scholarly journals The extracellular matrix regulates cortical layer dynamics and cross-columnar frequency integration in the auditory cortex

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Mohamed El-Tabbal ◽  
Hartmut Niekisch ◽  
Julia U. Henschke ◽  
Eike Budinger ◽  
Renato Frischknecht ◽  
...  
Keyword(s):  
Extracellular Matrix ◽  
Auditory Cortex ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Cortical Layer ◽  
Mongolian Gerbils ◽  
Beta Band ◽  
Vertebrate Brain ◽  
Local Injections ◽  
The Impact

AbstractIn the adult vertebrate brain, enzymatic removal of the extracellular matrix (ECM) is increasingly recognized to promote learning, memory recall, and restorative plasticity. The impact of the ECM on translaminar dynamics during cortical circuit processing is still not understood. Here, we removed the ECM in the primary auditory cortex (ACx) of adult Mongolian gerbils using local injections of hyaluronidase (HYase). Using laminar current-source density (CSD) analysis, we found layer-specific changes of the spatiotemporal synaptic patterns with increased cross-columnar integration and simultaneous weakening of early local sensory input processing within infragranular layers Vb. These changes had an oscillatory fingerprint within beta-band (25–36 Hz) selectively within infragranular layers Vb. To understand the laminar interaction dynamics after ECM digestion, we used time-domain conditional Granger causality (GC) measures to identify the increased drive of supragranular layers towards deeper infragranular layers. These results showed that ECM degradation altered translaminar cortical network dynamics with a stronger supragranular lead of the columnar response profile.

scholarly journals Removal of the extracellular matrix biases auditory cortical layer dynamics towards supragranular frequency integration

2020 ◽  
Author(s):  
M El-Tabbal ◽  
H Niekisch ◽  
JU Henschke ◽  
E Budinger ◽  
R Frischknecht ◽  
...  
Keyword(s):  
Extracellular Matrix ◽  
Activity Patterns ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Cortical Layer ◽  
Synaptic Activity ◽  
Mongolian Gerbils ◽  
Beta Band ◽  
Oscillatory Power ◽  
Local Injections

AbstractIn the adult vertebrate brain, enzymatic removal of the extracellular matrix (ECM) is increasingly recognized to promote learning, memory recall, and restorative plasticity. However, the underlying impact of local removal of the ECM on cortical circuit processing is still not understood. Here, we removed the ECM in the primary auditory cortex (ACx) of adult Mongolian gerbils using local injections of hyaluronidase (HYase). Using laminar current-source density (CSD) analysis, we found layer-specific changes of the spatiotemporal synaptic activity patterns. Applying multitaper spectral analysis and time-domain conditional Granger causality (GC) measures, we found increased stimulus-evoked oscillatory power in the beta band (25-36 Hz) selectively within infragranular layers Vb and enhanced supragranular synaptic activity. Our findings reveal new insights on how ECM modulation affects the sensory integration via altered translaminar cortical network dynamics with a supragranular lead of the columnar response profile.

scholarly journals Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex

2019 ◽  
Author(s):  
Michael G. K. Brunk ◽  
Katrina E. Deane ◽  
Martin Kisse ◽  
Matthias Deliano ◽  
Silvia Vieweg ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Information Transfer ◽  
Cortical Plasticity ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Mongolian Gerbils ◽  
Spectral Processing ◽  
Optogenetic Stimulation ◽  
Spectral Integration ◽  
Stimulation Of

AbstractBackgroundReward associations during auditory learning induce cortical plasticity in the primary auditory cortex. A prominent source of such influence is the ventral tegmental area (VTA), which conveys a dopaminergic teaching signal to the primary auditory cortex. It is currently unknown, however, how the VTA circuitry thereby influences cortical frequency information processing and spectral integration. In this study, we therefore investigated the temporal effects of direct optogenetic stimulation of the VTA onto spectral integration in the auditory cortex on a synaptic circuit level by current-source-density analysis in anesthetized Mongolian gerbils.ResultsWhile auditory lemniscal input predominantly terminates in the granular input layers III/IV, we found that VTA-mediated modulation of spectral processing is relayed by a different circuit, namely enhanced thalamic inputs to the infragranular layers Vb/VIa. Activation of this circuit yields a frequency-specific gain amplification of local sensory input and enhances corticocortical information transfer, especially in supragranular layers I/II. This effects further persisted over more than 30 minutes after VTA stimulation.ConclusionsAltogether, we demonstrate that the VTA exhibits a long-lasting influence on sensory cortical processing via infragranular layers transcending the signaling of a mere reward-prediction error. Our findings thereby demonstrate a cellular and circuit substrate for the influence of reinforcement-evaluating brain systems on sensory processing in the auditory cortex.

scholarly journals Layer-Specific Intracortical Amplification Shortens the Lifetime of Thalamocortical Repetition Suppression in Auditory Cortex

2021 ◽  
Author(s):  
Jing Ma ◽  
Michael Brunk ◽  
Artur Matysiak ◽  
Nina Härtwich ◽  
Frank Ohl ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Meriones Unguiculatus ◽  
Neural Adaptation ◽  
Fundamental Aspect ◽  
Mongolian Gerbils ◽  
Cortical Layers ◽  
Repetition Suppression ◽  
Granular Layers

Abstract Neural adaptation in sensory cortex serves important sensory functions, and is altered by various neurophsychiatric diseases. Although adaptation is a widely studied phenomenon, much remains unknown about its underlying mechanisms on a cortical circuit level. Here, we investigated repetition suppression as fundamental aspect of adaptation by layer-specific current source density analyses of synaptic mass activities in primary auditory cortex of anesthetized Mongolian gerbils (Meriones unguiculatus). We disentangled different synaptic contributions to repetition suppression in different cortical layers, and separated thalamocortical from intracortical inputs by cortical silencing with GABAA-agonist muscimol. We systematically varied stimulus onset intervals and employed statistically robust model fitting based on bootstrapping to determine the full suppression kinetics of different synaptic responses in the steady state. Whereas thalamocortical input to granular and infragranular layers was governed by longer lasting repetition suppression, most likely reflecting depression of thalamocortical synapses, intracortical amplification in granular layers shortened the lifetime of suppression by re-enhancing granular responses mainly through synchronization of synaptic events. With increasing latency, the shorter lasting suppression kinetics observed in granular layers at early latencies (<100ms) passed on to deeper layers replacing the longer lasting infragranular suppression kinetics. Granular circuit dynamics can therefore actively shape neural adaptation across cortical layers.

scholarly journals Optogenetic stimulation of the VTA modulates a frequency-specific gain of thalamocortical inputs in infragranular layers of the auditory cortex

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Michael G. K. Brunk ◽  
Katrina E. Deane ◽  
Martin Kisse ◽  
Matthias Deliano ◽  
Silvia Vieweg ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Information Transfer ◽  
Cortical Plasticity ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Mongolian Gerbils ◽  
Spectral Processing ◽  
Optogenetic Stimulation ◽  
Spectral Integration ◽  
Stimulation Of

AbstractReward associations during auditory learning induce cortical plasticity in the primary auditory cortex. A prominent source of such influence is the ventral tegmental area (VTA), which conveys a dopaminergic teaching signal to the primary auditory cortex. Yet, it is unknown, how the VTA influences cortical frequency processing and spectral integration. Therefore, we investigated the temporal effects of direct optogenetic stimulation of the VTA onto spectral integration in the auditory cortex on a synaptic circuit level by current-source-density analysis in anesthetized Mongolian gerbils. While auditory lemniscal input predominantly terminates in the granular input layers III/IV, we found that VTA-mediated modulation of spectral processing is relayed by a different circuit, namely enhanced thalamic inputs to the infragranular layers Vb/VIa. Activation of this circuit yields a frequency-specific gain amplification of local sensory input and enhances corticocortical information transfer, especially in supragranular layers I/II. This effects persisted over more than 30 minutes after VTA stimulation. Altogether, we demonstrate that the VTA exhibits a long-lasting influence on sensory cortical processing via infragranular layers transcending the signaling of a mere reward-prediction error. We thereby demonstrate a cellular and circuit substrate for the influence of reinforcement-evaluating brain systems on sensory processing in the auditory cortex.

scholarly journals Thalamocortical and intracortical contributions to stimulus-evoked and oscillatory activity in rodent primary auditory cortex

2021 ◽  
Author(s):  
Marcus Jeschke ◽  
Frank W. Ohl
Keyword(s):  
Auditory Cortex ◽  
Computational Models ◽  
Frequency Tuning ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Sensory Stimulation ◽  
Gamma Oscillations ◽  
Oscillatory Activity ◽  
Mongolian Gerbils ◽  
Horizontal Connections

Intracortical, horizontal connections seem ideally suited to contribute to cortical processing by spreading information across cortical space and coordinating activity between distant cortical sites. In sensory systems experiments have implicated horizontal connections in the generation of receptive fields and have in turn led to computational models of receptive field generation that rely on the contribution of horizontal connections. Testing the contribution of horizontal connections at the mesoscopic level has been difficult due to the lack of a suitable method to observe the activity of intracortical horizontal connections. Here, we develop such a method based on the analysis of the relative residues of the cortical laminar current source density reconstructions. In the auditory cortex of Mongolian gerbils, the method is then tested by manipulating the contribution of horizontal connections by surgical dissection. Our results indicate that intracortical horizontal connections contribute to the frequency-tuning of mesoscopic cortical patches. Futhermore, we dissociated a type of cortical gamma oscillation based on horizontal connections between mesoscopic patches from gamma oscillations locally generated within mesoscopic patches. The data further imply that global and local coordination of activity during sensory stimulation occur in a low and high gamma frequency band, respectively. Taken together the present data demonstrate that intracortical horizontal connections play an important role in generating cortical feature tuning and coordinate neuronal oscillations across cortex.

Current Source Density Profiles of Stimulus-Specific Adaptation in Rat Auditory Cortex

2009 ◽  
Vol 102 (3) ◽  
pp. 1483-1490 ◽  
Author(s):  
Francois D. Szymanski ◽  
Jose A. Garcia-Lazaro ◽  
Jan W. H. Schnupp
Keyword(s):  
Auditory Cortex ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Auditory Pathway ◽  
Afferent Input ◽  
Current Source Density ◽  
Specific Adaptation ◽  
Source Density ◽  
Density Analysis ◽  
Layer V

Neurons in primary auditory cortex (A1) are known to exhibit a phenomenon known as stimulus-specific adaptation (SSA), which means that, when tested with pure tones, they will respond more strongly to a particular frequency if it is presented as a rare, unexpected “oddball” stimulus than when the same stimulus forms part of a series of common, “standard” stimuli. Although SSA has occasionally been observed in midbrain neurons that form part of the paraleminscal auditory pathway, it is thought to be weak, rare, or nonexistent among neurons of the leminscal pathway that provide the main afferent input to A1, so that SSA seen in A1 is likely generated within A1 by local mechanisms. To study the contributions that neural processing within the different cytoarchitectonic layers of A1 may make to SSA, we recorded local field potentials in A1 of the rat in response to standard and oddball tones and subjected these to current source density analysis. Although our results show that SSA can be observed throughout all layers of A1, right from the earliest part of the response, there are nevertheless significant differences between layers, with SSA becoming significantly stronger as stimulus-related activity passes from the main thalamorecipient layers III and IV to layer V.

scholarly journals Spectral Resolution of Monkey Primary Auditory Cortex (A1) Revealed With Two-Noise Masking

2006 ◽  
Vol 96 (3) ◽  
pp. 1105-1115 ◽  
Author(s):  
Yonatan I. Fishman ◽  
Mitchell Steinschneider
Keyword(s):  
Auditory Cortex ◽  
Spectral Resolution ◽  
Goodness Of Fit ◽  
Auditory Evoked Potentials ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Frequency Separation ◽  
Frequency Resolution ◽  
Noise Masking ◽  
Neural Populations

An important function of the auditory nervous system is to analyze the frequency content of environmental sounds. The neural structures involved in determining psychophysical frequency resolution remain unclear. Using a two-noise masking paradigm, the present study investigates the spectral resolution of neural populations in primary auditory cortex (A1) of awake macaques and the degree to which it matches psychophysical frequency resolution. Neural ensemble responses (auditory evoked potentials, multiunit activity, and current source density) evoked by a pulsed 60-dB SPL pure-tone signal fixed at the best frequency (BF) of the recorded neural populations were examined as a function of the frequency separation (ΔF) between the tone and two symmetrically flanking continuous 80-dB SPL, 50-Hz-wide bands of noise. ΔFs ranged from 0 to 50% of the BF, encompassing the range typically examined in psychoacoustic experiments. Responses to the signal were minimal for ΔF = 0% and progressively increased with ΔF, reaching a maximum at ΔF = 50%. Rounded exponential functions, used to model auditory filter shapes in psychoacoustic studies of frequency resolution, provided excellent fits to neural masking functions. Goodness-of-fit was greatest for response components in lamina 4 and lower lamina 3 and least for components recorded in more superficial cortical laminae. Physiological equivalent rectangular bandwidths (ERBs) increased with BF, measuring nearly 15% of the BF. These findings parallel results of psychoacoustic studies in both monkeys and humans, and thus indicate that a representation of perceptual frequency resolution is available at the level of A1.

scholarly journals Acute and Long-Term Circuit-Level Effects in the Auditory Cortex After Sound Trauma

2021 ◽  
Vol 14 ◽  
Author(s):  
Marcus Jeschke ◽  
Max F. K. Happel ◽  
Konstantin Tziridis ◽  
Patrick Krauss ◽  
Achim Schilling ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Current Source ◽  
Auditory Pathway ◽  
Meriones Unguiculatus ◽  
Sensory Receptor ◽  
Mongolian Gerbils ◽  
Hearing Impairments ◽  
Density Analysis ◽  
Acute Changes ◽  
Open Question

Harmful environmental sounds are a prevailing source of chronic hearing impairments, including noise induced hearing loss, hyperacusis, or tinnitus. How these symptoms are related to pathophysiological damage to the sensory receptor epithelia and its effects along the auditory pathway, have been documented in numerous studies. An open question concerns the temporal evolution of maladaptive changes after damage and their manifestation in the balance of thalamocortical and corticocortical input to the auditory cortex (ACx). To address these issues, we investigated the loci of plastic reorganizations across the tonotopic axis of the auditory cortex of male Mongolian gerbils (Meriones unguiculatus) acutely after a sound trauma and after several weeks. We used a residual current-source density analysis to dissociate adaptations of intracolumnar input and horizontally relayed corticocortical input to synaptic populations across cortical layers in ACx. A pure tone-based sound trauma caused acute changes of subcortical inputs and corticocortical inputs at all tonotopic regions, particularly showing a broad reduction of tone-evoked inputs at tonotopic regions around the trauma frequency. At other cortical sites, the overall columnar activity acutely decreased, while relative contributions of lateral corticocortical inputs increased. After 4–6 weeks, cortical activity in response to the altered sensory inputs showed a general increase of local thalamocortical input reaching levels higher than before the trauma. Hence, our results suggest a detailed mechanism for overcompensation of altered frequency input in the auditory cortex that relies on a changing balance of thalamocortical and intracortical input and along the frequency gradient of the cortical tonotopic map.

scholarly journals Task rule and choice are reflected by layer-specific processing in rodent auditory cortical microcircuits

2019 ◽  
Author(s):  
Marina M. Zempeltzi ◽  
Martin Kisse ◽  
Michael G. K. Brunk ◽  
Claudia Glemser ◽  
Sümeyra Aksit ◽  
...  
Keyword(s):  
Decision Making ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Brain Network ◽  
Meriones Unguiculatus ◽  
Network Activity ◽  
Mongolian Gerbils ◽  
Population Activity ◽  
Mixed Effect ◽  
Related Information

AbstractThe primary auditory cortex (A1) is an essential node in the integrative brain network that encodes the behavioral relevance of acoustic stimuli, predictions, and auditory-guided decision making. Previous studies have revealed task-related information being present at both the single-unit and population activity. However, its realization with respect to the cortical microcircuitry is less well understood. In this study, we used chronic, laminar current source density (CSD) analysis from the A1 of behaving Mongolian gerbils (Meriones unguiculatus) in order to characterize layer-specific, spatiotemporal synaptic population activity. Animals were trained to first detect and subsequently to discriminate two pure tone frequencies in consecutive training phases in a Go/NoGo shuttle-box task. We demonstrate that not only sensory but also task- and choice-related information is represented in the mesoscopic neuronal population code distributed across cortical layers. Based on a single-trial analysis using generalized linear-mixed effect models (GLMM), we found infragranular layers to be involved in auditory-guided action initiation during tone detection. Supragranular layers, particularly, are involved in the coding of choice options during tone discrimination. Further, we found that the overall columnar synaptic network activity represents the accuracy of the opted choice. Our study thereby suggests a multiplexed representation of stimulus features in dependence of the task, action selection, and the behavioral options of the animal in preparation of correct choices. The findings expand our understanding of how individual layers contribute to the integrative circuit of the A1 in order to code task-relevant information and guide sensory-based decision making.

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