Feedback optimizes neural coding and perception of natural stimuli

Growing evidence suggests that sensory neurons achieve optimal encoding by matching their tuning properties to the natural stimulus statistics. However, the underlying mechanisms remain unclear. Here we demonstrate that feedback pathways from higher brain areas mediate optimized encoding of naturalistic stimuli via temporal whitening in the weakly electric fish Apteronotus leptorhynchus. While one source of direct feedback uniformly enhances neural responses, a separate source of indirect feedback selectively attenuates responses to low frequencies, thus creating a high-pass neural tuning curve that opposes the decaying spectral power of natural stimuli. Additionally, we recorded from two populations of higher brain neurons responsible for the direct and indirect descending inputs. While one population displayed broadband tuning, the other displayed high-pass tuning and thus performed temporal whitening. Hence, our results demonstrate a novel function for descending input in optimizing neural responses to sensory input through temporal whitening that is likely to be conserved across systems and species.

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Descending pathways mediate adaptive optimized coding of natural stimuli in weakly electric fish

Science Advances ◽

10.1126/sciadv.aax2211 ◽

2019 ◽

Vol 5 (10) ◽

pp. eaax2211 ◽

Cited By ~ 5

Author(s):

Chengjie G. Huang ◽

Michael G. Metzen ◽

Maurice J. Chacron

Keyword(s):

Environmental Changes ◽

Behavioral Responses ◽

Sensory Systems ◽

Weakly Electric Fish ◽

Descending Pathways ◽

Natural Stimuli ◽

Central Neurons ◽

Power Spectral ◽

Underlying Mechanisms ◽

Weakly Electric

Biological systems must be flexible to environmental changes to survive. This is exemplified by the fact that sensory systems continuously adapt to changes in the environment to optimize coding and behavioral responses. However, the nature of the underlying mechanisms remains poorly understood in general. Here, we investigated the mechanisms mediating adaptive optimized coding of naturalistic stimuli with varying statistics depending on the animal’s velocity during movement. We found that central neurons adapted their responses to stimuli with different power spectral densities such as to optimally encode them, thereby ensuring that behavioral responses are, in turn, better matched to the new stimulus statistics. Sensory adaptation further required descending inputs from the forebrain as well as the raphe nuclei. Our findings thus reveal a previously unknown functional role for descending pathways in mediating adaptive optimized coding of natural stimuli that is likely generally applicable across sensory systems and species.

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On the Importance of Static Nonlinearity in Estimating Spatiotemporal Neural Filters With Natural Stimuli

Journal of Neurophysiology ◽

10.1152/jn.01397.2007 ◽

2008 ◽

Vol 99 (5) ◽

pp. 2496-2509 ◽

Cited By ~ 28

Author(s):

Tatyana O. Sharpee ◽

Kenneth D. Miller ◽

Michael P. Stryker

Keyword(s):

Linear Model ◽

Neural Coding ◽

Predictive Power ◽

Gaussian White Noise ◽

Linear Filter ◽

Neural Responses ◽

Natural Stimulus ◽

Model Studies ◽

Natural Stimuli ◽

Static Nonlinearity

Understanding neural responses with natural stimuli has increasingly become an essential part of characterizing neural coding. Neural responses are commonly characterized by a linear–nonlinear (LN) model, in which the output of a linear filter applied to the stimulus is transformed by a static nonlinearity to determine neural response. To estimate the linear filter in the LN model, studies of responses to natural stimuli commonly use methods that are unbiased only for a linear model (in which there is no static nonlinearity): spike-triggered averages with correction for stimulus power spectrum, with or without regularization. Although these methods work well for artificial stimuli, such as Gaussian white noise, we show here that they estimate neural filters of LN models from responses to natural stimuli much more poorly. We studied simple cells in cat primary visual cortex. We demonstrate that the filters computed by directly taking the nonlinearity into account have better predictive power and depend less on the stimulus than those computed under the linear model. With noise stimuli, filters computed using the linear and LN models were similar, as predicted theoretically. With natural stimuli, filters of the two models can differ profoundly. Noise and natural stimulus filters differed significantly in spatial properties, but these differences were exaggerated when filters were computed using the linear rather than the LN model. Although regularization of filters computed under the linear model improved their predictive power, it also led to systematic distortions of their spatial frequency profiles, especially at low spatial and temporal frequencies.

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Mechanisms of Venoarteriolar Reflex in Type 2 Diabetes with or without Peripheral Neuropathy

Biology ◽

10.3390/biology10040333 ◽

2021 ◽

Vol 10 (4) ◽

pp. 333

Author(s):

Cécile Reynès ◽

Antonia Perez-Martin ◽

Houda Ennaifer ◽

Henrique Silva ◽

Yannick Knapp ◽

...

Keyword(s):

Type 2 Diabetes ◽

Peripheral Neuropathy ◽

Spectral Power ◽

Blood Perfusion ◽

Doppler Flowmetry ◽

Relative Contribution ◽

Total Spectral Power ◽

Underlying Mechanisms ◽

Endothelial Nitric Oxide

The aim of this study is to investigate the underlying mechanisms of the venoarteriolar reflex (VAR) in type 2 diabetes mellitus (T2DM), with and without peripheral neuropathy. Laser Doppler flowmetry (LDF) recordings were performed on the medial malleus and dorsal foot skin, before and during leg dependency in healthy controls, in persons with obesity, in those with T2DM, in those with T2DM and subclinical neuropathy, and in those with T2DM and confirmed neuropathy. LDF recordings were analyzed with the wavelet transform to evaluate the mechanisms controlling the flowmotion (i.e., endothelial nitric oxide-independent and -dependent, neurogenic, myogenic, respiratory and cardiac mechanisms). Skin blood perfusion decreased throughout leg dependency at both sites. The decrease was blunted in persons with confirmed neuropathy compared to those with T2DM alone and the controls. During leg dependency, total spectral power increased in all groups compared to rest. The relative contribution of the endothelial bands increased and of the myogenic band decreased, without differences between groups. Neurogenic contribution decreased in controls, in persons with obesity and in those with T2DM, whereas it increased in subclinical- and confirmed neuropathy. In conclusion, this study provides evidence that confirmed diabetic neuropathy alters the VAR through the neurogenic response to leg dependency.

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Effect of Age in Auditory Go/No-Go Tasks: A Magnetoencephalographic Study

Brain Sciences ◽

10.3390/brainsci10100667 ◽

2020 ◽

Vol 10 (10) ◽

pp. 667

Author(s):

Mei-Yin Lin ◽

Chia-Hsiung Cheng

Keyword(s):

Older Adults ◽

Response Inhibition ◽

Cortical Activation ◽

Middle Temporal Gyrus ◽

Neural Responses ◽

Source Imaging ◽

Age Related ◽

Aging Populations ◽

Neural Underpinnings ◽

Underlying Mechanisms

Response inhibition is frequently examined using visual go/no-go tasks. Recently, the auditory go/no-go paradigm has been also applied to several clinical and aging populations. However, age-related changes in the neural underpinnings of auditory go/no-go tasks are yet to be elucidated. We used magnetoencephalography combined with distributed source imaging methods to examine age-associated changes in neural responses to auditory no-go stimuli. Additionally, we compared the performance of high- and low-performing older adults to explore differences in cortical activation. Behavioral performance in terms of response inhibition was similar in younger and older adult groups. Relative to the younger adults, the older adults exhibited reduced cortical activation in the superior and middle temporal gyrus. However, we did not find any significant differences in cortical activation between the high- and low-performing older adults. Our results therefore support the hypothesis that inhibition is reduced during aging. The variation in cognitive performance among older adults confirms the need for further study on the underlying mechanisms of inhibition.

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A sciaenid swim bladder with long skinny fingers produces sound with an unusual frequency spectrum

Scientific Reports ◽

10.1038/s41598-020-75663-9 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Hin-Kiu Mok ◽

Shih-Chia Wu ◽

Soranuth Sirisuary ◽

Michael L. Fine

Keyword(s):

Frequency Spectrum ◽

Fundamental Frequency ◽

Pulse Repetition Rate ◽

Sound Production ◽

Swim Bladder ◽

Low Frequencies ◽

Pass Filter ◽

Number Of Cycles ◽

Almost All ◽

High Pass

Abstract Swim bladders in sciaenid fishes function in hearing in some and sound production in almost all species. Sciaenid swim bladders vary from simple carrot-shaped to two-chambered to possessing various diverticula. Diverticula that terminate close to the ears improve hearing. Other unusual diverticula heading in a caudal direction have not been studied. The fresh-water Asian species Boesemania microlepis has an unusual swim bladder with a slightly restricted anterior region and 6 long-slender caudally-directed diverticula bilaterally. We hypothesized that these diverticula modify sound spectra. Evening advertisement calls consist of a series of multicycle tonal pulses, but the fundamental frequency and first several harmonics are missing or attenuated, and peak frequencies are high, varying between < 1–2 kHz. The fundamental frequency is reflected in the pulse repetition rate and in ripples on the frequency spectrum but not in the number of cycles within a pulse. We suggest that diverticula function as Helmholz absorbers turning the swim bladder into a high-pass filter responsible for the absence of low frequencies typically present in sciaenid calls. Further, we hypothesize that the multicycle pulses are driven by the stretched aponeuroses (flat tendons that connect the sonic muscles to the swim bladder) in this and other sciaenids.

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Modeling of Brain-Like Concept Coding with Adulthood Neurogenesis in the Dentate Gyrus

Computational Intelligence and Neuroscience ◽

10.1155/2019/2367075 ◽

2019 ◽

Vol 2019 ◽

pp. 1-13

Author(s):

Ye Wang ◽

Yan Gao ◽

Yaling Deng ◽

Lei Yang

Keyword(s):

Dentate Gyrus ◽

Language Processing ◽

Neural Coding ◽

Experimental Studies ◽

Vital Role ◽

Knowledge Map ◽

Neural Responses ◽

New Concepts ◽

Word Representation ◽

Repetition Time

Mammalian brains respond to new concepts via a type of neural coding termed “concept coding.” During concept coding, the dentate gyrus (DG) plays a vital role in pattern separation and pattern integration of concepts because it is a brain region with substantial neurogenesis in adult mammals. Although concept coding properties of the brain have been extensively studied by experimental work, modeling of the process to guide both further experimental studies and applications such as natural language processing is scarce. To model brain-like concept coding, we built a spiking neural network inspired by adulthood neurogenesis in the DG. Our model suggests that neurogenesis may facilitate integration of closely related concepts and separation of less relevant concepts. Such pattern agrees with the previous experimental observations in classification tasks and place cells in the hippocampus. Therefore, our simulation provides insight for future experimental studies on the neural coding difference between perception and cognition. By presenting 14 contexts each containing 4 concepts to the network, we found that neural responses of the DG changed dynamically as the context repetition time increased and were eventually consistent with the category organization of humans. Thus, our work provides a new framework of word representation for the construction of brain-like knowledge map.

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Postnatal Maturation of Primary Auditory Cortex in the Mustached Bat, Pteronotus parnellii

Journal of Neurophysiology ◽

10.1152/jn.00517.2009 ◽

2010 ◽

Vol 103 (5) ◽

pp. 2339-2354 ◽

Cited By ~ 8

Author(s):

M. Vater ◽

E. Foeller ◽

E. C. Mora ◽

F. Coro ◽

I. J. Russell ◽

...

Keyword(s):

Auditory Cortex ◽

Cortical Neurons ◽

Second Harmonic ◽

Tuning Curve ◽

Primary Auditory Cortex ◽

Constant Frequency ◽

Low Frequencies ◽

Postnatal Maturation ◽

Mustached Bat ◽

Pteronotus Parnellii

The primary auditory cortex (AI) of adult Pteronotus parnellii features a foveal representation of the second harmonic constant frequency (CF2) echolocation call component. In the corresponding Doppler-shifted constant frequency (DSCF) area, the 61 kHz range is over-represented for extraction of frequency-shift information in CF2 echoes. To assess to which degree AI postnatal maturation depends on active echolocation or/and reflects ongoing cochlear maturation, cortical neurons were recorded in juveniles up to postnatal day P29, before the bats are capable of active foraging. At P1-2, neurons in posterior AI are tuned sensitively to low frequencies (22–45 dB SPL, 28–35 kHz). Within the prospective DSCF area, neurons had insensitive responses (>60 dB SPL) to frequencies <40 kHz and lacked sensitive tuning curve tips. Up to P10, when bats do not yet actively echolocate, tonotopy is further developed and DSCF neurons respond to frequencies of 51–57 kHz with maximum tuning sharpness ( Q10dB) of 57. Between P11 and 20, the frequency representation in AI includes higher frequencies anterior and dorsal to the DSCF area. More multipeaked neurons (33%) are found than at older age. In the oldest group, DSCF neurons are tuned to frequencies close to 61 kHz with Q10dB values ≤212, and threshold sensitivity, tuning sharpness and cortical latencies are adult-like. The data show that basic aspects of cortical tonotopy are established before the bats actively echolocate. Maturation of tonotopy, increase of tuning sharpness, and upward shift in the characteristic frequency of DSCF neurons appear to strongly reflect cochlear maturation.

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The frequency of cortical microstimulation shapes artificial touch

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1916453117 ◽

2019 ◽

Vol 117 (2) ◽

pp. 1191-1200 ◽

Cited By ~ 9

Author(s):

Thierri Callier ◽

Nathan W. Brantly ◽

Attilio Caravelli ◽

Sliman J. Bensmaia

Keyword(s):

Neural Coding ◽

Sensory Quality ◽

Narrow Range ◽

Low Frequencies ◽

Pulse Trains ◽

Sensation Magnitude ◽

Frequency Judgments ◽

Wide Range ◽

Tactile Sensations

Intracortical microstimulation (ICMS) of the somatosensory cortex evokes vivid tactile sensations and can be used to convey sensory feedback from brain-controlled bionic hands. Changes in ICMS frequency lead to changes in the resulting sensation, but the discriminability of frequency has only been investigated over a narrow range of low frequencies. Furthermore, the sensory correlates of changes in ICMS frequency remain poorly understood. Specifically, it remains to be elucidated whether changes in frequency only modulate sensation magnitude—as do changes in amplitude—or whether they also modulate the quality of the sensation. To fill these gaps, we trained monkeys to discriminate the frequency of ICMS pulse trains over a wide range of frequencies (from 10 to 400 Hz). ICMS amplitude also varied across stimuli to dissociate sensation magnitude from ICMS frequency and ensure that animals could not make frequency judgments based on magnitude. We found that animals could consistently discriminate ICMS frequency up to ∼200 Hz but that the sensory correlates of frequency were highly electrode dependent: On some electrodes, changes in frequency were perceptually distinguishable from changes in amplitude—seemingly giving rise to a change in sensory quality; on others, they were not. We discuss the implications of our findings for neural coding and for brain-controlled bionic hands.

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Coding of Stimuli by Ampullary Afferents in Gnathonemus petersii

Journal of Neurophysiology ◽

10.1152/jn.00503.2009 ◽

2010 ◽

Vol 104 (4) ◽

pp. 1955-1968 ◽

Cited By ~ 15

Author(s):

J. Engelmann ◽

S. Gertz ◽

J. Goulet ◽

A. Schuh ◽

G. von der Emde

Keyword(s):

Frequency Tuning ◽

Low Frequency ◽

Weakly Electric Fish ◽

Behavioral Experiments ◽

Low Frequencies ◽

Similar Frequency ◽

Linear Feature ◽

Reconstruction Methods ◽

Electric Fishes ◽

Weakly Electric

Weakly electric fish use electroreception for both active and passive electrolocation and for electrocommunication. While both active and passive electrolocation systems are prominent in weakly electric Mormyriform fishes, knowledge of their passive electrolocation ability is still scarce. To better estimate the contribution of passive electric sensing to the orientation toward electric stimuli in weakly electric fishes, we investigated frequency tuning applying classical input-output characterization and stimulus reconstruction methods to reveal the encoding capabilities of ampullary receptor afferents. Ampullary receptor afferents were most sensitive (threshold: 40 μV/cm) at low frequencies (<10 Hz) and appear to be tuned to a mix of amplitude and slope of the input signals. The low-frequency tuning was corroborated by behavioral experiments, but behavioral thresholds were one order of magnitude higher. The integration of simultaneously recorded afferents of similar frequency-tuning resulted in strongly enhanced signal-to-noise ratios and increased mutual information rates but did not increase the range of frequencies detectable by the system. Theoretically the neuronal integration of input from receptors experiencing opposite polarities of a stimulus (left and right side of the fish) was shown to enhance encoding of such stimuli, including an increase of bandwidth. Covariance and coherence analysis showed that spiking of ampullary afferents is sufficiently explained by the spike-triggered average, i.e., receptors respond to a single linear feature of the stimulus. Our data support the notion of a division of labor of the active and passive electrosensory systems in weakly electric fishes based on frequency tuning. Future experiments will address the role of central convergence of ampullary input that we expect to lead to higher sensitivity and encoding power of the system.

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