid changes in spectro-temporal response properties induced by attentional and motivational state.


Author(s):  
Israel Nelken

Understanding the principles by which sensory systems represent natural stimuli is one of the holy grails of neuroscience. In the auditory system, the study of the coding of natural sounds has a particular prominence. Indeed, the relationships between neural responses to simple stimuli (usually pure tone bursts)—often used to characterize auditory neurons—and complex sounds (in particular natural sounds) may be complex. Many different classes of natural sounds have been used to study the auditory system. Sound families that researchers have used to good effect in this endeavor include human speech, species-specific vocalizations, an “acoustic biotope” selected in one way or another, and sets of artificial sounds that mimic important features of natural sounds. Peripheral and brainstem representations of natural sounds are relatively well understood. The properties of the peripheral auditory system play a dominant role, and further processing occurs mostly within the frequency channels determined by these properties. At the level of the inferior colliculus, the highest brainstem station, representational complexity increases substantially due to the convergence of multiple processing streams. Undoubtedly, the most explored part of the auditory system, in term of responses to natural sounds, is the primary auditory cortex. In spite of over 50 years of research, there is still no commonly accepted view of the nature of the population code for natural sounds in the auditory cortex. Neurons in the auditory cortex are believed by some to be primarily linear spectro-temporal filters, by others to respond to conjunctions of important sound features, or even to encode perceptual concepts such as “auditory objects.” Whatever the exact mechanism is, many studies consistently report a substantial increase in the variability of the response patterns of cortical neurons to natural sounds. The generation of such variation may be the main contribution of auditory cortex to the coding of natural sounds.


2018 ◽  
Vol 29 (7) ◽  
pp. 2998-3009 ◽  
Author(s):  
Haifu Li ◽  
Feixue Liang ◽  
Wen Zhong ◽  
Linqing Yan ◽  
Lucas Mesik ◽  
...  

Abstract Spatial size tuning in the visual cortex has been considered as an important neuronal functional property for sensory perception. However, an analogous mechanism in the auditory system has remained controversial. In the present study, cell-attached recordings in the primary auditory cortex (A1) of awake mice revealed that excitatory neurons can be categorized into three types according to their bandwidth tuning profiles in response to band-passed noise (BPN) stimuli: nonmonotonic (NM), flat, and monotonic, with the latter two considered as non-tuned for bandwidth. The prevalence of bandwidth-tuned (i.e., NM) neurons increases significantly from layer 4 to layer 2/3. With sequential cell-attached and whole-cell voltage-clamp recordings from the same neurons, we found that the bandwidth preference of excitatory neurons is largely determined by the excitatory synaptic input they receive, and that the bandwidth selectivity is further enhanced by flatly tuned inhibition observed in all cells. The latter can be attributed at least partially to the flat tuning of parvalbumin inhibitory neurons. The tuning of auditory cortical neurons for bandwidth of BPN may contribute to the processing of complex sounds.


2012 ◽  
Vol 24 (9) ◽  
pp. 1896-1907 ◽  
Author(s):  
I-Hui Hsieh ◽  
Paul Fillmore ◽  
Feng Rong ◽  
Gregory Hickok ◽  
Kourosh Saberi

Frequency modulation (FM) is an acoustic feature of nearly all complex sounds. Directional FM sweeps are especially pervasive in speech, music, animal vocalizations, and other natural sounds. Although the existence of FM-selective cells in the auditory cortex of animals has been documented, evidence in humans remains equivocal. Here we used multivariate pattern analysis to identify cortical selectivity for direction of a multitone FM sweep. This method distinguishes one pattern of neural activity from another within the same ROI, even when overall level of activity is similar, allowing for direct identification of FM-specialized networks. Standard contrast analysis showed that despite robust activity in auditory cortex, no clusters of activity were associated with up versus down sweeps. Multivariate pattern analysis classification, however, identified two brain regions as selective for FM direction, the right primary auditory cortex on the supratemporal plane and the left anterior region of the superior temporal gyrus. These findings are the first to directly demonstrate existence of FM direction selectivity in the human auditory cortex.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Destinee A. Aponte ◽  
Gregory Handy ◽  
Amber M. Kline ◽  
Hiroaki Tsukano ◽  
Brent Doiron ◽  
...  

AbstractDetecting the direction of frequency modulation (FM) is essential for vocal communication in both animals and humans. Direction-selective firing of neurons in the primary auditory cortex (A1) has been classically attributed to temporal offsets between feedforward excitatory and inhibitory inputs. However, it remains unclear how cortical recurrent circuitry contributes to this computation. Here, we used two-photon calcium imaging and whole-cell recordings in awake mice to demonstrate that direction selectivity is not caused by temporal offsets between synaptic currents, but by an asymmetry in total synaptic charge between preferred and non-preferred directions. Inactivation of cortical somatostatin-expressing interneurons (SOM cells) reduced direction selectivity, revealing its cortical contribution. Our theoretical models showed that charge asymmetry arises due to broad spatial topography of SOM cell-mediated inhibition which regulates signal amplification in strongly recurrent circuitry. Together, our findings reveal a major contribution of recurrent network dynamics in shaping cortical tuning to behaviorally relevant complex sounds.


Author(s):  
Joshua D Downer ◽  
James Bigelow ◽  
Melissa Runfeldt ◽  
Brian James Malone

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.


1996 ◽  
Vol 76 (5) ◽  
pp. 3503-3523 ◽  
Author(s):  
N. Kowalski ◽  
D. A. Depireux ◽  
S. A. Shamma

1. Auditory stimuli referred to as moving ripples are used to characterize the responses of both single and multiple units in the ferret primary auditory cortex. Moving ripples are broadband complex sounds with a sinusoidal spectral profile that drift along the logarithmic frequency axis at a constant velocity. 2. Neuronal responses to moving ripples are locked to the phase of the ripple, i.e., they exhibit the same periodicity as that of the moving ripple profile. Neural responses are characterized as a function of ripple velocity (temporal property) and ripple frequency (spectral property). Transfer functions describing the response to these temporal and spectral modulations are constructed. Temporal transfer functions are inverse Fourier transformed to obtain impulse response functions that reflect the cell's temporal characteristics. Ripple transfer functions are inverse Fourier transformed to obtain the response field, a measure analogous to the cell's response area. These operations assume linearity in the cell's response to moving ripples. 3. Transfer functions and other response functions are shown to be fairly independent on the overall level or depth of modulation of the ripple stimuli. Only downward moving ripples were used in this study. 4. The temporal and ripple transfer functions are found to be separable, in that their shapes remain unchanged for different test parameters. Thus ripple transfer functions and response fields remain statistically similar in shape (to within an overall scale factor) regardless of the ripple velocity or whether stationary or moving ripples are used in the measurement. The same stability in shape holds for the temporal transfer functions and the impulse response functions measured with different ripple frequencies. Separability implies that the combined spectrotemporal transfer function of a cell can be written as the product of a purely ripple and a purely temporal transfer functions, and thus that the neuron can be computationally modeled as processing spectral and temporal information in two separate and successive stages. 5. The ripple parameters that characterize cortical cells are distributed somewhat evenly, with the characteristic ripple frequencies ranging from 0.2 to > 2 cycles/octave and the characteristic angular frequency typically ranging from 2 to 20 Hz. 6. Many responses exhibit periodicities in the spectral envelope of the stimulus. These periodicities are of two types. Slow rebounds, not found in the spectral envelope, and with a period of approximately 150 ms, appear with various strengths in approximately 30% of the cells. Fast regular firings with interspike intervals of approximately 10 ms are much less common and appear to correspond to interactions between the component tones that make up a ripple.


2020 ◽  
Author(s):  
Joshua D. Downer ◽  
Jessica R. Verhein ◽  
Brittany C. Rapone ◽  
Kevin N. O’Connor ◽  
Mitchell L. Sutter

ABSTRACTTextbook descriptions of primary sensory cortex (PSC) revolve around single neurons’ representation of low-dimensional sensory features, such as visual object orientation in V1, location of somatic touch in S1, and sound frequency in A1. Typically, studies of PSC measure neurons’ responses along few (1 or 2) stimulus and/or behavioral dimensions. However, real-world stimuli usually vary along many feature dimensions and behavioral demands change constantly. In order to illuminate how A1 supports flexible perception in rich acoustic environments, we recorded from A1 neurons while rhesus macaques performed a feature-selective attention task. We presented sounds that varied along spectral and temporal feature dimensions (carrier bandwidth and temporal envelope, respectively). Within a block, subjects attended to one feature of the sound in a selective change detection task. We find that single neurons tend to be high-dimensional, in that they exhibit substantial mixed selectivity for both sound features, as well as task context. Contrary to common findings in many previous experiments, attention does not enhance the single-neuron representation of attended features in our data. However, a population-level analysis reveals that ensembles of neurons exhibit enhanced encoding of attended sound features, and this population code tracks subjects’ performance. Importantly, surrogate neural populations with intact single-neuron tuning but shuffled higher-order correlations among neurons failed to yield attention-related effects observed in the intact data. These results suggest that an emergent population code not measurable at the single-neuron level might constitute the functional unit of sensory representation in PSC.SIGNIFICANCE STATEMENTThe ability to adapt to a dynamic sensory environment promotes a range of important natural behaviors. We recorded from single neurons in monkey primary auditory cortex while subjects attended to either the spectral or temporal features of complex sounds. Surprisingly, we find no average increase in responsiveness to, or encoding of, the attended feature across single neurons. However, when we pool the activity of the sampled neurons via targeted dimensionality reduction, we find enhanced population-level representation of the attended feature and suppression of the distractor feature. This dissociation of the effects of attention at the level of single neurons vs. the population highlights the synergistic nature of cortical sound encoding and enriches our understanding of sensory cortical function.


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