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

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.

2005 ◽  
Vol 93 (1) ◽  
pp. 71-83 ◽  
Author(s):  
Jun Yan ◽  
Yunfeng Zhang ◽  
Günter Ehret

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.


2000 ◽  
Vol 83 (4) ◽  
pp. 1856-1863 ◽  
Author(s):  
Syed A. Chowdhury ◽  
Nobuo Suga

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.


2021 ◽  
Vol 15 ◽  
Author(s):  
Wenlu Pan ◽  
Jing Pan ◽  
Yan Zhao ◽  
Hongzheng Zhang ◽  
Jie Tang

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.


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.


2004 ◽  
Vol 92 (3) ◽  
pp. 1445-1463 ◽  
Author(s):  
Yves Manunta ◽  
Jean-Marc Edeline

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.


2003 ◽  
Vol 90 (4) ◽  
pp. 2660-2675 ◽  
Author(s):  
Jennifer F. Linden ◽  
Robert C. Liu ◽  
Maneesh Sahani ◽  
Christoph E. Schreiner ◽  
Michael M. Merzenich

The mouse is a promising model system for auditory cortex research because of the powerful genetic tools available for manipulating its neural circuitry. Previous studies have identified two tonotopic auditory areas in the mouse—primary auditory cortex (AI) and anterior auditory field (AAF)— but auditory receptive fields in these areas have not yet been described. To establish a foundation for investigating auditory cortical circuitry and plasticity in the mouse, we characterized receptive-field structure in AI and AAF of anesthetized mice using spectrally complex and temporally dynamic stimuli as well as simple tonal stimuli. Spectrotemporal receptive fields (STRFs) were derived from extracellularly recorded responses to complex stimuli, and frequency-intensity tuning curves were constructed from responses to simple tonal stimuli. Both analyses revealed temporal differences between AI and AAF responses: peak latencies and receptive-field durations for STRFs and first-spike latencies for responses to tone bursts were significantly longer in AI than in AAF. Spectral properties of AI and AAF receptive fields were more similar, although STRF bandwidths were slightly broader in AI than in AAF. Finally, in both AI and AAF, a substantial minority of STRFs were spectrotemporally inseparable. The spectrotemporal interaction typically appeared in the form of clearly disjoint excitatory and inhibitory subfields or an obvious spectrotemporal slant in the STRF. These data provide the first detailed description of auditory receptive fields in the mouse and suggest that although neurons in areas AI and AAF share many response characteristics, area AAF may be specialized for faster temporal processing.


2002 ◽  
Vol 87 (1) ◽  
pp. 305-321 ◽  
Author(s):  
Jos J. Eggermont

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.


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.


1997 ◽  
Vol 78 (6) ◽  
pp. 3489-3492 ◽  
Author(s):  
Yunfeng Zhang ◽  
Nobuo Suga

Zhang, Yunfeng and Nobuo Suga. Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. J. Neurophysiol. 78: 3489–3492, 1997. Since 1962, physiological data of corticofugal effects on subcortical auditory neurons have been controversial: inhibitory, excitatory, or both. An inhibitory effect has been much more frequently observed than an excitatory effect. Recent studies performed with an improved experimental design indicate that corticofugal system mediates a highly focused positive feedback to physiologically “matched” subcortical neurons, and widespread lateral inhibition to “unmatched” subcortical neurons, in order to adjust and improve information processing. These results lead to a question: what happens to subcortical auditory responses when the corticofugal system, including matched and unmatched cortical neurons, is functionally eliminated? We temporarily inactivated both matched and unmatched neurons in the primary auditory cortex of the mustached bat with muscimol (an agonist of inhibitory synaptic transmitter) and measured the effect of cortical inactivation on subcortical auditory responses. Cortical inactivation reduced auditory responses in the medial geniculate body and the inferior colliculus. This reduction was larger (60 vs. 34%) and faster (11 vs. 31 min) for thalamic neurons than for collicular neurons. Our data indicate that the corticofugal system amplifies collicular auditory responses by 1.5 times and thalamic responses by 2.5 times on average. The data are consistant with a scheme in which positive feedback from the auditory cortex is modulated by inhibition that may mostly take place in the cortex.


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