scholarly journals Behavioral training restores temporal processing in auditory cortex of long-deaf cats

2011 ◽  
Vol 106 (5) ◽  
pp. 2423-2436 ◽  
Author(s):  
Maike Vollmer ◽  
Ralph E. Beitel
Keyword(s):  
Auditory Cortex ◽  
Temporal Processing ◽  
Cortical Neurons ◽  
Primary Auditory Cortex ◽  
Spike Timing ◽  
Cochlear Prosthesis ◽  
Behavioral Training ◽  
Stimulus Rate ◽  
Spiral Ganglion Cell

Temporal auditory processing is poor in prelingually hearing-impaired patients fitted with cochlear prostheses as adults. In an animal model of prelingual long-term deafness, we investigated the effects of behavioral training on temporal processing in the adult primary auditory cortex (AI). Neuronal responses to pulse trains of increasing frequencies were recorded in three groups of neonatally deafened cats that received a cochlear prosthesis after >3 yr of deafness: 1) acutely implanted animals that received no electric stimulation before study, 2) animals that received chronic-passive stimulation for several weeks to months before study, and 3) animals that received chronic-passive stimulation and additional behavioral training (signal detection). A fourth group of normal adult cats that was deafened acutely and implanted served as controls. The neuronal temporal response parameters of interest included the stimulus rate that evoked the maximum number of phase-locked spikes [best repetition rate (BRR)], the stimulus rate that produced 50% of the spike count at BRR (cutoff rate), the peak-response latency, and the first spike latency and timing-jitter. All long-deaf animals demonstrated a severe reduction in spiral ganglion cell density (mean, <6% of normal). Long-term deafness resulted in a significantly reduced temporal following capacity and spike-timing precision of cortical neurons in all parameters tested. Neurons in deaf animals that received only chronic-passive stimulation showed a gain in BRR but otherwise were similar to deaf cats that received no stimulation. In contrast, training with behaviorally relevant stimulation significantly enhanced all temporal processing parameters to normal levels with the exception of minimum latencies. These results demonstrate the high efficacy of learning-based remodeling of fundamental timing properties in cortical processing even in the adult, long-deaf auditory system, suggesting rehabilitative strategies for patients with long-term hearing loss.

scholarly journals Temporal coding of echo spectral shape in the bat auditory cortex

PLoS Biology ◽  
2020 ◽  
Vol 18 (11) ◽  
pp. e3000831 ◽  
Author(s):  
Silvio Macias ◽  
Kushal Bakshi ◽  
Francisco Garcia-Rosales ◽  
Julio C. Hechavarria ◽  
Michael Smotherman
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Computational Models ◽  
Shape Representation ◽  
Primary Auditory Cortex ◽  
Feature Space ◽  
Spike Timing ◽  
Temporal Coding ◽  
Spectral Interference ◽  
Network Activity

Echolocating bats rely upon spectral interference patterns in echoes to reconstruct fine details of a reflecting object’s shape. However, the acoustic modulations required to do this are extremely brief, raising questions about how their auditory cortex encodes and processes such rapid and fine spectrotemporal details. Here, we tested the hypothesis that biosonar target shape representation in the primary auditory cortex (A1) is more reliably encoded by changes in spike timing (latency) than spike rates and that latency is sufficiently precise to support a synchronization-based ensemble representation of this critical auditory object feature space. To test this, we measured how the spatiotemporal activation patterns of A1 changed when naturalistic spectral notches were inserted into echo mimic stimuli. Neurons tuned to notch frequencies were predicted to exhibit longer latencies and lower mean firing rates due to lower signal amplitudes at their preferred frequencies, and both were found to occur. Comparative analyses confirmed that significantly more information was recoverable from changes in spike times relative to concurrent changes in spike rates. With this data, we reconstructed spatiotemporal activation maps of A1 and estimated the level of emerging neuronal spike synchrony between cortical neurons tuned to different frequencies. The results support existing computational models, indicating that spectral interference patterns may be efficiently encoded by a cascading tonotopic sequence of neural synchronization patterns within an ensemble of network activity that relates to the physical features of the reflecting object surface.

scholarly journals Passive stimulation and behavioral training differentially transform temporal processing in the inferior colliculus and primary auditory cortex

2017 ◽  
Vol 117 (1) ◽  
pp. 47-64 ◽  
Author(s):  
Maike Vollmer ◽  
Ralph E. Beitel ◽  
Christoph E. Schreiner ◽  
Patricia A. Leake
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Temporal Processing ◽  
Electric Stimulation ◽  
Primary Auditory Cortex ◽  
Central Nucleus ◽  
Electrophysiological Recording ◽  
Response Patterns ◽  
Behavioral Training ◽  
Auditory Midbrain

In profoundly deaf cats, behavioral training with intracochlear electric stimulation (ICES) can improve temporal processing in the primary auditory cortex (AI). To investigate whether similar effects are manifest in the auditory midbrain, ICES was initiated in neonatally deafened cats either during development after short durations of deafness (8 wk of age) or in adulthood after long durations of deafness (≥3.5 yr). All of these animals received behaviorally meaningless, “passive” ICES. Some animals also received behavioral training with ICES. Two long-deaf cats received no ICES prior to acute electrophysiological recording. After several months of passive ICES and behavioral training, animals were anesthetized, and neuronal responses to pulse trains of increasing rates were recorded in the central (ICC) and external (ICX) nuclei of the inferior colliculus. Neuronal temporal response patterns (repetition rate coding, minimum latencies, response precision) were compared with results from recordings made in the AI of the same animals (Beitel RE, Vollmer M, Raggio MW, Schreiner CE. J Neurophysiol 106: 944–959, 2011; Vollmer M, Beitel RE. J Neurophysiol 106: 2423–2436, 2011). Passive ICES in long-deaf cats remediated severely degraded temporal processing in the ICC and had no effects in the ICX. In contrast to observations in the AI, behaviorally relevant ICES had no effects on temporal processing in the ICC or ICX, with the single exception of shorter latencies in the ICC in short-deaf cats. The results suggest that independent of deafness duration passive stimulation and behavioral training differentially transform temporal processing in auditory midbrain and cortex, and primary auditory cortex emerges as a pivotal site for behaviorally driven neuronal temporal plasticity in the deaf cat. NEW & NOTEWORTHY Behaviorally relevant vs. passive electric stimulation of the auditory nerve differentially affects neuronal temporal processing in the central nucleus of the inferior colliculus (ICC) and the primary auditory cortex (AI) in profoundly short-deaf and long-deaf cats. Temporal plasticity in the ICC depends on a critical amount of electric stimulation, independent of its behavioral relevance. In contrast, the AI emerges as a pivotal site for behaviorally driven neuronal temporal plasticity in the deaf auditory system.

scholarly journals Behavioral training enhances cortical temporal processing in neonatally deafened juvenile cats

2011 ◽  
Vol 106 (2) ◽  
pp. 944-959 ◽  
Author(s):  
Ralph E. Beitel ◽  
Maike Vollmer ◽  
Marcia W. Raggio ◽  
Christoph E. Schreiner
Keyword(s):  
Temporal Processing ◽  
Electric Stimulation ◽  
Primary Auditory Cortex ◽  
Cochlear Prosthesis ◽  
Behavioral Training ◽  
Stimulus Repetition ◽  
Electric Pulses ◽  
Temporal Cues ◽  
Auditory Experience ◽  
Cutoff Rate

Deaf humans implanted with a cochlear prosthesis depend largely on temporal cues for speech recognition because spectral information processing is severely impaired. Training with a cochlear prosthesis is typically required before speech perception shows improvement, suggesting that relevant experience modifies temporal processing in the central auditory system. We tested this hypothesis in neonatally deafened cats by comparing temporal processing in the primary auditory cortex (AI) of cats that received only chronic passive intracochlear electric stimulation (ICES) with cats that were also trained with ICES to detect temporally challenging trains of electric pulses. After months of chronic passive stimulation and several weeks of detection training in behaviorally trained cats, multineuronal AI responses evoked by temporally modulated ICES were recorded in anesthetized animals. The stimulus repetition rates that produced the maximum number of phase-locked spikes (best repetition rate) and 50% cutoff rate were significantly higher in behaviorally trained cats than the corresponding rates in cats that received only chronic passive ICES. Behavioral training restored neuronal temporal following ability to levels comparable with those recorded in naïve prior normal-hearing adult deafened animals. Importantly, best repetitition rates and cutoff rates were highest for neuronal clusters activated by the electrode configuration used in behavioral training. These results suggest that neuroplasticity in the AI is induced by behavioral training and perceptual learning in animals deprived of ordinary auditory experience during development and indicate that behavioral training can ameliorate or restore temporal processing in the AI of profoundly deaf animals.

Neural Responses in Primary Auditory Cortex Mimic Psychophysical, Across-Frequency-Channel, Gap-Detection Thresholds

2000 ◽  
Vol 84 (3) ◽  
pp. 1453-1463 ◽  
Author(s):  
Jos J. Eggermont
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Primary Auditory Cortex ◽  
Noise Burst ◽  
Gap Detection ◽  
Frequency Content ◽  
Neural Responses ◽  
Frequency Channel ◽  
Interval Representations ◽  
Onset Response

Responses of single- and multi-units in primary auditory cortex were recorded for gap-in-noise stimuli for different durations of the leading noise burst. Both firing rate and inter-spike interval representations were evaluated. The minimum detectable gap decreased in exponential fashion with the duration of the leading burst to reach an asymptote for durations of 100 ms. Despite the fact that leading and trailing noise bursts had the same frequency content, the dependence on leading burst duration was correlated with psychophysical estimates of across frequency channel (different frequency content of leading and trailing burst) gap thresholds in humans. The duration of the leading burst plus that of the gap was represented in the all-order inter-spike interval histograms for cortical neurons. The recovery functions for cortical neurons could be modeled on basis of fast synaptic depression and after-hyperpolarization produced by the onset response to the leading noise burst. This suggests that the minimum gap representation in the firing pattern of neurons in primary auditory cortex, and minimum gap detection in behavioral tasks is largely determined by properties intrinsic to those, or potentially subcortical, cells.

scholarly journals Serotonin Transporter Defect Disturbs Structure and Function of the Auditory Cortex in Mice

2021 ◽  
Vol 15 ◽  
Author(s):  
Wenlu Pan ◽  
Jing Pan ◽  
Yan Zhao ◽  
Hongzheng Zhang ◽  
Jie Tang
Keyword(s):  
Auditory Cortex ◽  
Serotonin Transporter ◽  
Cortical Neurons ◽  
Pyramidal Neurons ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Neuronal Morphology ◽  
Neuronal Connections ◽  
The Central Nervous System ◽  
And Function

Serotonin transporter (SERT) modulates the level of 5-HT and significantly affects the activity of serotonergic neurons in the central nervous system. The manipulation of SERT has lasting neurobiological and behavioral consequences, including developmental dysfunction, depression, and anxiety. Auditory disorders have been widely reported as the adverse events of these mental diseases. It is unclear how SERT impacts neuronal connections/interactions and what mechanism(s) may elicit the disruption of normal neural network functions in auditory cortex. In the present study, we report on the neuronal morphology and function of auditory cortex in SERT knockout (KO) mice. We show that the dendritic length of the fourth layer (L-IV) pyramidal neurons and the second-to-third layer (L-II/III) interneurons were reduced in the auditory cortex of the SERT KO mice. The number and density of dendritic spines of these neurons were significantly less than those of wild-type neurons. Also, the frequency-tonotopic organization of primary auditory cortex was disrupted in SERT KO mice. The auditory neurons of SERT KO mice exhibited border frequency tuning with high-intensity thresholds. These findings indicate that SERT plays a key role in development and functional maintenance of auditory cortical neurons. Auditory function should be examined when SERT is selected as a target in the treatment for psychiatric disorders.

scholarly journals Dopaminergic Neuromodulation of Spike Timing Dependent Plasticity in Mature Adult Rodent and Human Cortical Neurons

2021 ◽  
Vol 15 ◽  
Author(s):  
Emma Louise Louth ◽  
Rasmus Langelund Jørgensen ◽  
Anders Rosendal Korshoej ◽  
Jens Christian Hedemann Sørensen ◽  
Marco Capogna
Keyword(s):  
Learning And Memory ◽  
Cortical Neurons ◽  
Synaptic Depression ◽  
Spike Timing ◽  
Therapeutic Interventions ◽  
Spike Timing Dependent Plasticity ◽  
Mature Adult ◽  
Dependent Plasticity ◽  
Cortical Synapses

Synapses in the cerebral cortex constantly change and this dynamic property regulated by the action of neuromodulators such as dopamine (DA), is essential for reward learning and memory. DA modulates spike-timing-dependent plasticity (STDP), a cellular model of learning and memory, in juvenile rodent cortical neurons. However, it is unknown whether this neuromodulation also occurs at excitatory synapses of cortical neurons in mature adult mice or in humans. Cortical layer V pyramidal neurons were recorded with whole cell patch clamp electrophysiology and an extracellular stimulating electrode was used to induce STDP. DA was either bath-applied or optogenetically released in slices from mice. Classical STDP induction protocols triggered non-hebbian excitatory synaptic depression in the mouse or no plasticity at human cortical synapses. DA reverted long term synaptic depression to baseline in mouse via dopamine 2 type receptors or elicited long term synaptic potentiation in human cortical synapses. Furthermore, when DA was applied during an STDP protocol it depressed presynaptic inhibition in the mouse but not in the human cortex. Thus, DA modulates excitatory synaptic plasticity differently in human vs. mouse cortex. The data strengthens the importance of DA in gating cognition in humans, and may inform on therapeutic interventions to recover brain function from diseases.

Neuronal Responses in Cat Primary Auditory Cortex to Electrical Cochlear Stimulation. III. Activation Patterns in Short- and Long-Term Deafness

1999 ◽  
Vol 82 (6) ◽  
pp. 3506-3526 ◽  
Author(s):  
Marcia W. Raggio ◽  
Christoph E. Schreiner
Keyword(s):  
Auditory Cortex ◽  
Primary Auditory Cortex ◽  
Cortical Response ◽  
High Threshold ◽  
Short Term ◽  
Acute Group ◽  
Low Threshold ◽  
Response Thresholds ◽  
Adult Cat

The effects of auditory deprivation on the spatial distribution of cortical response thresholds to electrical stimulation of the adult cat cochlea were evaluated. Threshold distributions for single- and multiple-unit responses from the middle cortical layers were obtained on the ectosylvian gyrus in three groups of animals: adult, acutely implanted animals (“acute group”); adult animals, 2 wk after deafening and implantation (“short-term group”); adult, neonatally deafened animals (“long-term group”) implanted after 2–5 years of deafness. For all three groups, we observed similar patterns of circumscribed regions of low response thresholds in the region of primary auditory cortex (AI). A dorsal and a ventral region of low response thresholds were found separated by a narrow, anterior-posterior strip of elevated thresholds. The two low-threshold regions in the acute and the short-term group were arranged cochleotopically. This was reflected in a systematic shift of the cortical locations with minimum thresholds as a function of cochlear position of the radial and monopolar stimulation electrodes. By contrast, the long-term deafened animals maintained only weak or no signs of cochleotopicity. In some cases of this group, significant deviations from a simple tri-partition of the dorsoventral axis of AI was observed. Analysis of the spatial extent of the low-threshold regions revealed that the activated area in acute cases was significantly smaller than the long- and the short-term cases for both dorsal and ventral AI. There were no significant differences in the rostrocaudal extent of activation between long- and short-term deafening, although the total activated area in the short-term cases was larger than in long-term deafened animals. The width of the narrow high-threshold ridge that separated the dorsal and ventral low-threshold regions was the widest for the acute cases and the narrowest for the short-term deafened animals. The findings of relative large differences in cortical response distributions between the acute and short-term animals suggests that the effects observed in long-term deafened animals are not solely a consequence of loss of peripheral innervation density. The effects may reflect electrode-specific effects or reorganizational changes based on factors such as differences in excitatory and inhibitory balance.

Tonotopic and functional organization in the auditory cortex of the big brown bat, Eptesicus fuscus

1993 ◽  
Vol 70 (5) ◽  
pp. 1988-2009 ◽  
Author(s):  
S. P. Dear ◽  
J. Fritz ◽  
T. Haresign ◽  
M. Ferragamo ◽  
J. A. Simmons
Keyword(s):  
Auditory Cortex ◽  
Surface Area ◽  
Cortical Neurons ◽  
Functional Organization ◽  
Primary Auditory Cortex ◽  
Target Range ◽  
Cortical Surface ◽  
Behavioral Experiments ◽  
Cortical Surface Area ◽  
Harmonic Ratio

1. In Eptesicus the auditory cortex, as defined by electrical activity recorded from microelectrodes in response to tone bursts, FM sweeps, and combinations of FM sweeps, encompasses an average cortical surface area of 5.7 mm2. This area is large with respect to the total cortical surface area and reflects the importance of auditory processing to this species of bat. 2. The predominant pattern of organization in response to tone bursts observed in each cortex is tonotopic, with three discernible divisions revealed by our data. However, although cortical best-frequency (BF) maps from most of the individual bats are similar, no two maps are identical. The largest division contains an average of 84% of the auditory cortical surface area, with BF tonotopically mapped from high to low along the anteroposterior axis and is part of the primary auditory cortex. The medium division encompasses an average of 13% of the auditory cortical surface area, with highly variable BF organization across bats. The third region is the smallest, with an average of only 3% of auditory cortical surface area and is located at the anterolateral edge of the cortex. This region is marked by a reversal of the tonotopic axis and a restriction in the range of BFs as compared with the larger, tonotopically organized division. 3. A population of cortical neurons was found (n = 39) in which each neuron exhibited two BF threshold minima (BF1 and BF2) in response to tone bursts. These neurons thus have multipeaked frequency threshold tuning curves. In Eptesicus the majority of multipeaked frequency-tuned neurons (n = 27) have threshold minima at frequencies that correspond to a harmonic ratio of three-to-one. In contrast, the majority of multipeaked neurons in cats have threshold minima at frequencies in a ratio of three-to-two. A three-to-one harmonic ratio corresponds to the "spectral notches" produced by interference between overlapping echoes from multiple reflective surfaces in complex sonar targets. Behavioral experiments have demonstrated the ability of Eptesicus to use spectral interference notches for perceiving target shape, and this subpopulation of multipeaked frequency-tuned neurons may be involved in coding of spectral notches. 4. The auditory cortex contains delay-tuned neurons that encode target range (n = 99). Most delay-tuned neurons respond poorly to tones or individual FM sweeps and require combinations of FM sweeps. They are combination sensitive and delay tuned.(ABSTRACT TRUNCATED AT 400 WORDS)

Neural interaction in cat primary auditory cortex II. Effects of sound stimulation

1994 ◽  
Vol 71 (1) ◽  
pp. 246-270 ◽  
Author(s):  
J. J. Eggermont
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Relative Size ◽  
Primary Auditory Cortex ◽  
Mean Value ◽  
Neural Synchrony ◽  
Sound Stimulation ◽  
Common Input ◽  
Neural Correlation ◽  
The Mean

1. The effect of auditory stimulation with click trains, noise bursts, amplitude-modulated noise bursts, and amplitude-modulated tone bursts on the correlation of firing of 1,290 neuron pairs recorded on one or two electrodes in primary auditory cortex of the cat was investigated. A distinction was made between neural synchrony (the correlation under stimulus conditions) and neural correlation (the correlation under spontaneous or under stimulus conditions after correction for stimulus-related correlations). For neural correlation 63% of the single-electrode pairs showed a unilateral excitation component, often combined with a common-input peak, and only 11% of the dual electrode pairs showed this unilateral excitation. 2. Under poststimulus conditions the incidence of correlograms with clear peaks was high for single-electrode pairs (80–90% range) and somewhat lower for dual-electrode pairs (50–60% range). The strength of the neural correlation for poststimulus conditions, from 0.5 to 2 s after a 1-s stimulus, was comparable with that obtained for 15-min continuous silence, suggesting that aftereffects of stimulation had largely disappeared after 0.5 s. A stationary analysis of the correlation coefficient corroborated this. 3. Two stimulus-correction procedures, one based on the shift predictor and the other based on the joint peristimulus-time histogram (JPSTH) were compared. The mean value of the neural correlation under stimulus conditions obtained after applying the poststimulus time (PST) predictor was on average 20% larger than the mean value obtained after application of the shift predictor; however, this was not significantly different at the 0.05 level. There were no differences in the shape of the correlograms. This suggests that the less time-consuming shift predictor-based stimulus-correction procedure can be used for cortical neurons. 4. Under stimulus conditions neural correlation coefficients could be < or = 50% smaller than for spontaneous conditions. The strength of the stimulus-corrected neural correlation was inversely related to the relative size of the stimulus predictor (compared with the neural synchrony) and thus to the effectiveness of stimulation. This suggests that the assumption of additivity of stimulus and connectivity effects on neural synchrony is generally violated both for shift predictor and PST predictor procedures. 5. The neural correlogram peaks were narrower for single-electrode pairs than for dual-electrode pairs both under stimulus and spontaneous conditions. Under stimulus conditions the peaks were generally narrower than under spontaneous firing conditions.(ABSTRACT TRUNCATED AT 400 WORDS)

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

2010 ◽  
Vol 103 (5) ◽  
pp. 2339-2354 ◽  
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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