Reorganization of the Frequency Map of the Auditory Cortex Evoked by Cortical Electrical Stimulation in the Big Brown Bat

2000 ◽  
Vol 83 (4) ◽  
pp. 1856-1863 ◽  
Author(s):  
Syed A. Chowdhury ◽  
Nobuo Suga
Keyword(s):  
Electrical Stimulation ◽  
Auditory Cortex ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Acoustic Stimulus ◽  
Primary Auditory Cortex ◽  
Neural Representation ◽  
Tuning Curves ◽  
Big Brown Bat ◽  
Frequency Map

In a search phase of echolocation, big brown bats, Eptesicus fuscus, emit biosonar pulses at a rate of 10/s and listen to echoes. When a short acoustic stimulus was repetitively delivered at this rate, the reorganization of the frequency map of the primary auditory cortex took place at and around the neurons tuned to the frequency of the acoustic stimulus. Such reorganization became larger when the acoustic stimulus was paired with electrical stimulation of the cortical neurons tuned to the frequency of the acoustic stimulus. This reorganization was mainly due to the decrease in the best frequencies of the neurons that had best frequencies slightly higher than those of the electrically stimulated cortical neurons or the frequency of the acoustic stimulus. Neurons with best frequencies slightly lower than those of the acoustically and/or electrically stimulated neurons slightly increased their best frequencies. These changes resulted in the over-representation of repetitively delivered acoustic stimulus. Because the over-representation resulted in under-representation of other frequencies, the changes increased the contrast of the neural representation of the acoustic stimulus. Best frequency shifts for over-representation were associated with sharpening of frequency-tuning curves of 25% of the neurons studied. Because of the increases in both the contrast of neural representation and the sharpness of tuning, the over-representation of the acoustic stimulus is accompanied with an improvement of analysis of the acoustic stimulus.

Lateral Inhibition for Center-Surround Reorganization of the Frequency Map of Bat Auditory Cortex

2004 ◽  
Vol 92 (6) ◽  
pp. 3192-3199 ◽  
Author(s):  
Xiaofeng Ma ◽  
Nobuo Suga
Keyword(s):  
Auditory Cortex ◽  
Lateral Inhibition ◽  
Cortical Neurons ◽  
Electric Stimulation ◽  
Frequency Tuning ◽  
Constant Frequency ◽  
Specialized Area ◽  
Big Brown Bat ◽  
Frequency Map ◽  
Stimulation Of

Repetitive acoustic stimulation, auditory fear conditioning, and focal electric stimulation of the auditory cortex (AC) each evoke the reorganization of the central auditory system. Our current study of the big brown bat indicates that focal electric stimulation of the AC evokes center-surround reorganization of the frequency map of the AC. In the center, the neuron's best frequencies (BFs), together with their frequency–tuning curves, shift toward the BFs of electrically stimulated cortical neurons (centripetal BF shifts). In the surround, BFs shift away from the stimulated cortical BF (centrifugal BF shifts). Centripetal BF shifts are much larger than centrifugal BF shifts. An antagonist (bicuculline methiodide) of inhibitory synaptic transmitter receptors changes centrifugal BF shifts into centripetal BF shifts, whereas its agonist (muscimol) changes centripetal BF shifts into centrifugal BF shifts. This reorganization of the AC thus depends on a balance between facilitation and inhibition evoked by focal cortical electric stimulation. Unlike neurons in the AC of the big brown bat, neurons in the Doppler-shifted constant-frequency (DSCF) area of the AC of the mustached bat are highly specialized for fine-frequency analysis and show almost exclusively centrifugal BF shifts for focal electric stimulation of the DSCF area. Our current data indicate that in the highly specialized area, lateral inhibition is strong compared with the less-specialized area and that the specialized and nonspecialized areas both share the same inhibitory mechanism for centrifugal BF shifts.

scholarly journals Network Architecture, Receptive Fields, and Neuromodulation: Computational and Functional Implications of Cholinergic Modulation in Primary Auditory Cortex

2006 ◽  
Vol 96 (6) ◽  
pp. 2972-2983 ◽  
Author(s):  
Gabriel Soto ◽  
Nancy Kopell ◽  
Kamal Sen
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Network Architecture ◽  
Frequency Tuning ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Physiological Data ◽  
Cholinergic Modulation ◽  
Tuning Curves ◽  
Intracortical Circuits

Two fundamental issues in auditory cortical processing are the relative importance of thalamocortical versus intracortical circuits in shaping response properties in primary auditory cortex (ACx), and how the effects of neuromodulators on these circuits affect dynamic changes in network and receptive field properties that enhance signal processing and adaptive behavior. To investigate these issues, we developed a computational model of layers III and IV (LIII/IV) of AI, constrained by anatomical and physiological data. We focus on how the local and global cortical architecture shape receptive fields (RFs) of cortical cells and on how different well-established cholinergic effects on the cortical network reshape frequency-tuning properties of cells in ACx. We identify key thalamocortical and intracortical circuits that strongly affect tuning curves of model cortical neurons and are also sensitive to cholinergic modulation. We then study how differential cholinergic modulation of network parameters change the tuning properties of our model cells and propose two different mechanisms: one intracortical (involving muscarinic receptors) and one thalamocortical (involving nicotinic receptors), which may be involved in rapid plasticity in ACx, as recently reported in a study by Fritz and coworkers.

Corticofugal Shaping of Frequency Tuning Curves in the Central Nucleus of the Inferior Colliculus of Mice

2005 ◽  
Vol 93 (1) ◽  
pp. 71-83 ◽  
Author(s):  
Jun Yan ◽  
Yunfeng Zhang ◽  
Günter Ehret
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Tuning Curve ◽  
Primary Auditory Cortex ◽  
Nerve Fibers ◽  
Cortical Activation ◽  
Central Nucleus ◽  
Tuning Curves

Plasticity of the auditory cortex can be induced by conditioning or focal cortical stimulation. The latter was used here to measure how stimulation in the tonotopy of the mouse primary auditory cortex influences frequency tuning in the midbrain central nucleus of the inferior colliculus (ICC). Shapes of collicular frequency tuning curves (FTCs) were quantified before and after cortical activation by measuring best frequencies, FTC bandwidths at various sound levels, level tolerance, Q-values, steepness of low- and high-frequency slopes, and asymmetries. We show here that all of these measures were significantly changed by focal cortical activation. The changes were dependent not only on the relationship of physiological properties between the stimulated cortical neurons and recorded collicular neurons but also on the tuning curve class of the collicular neuron. Cortical activation assimilated collicular FTC shapes; sharp and broad FTCs were changed to the shapes comparable to those of auditory nerve fibers. Plasticity in the ICC was organized in a center (excitatory)-surround (inhibitory) way with regard to the stimulated location (i.e., the frequency) of cortical tonotopy. This ensures, together with the spatial gradients of distribution of collicular FTC shapes, a sharp spectral filtering at the core of collicular frequency-band laminae and an increase in frequency selectivity at the periphery of the laminae. Mechanisms of FTC plasticity were suggested to comprise both corticofugal and local ICC components of excitatory and inhibitory modulation leading to a temporary change of the balance between excitation and inhibition in the ICC.

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.

Noradrenergic Induction of Selective Plasticity in the Frequency Tuning of Auditory Cortex Neurons

2004 ◽  
Vol 92 (3) ◽  
pp. 1445-1463 ◽  
Author(s):  
Yves Manunta ◽  
Jean-Marc Edeline
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Cortical Plasticity ◽  
Frequency Tuning ◽  
Tone Frequency ◽  
Cortical Cells ◽  
Tuning Curves ◽  
Alpha Receptors ◽  
Frequency Changes ◽  
Selective Effects

Neuromodulators have long been viewed as permissive factors in experience-induced cortical plasticity, both during development and in adulthood. Experiments performed over the last two decades have reported the potency of acetylcholine to promote changes in functional properties of cortical cells in the auditory, visual, and somatosensory modality. In contrast, very few attempts were made with the monoaminergic systems. The present study evaluates how repeated presentation of brief pulses of noradrenaline (NA) concomitant with presentation of a particular tone frequency changes the frequency tuning curves of auditory cortex neurons determined at 20 dB above threshold. After 100 trials of NA-tone pairing, 28% of the cells (19/67) exhibited selective tuning modifications for the frequency paired with NA. All the selective effects were obtained when the paired frequency was within 1/4 of an octave from the initial best frequency. For these cells, selective decreases were prominent (15/19 cases), and these effects lasted ≥15 min after pairing. No selective effects were observed under various control conditions: tone alone ( n = 10 cells), NA alone ( n = 11 cells), pairing with ascorbic acid ( n = 6 cells), or with GABA ( n = 20 cells). Selective effects were observed when the NA-tone pairing was performed in the presence of propranolol (4/10 cells) but not when it was performed in the presence phentolamine (0/13 cells), suggesting that the effects were mediated by alpha receptors. These results indicate that brief increases in noradrenaline concentration can trigger selective modifications in the tuning curves of cortical neurons that, in most of the cases, go in opposite direction compared with those usually reported with acetylcholine.

Development of Reorganization of the Auditory Cortex Caused by Fear Conditioning: Effect of Atropine

2003 ◽  
Vol 90 (3) ◽  
pp. 1904-1909 ◽  
Author(s):  
Weiqing Ji ◽  
Nobuo Suga
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Acetylcholine Receptors ◽  
Conditioning Session ◽  
Acoustic Stimulation ◽  
Muscarinic Acetylcholine Receptors ◽  
Response Curves ◽  
Big Brown Bat ◽  
Frequency Map

Reorganization of the frequency map in the central auditory system is based on shifts in the best frequencies (BFs; hereafter, BF shifts), together with the frequency-response curves, of auditory neurons. In the big brown bat, conditioning with acoustic stimulation followed by electric leg-stimulation causes BF shifts of collicular and cortical neurons. The collicular BF shift develops quickly and is short term, whereas the cortical BF shift develops slowly and is long term. The acetycholine level in the auditory cortex must be high during conditioning to develop these BF shifts. We studied the effect of atropine (an antagonist of muscarinic acetylcholine receptors) applied to the auditory cortex on the development of the long-term cortical BF shift in the awake bat caused by a 30-min conditioning session. We found 1) the cortical BF shift starts to develop ∼15 min after the onset of the conditioning, gradually increases over 60 min, and reaches a plateau, 2) the cortical BF shift changes from short to long term ∼45 min after the onset of the conditioning, 3) the cortical BF shift can plateau at different frequencies between the BF of a given neuron in the control condition and the frequency of the conditioning tone, 4) the maximum BF shift is determined ∼70 min after the onset of the conditioning, and 5) acetylcholine plays an important role in the development of the cortical BF shift. Its role ends ∼180 min after the onset of the conditioning.

scholarly journals Temporal Modulation Transfer Functions in Cat Primary Auditory Cortex: Separating Stimulus Effects From Neural Mechanisms

2002 ◽  
Vol 87 (1) ◽  
pp. 305-321 ◽  
Author(s):  
Jos J. Eggermont
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Transfer Functions ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Modulation Transfer ◽  
Temporal Modulation ◽  
Pass Filter ◽  
Low Pass Filter ◽  
Low Pass

We present here a comparison between the local field potentials (LFP) and multiunit (MU) responses, comprising 401 single units, in primary auditory cortex (AI) of 31 cats to periodic click trains, gamma-tone and time-reversed gamma-tone trains, AM noise, AM tones, and frequency-modulated (FM) tones. In a large number of cases, the response to all six stimuli was obtained for the same neurons. We investigate whether cortical neurons are likely to respond to all types of repetitive transients and modulated stimuli and whether a dependence on modulating waveform, or tone or noise carrier, exists. In 97% of the recordings, a temporal modulation transfer function (tMTF) for MU activity was obtained for gamma-tone trains, in 92% for periodic click trains, in 83% for time-reversed gamma-tone trains, in 82% for AM noise, in 71% for FM tones, and only in 53% for AM tones. In 31% of the cases, the units responded to all six stimuli in an envelope-following way. These particular units had significantly larger onset responses to each stimulus compared with all other units. The overall response distribution shows the preference of AI units for stimuli with short rise times such as clicks and gamma tones. It also shows a clear asymmetry in the ability to respond to AM noise and AM tones and points to a strong effect of the frequency content of the carrier on the subcortical processing of AM stimuli. Yet all temporal response properties were independent of characteristic frequency and frequency-tuning curve bandwidth. We show that the observed differences in the tMTFs for different stimuli are to a large extent produced by the different degree of phase locking of the neuronal firings to the envelope of the first stimulus in the train or first modulation period. A normalization procedure, based on these synchronization differences, unified the tMTFs for all stimuli except clicks and allowed the identification of a largely stimulus-invariant, low-pass temporal filter function that most likely reflects the properties of synaptic depression and facilitation. For nonclick stimuli, the low-pass filter has a cutoff frequency of ∼10 Hz and a slope of ∼6 dB/octave. For nonclick stimuli, there was a systematic difference between the vector strength for LFPs and MU activity that can likely be attributed to postactivation suppression mechanisms.

Temporally precise population coding of dynamic sounds by auditory cortex

2021 ◽  
Author(s):  
Joshua D Downer ◽  
James Bigelow ◽  
Melissa Runfeldt ◽  
Brian James Malone
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Average Rate ◽  
Relative Effectiveness ◽  
Primary Auditory Cortex ◽  
Population Based ◽  
Population Coding ◽  
Complex Sounds ◽  
Animal Vocalizations

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.

Evaluating Information Transfer Between Auditory Cortical Neurons

2007 ◽  
Vol 97 (3) ◽  
pp. 2533-2543 ◽  
Author(s):  
Boris Gourévitch ◽  
Jos J. Eggermont
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Information Transfer ◽  
Cross Correlation ◽  
Past History ◽  
Temporal Integration ◽  
Acoustic Stimulus ◽  
Primary Auditory Cortex ◽  
Transfer Entropy ◽  
Neural Assembly

Transfer entropy, presented as a new tool for investigating neural assemblies, quantifies the fraction of information in a neuron found in the past history of another neuron. The asymmetry of the measure allows feedback evaluations. In particular, this tool has potential applications in investigating windows of temporal integration and stimulus-induced modulation of firing rate. Transfer entropy is also able to eliminate some effects of common history in spike trains and obtains results that are different from cross-correlation. The basic transfer entropy properties are illustrated with simulations. The information transfer through a network of 16 simultaneous multiunit recordings in cat's auditory cortex was examined for a large number of acoustic stimulus types. Application of the transfer entropy to a large database of multiple single-unit activity in cat's primary auditory cortex revealed that most windows of temporal integration found during spontaneous activity range between 2 and 15 ms. The normalized transfer entropy shows similarities and differences with the strength of cross-correlation; these form the basis for revisiting the neural assembly concept.

scholarly journals Effects of Acetylcholine and Atropine on Plasticity of Central Auditory Neurons Caused by Conditioning in Bats

2001 ◽  
Vol 86 (1) ◽  
pp. 211-225 ◽  
Author(s):  
Weiqing Ji ◽  
Enquan Gao ◽  
Nobuo Suga
Keyword(s):  
Somatosensory Cortex ◽  
Basal Forebrain ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Auditory Neurons ◽  
Tuning Curves ◽  
Acoustic Stimuli ◽  
Cholinergic Basal Forebrain ◽  
Big Brown Bat ◽  
Central Auditory Neurons

In the big brown bat ( Eptesicus fuscus), conditioning with acoustic stimuli followed by electric leg-stimulation causes shifts in frequency-tuning curves and best frequencies (hereafter BF shifts) of collicular and cortical neurons, i.e., reorganization of the cochleotopic (frequency) maps in the inferior colliculus (IC) and auditory cortex (AC). The collicular BF shift recovers 180 min after the conditioning, but the cortical BF shift lasts longer than 26 h. The collicular BF shift is not caused by conditioning, as the AC is inactivated during conditioning. Therefore it has been concluded that the collicular BF shift is caused by the corticofugal auditory system. The collicular and cortical BF shifts both are not caused by conditioning as the somatosensory cortex is inactivated during conditioning. Therefore it has been hypothesized that the cortical BF shift is mostly caused by both the subcortical (e.g., collicular) BF shift and the activity of nonauditory systems such as the somatosensory cortex excited by an unconditioned leg-stimulation and the cholinergic basal forebrain. The main aims of our present studies are to examine whether acetylcholine (ACh) applied to the AC augments the collicular and cortical BF shifts caused by the conditioning and whether atropine applied to the AC abolishes the cortical BF shift but not the collicular BF shift, as expected from the preceding hypothesis. In the awake bat, we made the following findings. ACh applied to the AC augments not only the cortical BF shift but also the collicular BF shift through the corticofugal system. Atropine applied to the AC reduces the collicular BF shift and abolishes the cortical BF shift which otherwise would be caused. ACh applied to the IC significantly augments the collicular BF shift but affects the cortical BF shift only slightly. ACh makes the cortical BF shift long-lasting beyond 4 h, but it cannot make the collicular BF shift long-lasting beyond 3 h. Atropine applied to the IC abolishes the collicular BF shift. It reduces the cortical BF shift but does not abolish it. Our findings favor the hypothesis that the BF shifts evoked by the corticofugal system, and an increased ACh level in the AC evoked by the basal forebrain are both necessary to evoke a long-lasting cortical BF shift.

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