scholarly journals Adaptive efficient coding of correlated acoustic properties

2019 ◽  
Author(s):  
Kai Lu ◽  
Wanyi Liu ◽  
Kelsey Dutta ◽  
Jonathan B. Fritz ◽  
Shihab A. Shamma

AbstractNatural sounds such as vocalizations often have co-varying acoustic attributes where one acoustic feature can be predicted from another, resulting in redundancy in neural coding. It has been proposed that sensory systems are able to detect such covariation and adapt to reduce redundancy, leading to more efficient neural coding. Results of recent psychoacoustic studies suggest that, following passive exposure to sounds in which temporal and spectral attributes covaried in a correlated fashion, the auditory system adapts to efficiently encode the two co-varying dimensions as a single dimension, at the cost of lost sensitivity to the orthogonal dimension. Here we explore the neural basis of this psychophysical phenomenon by recording single-unit responses from primary auditory cortex (A1) in awake ferrets exposed passively to stimuli with two correlated attributes in the temporal and spectral domain similar to that utilized in the psychoacoustic experiments. We found that: (1) the signal-to-noise (SNR) ratio of spike rate coding of cortical responses driven by sounds with correlated attributes was reduced along the orthogonal dimension; while the SNR ratio remained intact along the exposure dimension; (2) Mutual information of spike temporal coding increased only along the exposure dimension; (3) correlation between neurons tuned to the two covarying attributes decreased after exposure; (4) these exposure effects still occurred if sounds were correlated along two acoustic dimensions, but varied randomly along a third dimension. These neurophysiological results are consistent with the Efficient Learning Hypothesis and may deepen our understanding of how the auditory system represents acoustic regularities and covariance.SignificanceIn the Efficient Coding (EC) hypothesis, proposed by Barlow in 1961, the neural code in sensory systems efficiently encodes natural stimuli by minimizing the number of spikes to transmit a sensory signal. Results of recent psychoacoustic studies are consistent with the EC hypothesis, showing that following passive exposure to stimuli with correlated attributes, the auditory system adapts so as to more efficiently encode the two co-varying dimensions as a single dimension. In the current neurophysiological experiments, using a similar stimulus design and experimental paradigm to the psychoacoustic studies of Stilp and colleagues (2010, 2011, 2012, 2016), we recorded responses from single neurons in the auditory cortex of the awake ferret, showing adaptive efficient neural coding of correlated acoustic properties.

2019 ◽  
Author(s):  
Xiangbin Teng ◽  
David Poeppel

AbstractNatural sounds have broadband modulation spectra and contain acoustic dynamics ranging from tens to hundreds of milliseconds. How does the human auditory system encode acoustic information over wide-ranging timescales to achieve sound recognition? Previous work (Teng et al., 2017) demonstrated a temporal coding preference in the auditory system for the theta (4 – 7 Hz) and gamma (30 – 45 Hz) ranges, but it remains unclear how acoustic dynamics between these two ranges is encoded. Here we generated artificial sounds with temporal structures over timescales from ~200 ms to ~30 ms and investigated temporal coding on different timescales in the human auditory cortex. Participants discriminated sounds with temporal structures at different timescales while undergoing magnetoencephalography (MEG) recording. The data show robust neural entrainment in the theta and the gamma bands, but not in the alpha and beta bands. Classification analyses as well as stimulus reconstruction reveal that the acoustic information of all timescales can be differentiated through the theta and gamma bands, but the acoustic dynamics in the theta and gamma ranges are preferentially encoded. We replicate earlier findings of multi-time scale processing and further demonstrate that the theta and gamma bands show generality of temporal coding across all timescales with comparable capacity. The results support the hypothesis that the human auditory cortex primarily encodes auditory information employing neural processes within two discrete temporal regimes.SignificanceNatural sounds contain rich acoustic dynamics over wide-ranging timescales, but perceptually relevant regularities often occupy specific temporal ranges. For instance, speech carries phonemic information on a shorter timescale than syllabic information at ~ 200 ms. How does the brain efficiently ‘sample’ continuous acoustic input to perceive temporally structured sounds? We presented sounds with temporal structures at different timescales and measured cortical entrainment using magnetoencephalography. We found, unexpectedly, that the human auditory system preserves high temporal coding precision on two non-overlapping timescales, the slower (theta) and faster (gamma) bands, to track acoustic dynamics over all timescales. The results suggest that the acoustic environment which we experience as seamless and continuous is segregated by discontinuous neural processing, or ‘sampled.’


2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Sidney R. Lehky ◽  
Keiji Tanaka ◽  
Anne B. Sereno

AbstractWhen measuring sparseness in neural populations as an indicator of efficient coding, an implicit assumption is that each stimulus activates a different random set of neurons. In other words, population responses to different stimuli are, on average, uncorrelated. Here we examine neurophysiological data from four lobes of macaque monkey cortex, including V1, V2, MT, anterior inferotemporal cortex, lateral intraparietal cortex, the frontal eye fields, and perirhinal cortex, to determine how correlated population responses are. We call the mean correlation the pseudosparseness index, because high pseudosparseness can mimic statistical properties of sparseness without being authentically sparse. In every data set we find high levels of pseudosparseness ranging from 0.59–0.98, substantially greater than the value of 0.00 for authentic sparseness. This was true for synthetic and natural stimuli, as well as for single-electrode and multielectrode data. A model indicates that a key variable producing high pseudosparseness is the standard deviation of spontaneous activity across the population. Consistently high values of pseudosparseness in the data demand reconsideration of the sparse coding literature as well as consideration of the degree to which authentic sparseness provides a useful framework for understanding neural coding in the cortex.


2019 ◽  
Vol 2019 ◽  
pp. 1-9 ◽  
Author(s):  
Zheng-De Du ◽  
Wei Wei ◽  
Shukui Yu ◽  
Qing-Ling Song ◽  
Ke Liu ◽  
...  

Clinical data has confirmed that auditory impairment may be a secondary symptom of type 2 diabetes mellitus (T2DM). However, mechanisms underlying pathologic changes that occur in the auditory system, especially in the central auditory system (CAS), remain poorly understood. In this study, Zucker diabetic fatty (ZDF) rats were used as a T2DM rat model to observe ultrastructural alterations in the auditory cortex and investigate possible mechanisms underlying CAS damage in T2DM. The auditory brainstem response (ABR) of ZDF rats was found to be markedly elevated in low (8 kHz) and high (32 kHz) frequencies. Protein expression of NADPH oxidase 2 (NOX2) and its matching subunits P22phox, P47phox, and P67phox was increased in the auditory cortex of ZDF rats. Expression of 8-hydroxy-2-deoxyguanosine (8-OHdG), a marker of DNA oxidative damage, was also increased in the neuronal mitochondria of the auditory cortex of ZDF rats. Additionally, decreases in the mitochondrial total antioxidant capabilities (T-AOC), adenosine triphosphate (ATP) production, and mitochondrial membrane potential (MMP) were detected in the auditory cortex of ZDF rats, suggesting mitochondrial dysfunction. Transmission electron microscopy results indicated that ultrastructural damage had occurred to neurovascular units and mitochondria in the auditory cortex of ZDF rats. Furthermore, cytochrome c (Cyt c) translocation from mitochondria to cytoplasm and caspase 3-dependent apoptosis were also detected in the auditory cortex of ZDF rats. Consequently, the study demonstrated that T2DM may cause morphological damage to the CAS and that NOX2-associated mitochondrial oxidative damage and apoptosis may be partly responsible for this insult.


2019 ◽  
Author(s):  
Jérémy Giroud ◽  
Agnès Trébuchon ◽  
Daniele Schön ◽  
Patrick Marquis ◽  
Catherine Liegeois-Chauvel ◽  
...  

AbstractSpeech perception is mediated by both left and right auditory cortices, but with differential sensitivity to specific acoustic information contained in the speech signal. A detailed description of this functional asymmetry is missing, and the underlying models are widely debated. We analyzed cortical responses from 96 epilepsy patients with electrode implantation in left or right primary, secondary, and/or association auditory cortex. We presented short acoustic transients to reveal the stereotyped spectro-spatial oscillatory response profile of the auditory cortical hierarchy. We show remarkably similar bimodal spectral response profiles in left and right primary and secondary regions, with preferred processing modes in the theta (∼4-8 Hz) and low gamma (∼25-50 Hz) ranges. These results highlight that the human auditory system employs a two-timescale processing mode. Beyond these first cortical levels of auditory processing, a hemispheric asymmetry emerged, with delta and beta band (∼3/15 Hz) responsivity prevailing in the right hemisphere and theta and gamma band (∼6/40 Hz) activity in the left. These intracranial data provide a more fine-grained and nuanced characterization of cortical auditory processing in the two hemispheres, shedding light on the neural dynamics that potentially shape auditory and speech processing at different levels of the cortical hierarchy.Author summarySpeech processing is now known to be distributed across the two hemispheres, but the origin and function of lateralization continues to be vigorously debated. The asymmetric sampling in time (AST) hypothesis predicts that (1) the auditory system employs a two-timescales processing mode, (2) present in both hemispheres but with a different ratio of fast and slow timescales, (3) that emerges outside of primary cortical regions. Capitalizing on intracranial data from 96 epileptic patients we sensitively validated each of these predictions and provide a precise estimate of the processing timescales. In particular, we reveal that asymmetric sampling in associative areas is subtended by distinct two-timescales processing modes. Overall, our results shed light on the neurofunctional architecture of cortical auditory processing.


2019 ◽  
Author(s):  
Jesyin Lai ◽  
Stephen V. David

ABSTRACTChronic vagus nerve stimulation (VNS) can facilitate learning of sensory and motor behaviors. VNS is believed to trigger release of neuromodulators, including norepinephrine and acetylcholine, which can mediate cortical plasticity associated with learning. Most previous work has studied effects of VNS over many days, and less is known about how acute VNS influences neural coding and behavior over the shorter term. To explore this question, we measured effects of VNS on learning of an auditory discrimination over 1-2 days. Ferrets implanted with cuff electrodes on the vagus nerve were trained by classical conditioning on a tone frequency-reward association. One tone was associated with reward while another tone, was not. The frequencies and reward associations of the tones were changed every two days, requiring learning of a new relationship. When the tones (both rewarded and non-rewarded) were paired with VNS, rates of learning increased on the first day following a change in reward association. To examine VNS effects on auditory coding, we recorded single- and multi-unit neural activity in primary auditory cortex (A1) of passively listening animals following brief periods of VNS (20 trials/session) paired with tones. Because afferent VNS induces changes in pupil size associated with fluctuations in neuromodulation, we also measured pupil during recordings. After pairing VNS with a neuron’s best-frequency (BF) tone, responses in a subpopulation of neurons were reduced. Pairing with an off-BF tone or performing VNS during the inter-trial interval had no effect on responses. We separated the change in A1 activity into two components, one that could be predicted by fluctuations in pupil and one that persisted after VNS and was not accounted for by pupil. The BF-specific reduction in neural responses remained, even after regressing out changes that could be explained by pupil. In addition, the size of VNS-mediated changes in pupil predicted the magnitude of persistent changes in the neural response. This interaction suggests that changes in neuromodulation associated with arousal gate the long-term effects of VNS on neural activity. Taken together, these results support a role for VNS in auditory learning and help establish VNS as a tool to facilitate neural plasticity.


1980 ◽  
Vol 86 (1) ◽  
pp. 135-151
Author(s):  
K. G. HILL ◽  
D. B. LEWIS ◽  
M. E. HUTCHINGS ◽  
R. B. COLES

The auditory tympana in the quail, Coturnix coturnix japonica (L.) are internally coupled by an interaural air space. Unilaterally applied sound causing vibration of the ipsilateral tympanum is conducted through the interauralcavity to the inside surface of the contralateral tympanum. In a free soundfield at frequencies up to 3150 Hz, sound pressure at the external surface of the tympanum contralateral to the source is within about 3 dB of the pressure exterior to the ipsilateral tympanum. Sound pressures developed at the inner surfaces of the tympana are of similar amplitude to the external pressures at several frequencies in the range 800–6300 Hz. In addition, pressure ateach side of the tympanum ipsilateral to the source are generally out of phase, whereas pressures at each side of the contralateral tympanum are relatively close to the same phase. From measurements of amplitude and phase of the interacting pressures at the tympanum, the calculated driving pressure at the ipsilateral tympanum exceeds that at the contralateral tympanum by 10–20 dB over a range of frequencies. The auditory tympana in quail have considerable inherent directionality, therefore, due to their function aspressure-gradient receivers. Anatomical analogies with anurans and reptiles indicate that they derive directional hearing from the same acoustic mechanism that operates in the quail.


2019 ◽  
Vol 39 (44) ◽  
pp. 8664-8678 ◽  
Author(s):  
Kai Lu ◽  
Wanyi Liu ◽  
Kelsey Dutta ◽  
Peng Zan ◽  
Jonathan B. Fritz ◽  
...  

1998 ◽  
Vol 80 (5) ◽  
pp. 2743-2764 ◽  
Author(s):  
Jos J. Eggermont

Eggermont, Jos J. Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. J. Neurophysiol. 80: 2743–2764, 1998. This study investigates the degree of similarity of three different auditory cortical areas with respect to the coding of periodic stimuli. Simultaneous single- and multiunit recordings in response to periodic stimuli were made from primary auditory cortex (AI), anterior auditory field (AAF), and secondary auditory cortex (AII) in the cat to addresses the following questions: is there, within each cortical area, a difference in the temporal coding of periodic click trains, amplitude-modulated (AM) noise bursts, and AM tone bursts? Is there a difference in this coding between the three cortical fields? Is the coding based on the temporal modulation transfer function (tMTF) and on the all-order interspike-interval (ISI) histogram the same? Is the perceptual distinction between rhythm and roughness for AM stimuli related to a temporal versus spatial representation of AM frequency in auditory cortex? Are interarea differences in temporal response properties related to differences in frequency tuning? The results showed that: 1) AM stimuli produce much higher best modulation frequencies (BMFs) and limiting rates than periodic click trains. 2) For periodic click trains and AM noise, the BMFs and limiting rates were not significantly different for the three areas. However, for AM tones the BMF and limiting rates were about a factor 2 lower in AAF compared with the other areas. 3) The representation of stimulus periodicity in ISIs resulted in significantly lower mean BMFs and limiting rates compared with those estimated from the tMTFs. The difference was relatively small for periodic click trains but quite large for both AM stimuli, especially in AI and AII. 4) Modulation frequencies <20 Hz were represented in the ISIs, suggesting that rhythm is coded in auditory cortex in temporal fashion. 5) In general only a modest interdependence of spectral- and temporal-response properties in AI and AII was found. The BMFs were correlated positively with characteristic frequency in AAF. The limiting rate was positively correlated with the frequency-tuning curve bandwidth in AI and AII but not in AAF. Only in AAF was a correlation between BMF and minimum latency was found. Thus whereas differences were found in the frequency-tuning curve bandwidth and minimum response latencies among the three areas, the coding of periodic stimuli in these areas was fairly similar with the exception of the very poor representation of AM tones in AII. This suggests a strong parallel processing organization in auditory cortex.


2019 ◽  
Vol 30 (4) ◽  
pp. 2586-2599 ◽  
Author(s):  
Stitipragyan Bhumika ◽  
Mari Nakamura ◽  
Patricia Valerio ◽  
Magdalena Solyga ◽  
Henrik Lindén ◽  
...  

Abstract Neuronal circuits are shaped by experience during time windows of increased plasticity in postnatal development. In the auditory system, the critical period for the simplest sounds—pure frequency tones—is well defined. Critical periods for more complex sounds remain to be elucidated. We used in vivo electrophysiological recordings in the mouse auditory cortex to demonstrate that passive exposure to frequency modulated sweeps (FMS) from postnatal day 31 to 38 leads to long-term changes in the temporal representation of sweep directions. Immunohistochemical analysis revealed a decreased percentage of layer 4 parvalbumin-positive (PV+) cells during this critical period, paralleled with a transient increase in responses to FMS, but not to pure tones. Preventing the PV+ cell decrease with continuous white noise exposure delayed the critical period onset, suggesting a reduction in inhibition as a mechanism for this plasticity. Our findings shed new light on the dependence of plastic windows on stimulus complexity that persistently sculpt the functional organization of the auditory cortex.


2015 ◽  
Vol 282 (1811) ◽  
pp. 20151203 ◽  
Author(s):  
Gregory S. Berns ◽  
Peter F. Cook ◽  
Sean Foxley ◽  
Saad Jbabdi ◽  
Karla L. Miller ◽  
...  

The brains of odontocetes (toothed whales) look grossly different from their terrestrial relatives. Because of their adaptation to the aquatic environment and their reliance on echolocation, the odontocetes' auditory system is both unique and crucial to their survival. Yet, scant data exist about the functional organization of the cetacean auditory system. A predominant hypothesis is that the primary auditory cortex lies in the suprasylvian gyrus along the vertex of the hemispheres, with this position induced by expansion of ‘associative′ regions in lateral and caudal directions. However, the precise location of the auditory cortex and its connections are still unknown. Here, we used a novel diffusion tensor imaging (DTI) sequence in archival post-mortem brains of a common dolphin ( Delphinus delphis ) and a pantropical dolphin ( Stenella attenuata ) to map their sensory and motor systems. Using thalamic parcellation based on traditionally defined regions for the primary visual (V1) and auditory cortex (A1), we found distinct regions of the thalamus connected to V1 and A1. But in addition to suprasylvian-A1, we report here, for the first time, the auditory cortex also exists in the temporal lobe, in a region near cetacean-A2 and possibly analogous to the primary auditory cortex in related terrestrial mammals (Artiodactyla). Using probabilistic tract tracing, we found a direct pathway from the inferior colliculus to the medial geniculate nucleus to the temporal lobe near the sylvian fissure. Our results demonstrate the feasibility of post-mortem DTI in archival specimens to answer basic questions in comparative neurobiology in a way that has not previously been possible and shows a link between the cetacean auditory system and those of terrestrial mammals. Given that fresh cetacean specimens are relatively rare, the ability to measure connectivity in archival specimens opens up a plethora of possibilities for investigating neuroanatomy in cetaceans and other species.


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