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 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 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 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.

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 An Oscillatory Hierarchy Controlling Neuronal Excitability and Stimulus Processing in the Auditory Cortex

2005 ◽  
Vol 94 (3) ◽  
pp. 1904-1911 ◽  
Author(s):  
Peter Lakatos ◽  
Ankoor S. Shah ◽  
Kevin H. Knuth ◽  
Istvan Ulbert ◽  
George Karmos ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Neuronal Excitability ◽  
Spatial Scales ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Hierarchical Organization ◽  
Synaptic Activity ◽  
Oscillatory Activity ◽  
Theta Phase

EEG oscillations are hypothesized to reflect cyclical variations in the neuronal excitability, with particular frequency bands reflecting differing spatial scales of brain operation. However, despite decades of clinical and scientific investigation, there is no unifying theory of EEG organization, and the role of ongoing activity in sensory processing remains controversial. This study analyzed laminar profiles of synaptic activity [current source density CSD] and multiunit activity (MUA), both spontaneous and stimulus-driven, in primary auditory cortex of awake macaque monkeys. Our results reveal that the EEG is hierarchically organized; delta (1–4 Hz) phase modulates theta (4–10 Hz) amplitude, and theta phase modulates gamma (30–50 Hz) amplitude. This oscillatory hierarchy controls baseline excitability and thus stimulus-related responses in a neuronal ensemble. We propose that the hierarchical organization of ambient oscillatory activity allows auditory cortex to structure its temporal activity pattern so as to optimize the processing of rhythmic inputs.

scholarly journals Auditory Thalamocortical Synaptic Transmission In Vitro

2002 ◽  
Vol 87 (1) ◽  
pp. 361-384 ◽  
Author(s):  
Scott J. Cruikshank ◽  
Heather J. Rose ◽  
Raju Metherate
Keyword(s):  
Current Source ◽  
Temporal Cortex ◽  
Gross Anatomy ◽  
Primary Auditory Cortex ◽  
Cortical Layer ◽  
Slice Preparation ◽  
Functional Connection ◽  
Antidromic Activation ◽  
Medial Geniculate

To facilitate an understanding of auditory thalamocortical mechanisms, we have developed a mouse brain-slice preparation with a functional connection between the ventral division of the medial geniculate (MGv) and the primary auditory cortex (ACx). Here we present the basic characteristics of the slice in terms of physiology (intracellular and extracellular recordings, including current source density analysis), pharmacology (including glutamate receptor involvement), and anatomy (gross anatomy, Nissl, parvalbumin immunocytochemistry, and tract tracing with 1,1′-dioctadecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate). Thalamocortical transmission in this preparation (the “primary” slice) involves both α-amino-3-hydroxy-5-methylisoxazole-4-proprionic acid/kainate and N-methyl-d-aspartate-type glutamate receptors that appear to mediate monosynaptic inputs to layers 3-4 of ACx. MGv stimulation also initiates disynaptic inhibitory postsynaptic potentials and longer-duration intracortical, polysynaptic activity. Important differences between responses elicited by MGv versus conventional columnar (“on-beam”) stimulation emphasize the necessity of thalamic activation to infer thalamocortical mechanisms. We also introduce a second slice preparation, the “shell” slice, obtained from the brain region immediately ventral to the primary slice, that may contain a nonprimary thalamocortical pathway to temporal cortex. In the shell slice, stimulation of the thalamus or the region immediately ventral to it appears to produce fast activation of synapses in cortical layer 1 followed by robust intracortical polysynaptic activity. The layer 1 responses may result from orthodromic activation of nonprimary thalamocortical pathways; however, a plausible alternative could involve antidromic activation of corticotectal neurons and their layer 1 collaterals. The primary and shell slices will provide useful tools to investigate mechanisms of information processing in the ACx.

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.

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

2020 ◽  
Vol 3 (1) ◽  
Author(s):  
Marina M. Zempeltzi ◽  
Martin Kisse ◽  
Michael G. K. Brunk ◽  
Claudia Glemser ◽  
Sümeyra Aksit ◽  
...  
Keyword(s):  
Decision Making ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Relevant Information ◽  
Neuronal Population ◽  
Meriones Unguiculatus ◽  
Mongolian Gerbils ◽  
Population Activity ◽  
Mixed Effect ◽  
Task Rule

AbstractThe primary auditory cortex (A1) is an essential, integrative node that encodes the behavioral relevance of acoustic stimuli, predictions, and auditory-guided decision-making. However, the realization of this integration with respect to the cortical microcircuitry is not well understood. Here, we characterize layer-specific, spatiotemporal synaptic population activity with chronic, laminar current source density analysis in Mongolian gerbils (Meriones unguiculatus) trained in an auditory decision-making 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 of A1. Based on generalized linear-mixed effect models we found a layer-specific and multiplexed representation of the task rule, action selection, and the animal’s behavioral options as accumulating evidence in preparation of correct choices. The findings expand our understanding of how individual layers contribute to the integrative circuit in the sensory cortex in order to code task-relevant information and guide sensory-based decision-making.

scholarly journals Prestimulus feedback connectivity biases the content of visual experiences

2019 ◽  
Vol 116 (32) ◽  
pp. 16056-16061 ◽  
Author(s):  
Elie Rassi ◽  
Andreas Wutz ◽  
Nadia Müller-Voggel ◽  
Nathan Weisz
Keyword(s):  
Neural Activity ◽  
Activity Patterns ◽  
Low Frequency ◽  
Brain Regions ◽  
Stimulus Onset ◽  
Neural Excitability ◽  
Gamma Frequency ◽  
Face Area ◽  
Oscillatory Power ◽  
The Impact

Ongoing fluctuations in neural excitability and in networkwide activity patterns before stimulus onset have been proposed to underlie variability in near-threshold stimulus detection paradigms—that is, whether or not an object is perceived. Here, we investigated the impact of prestimulus neural fluctuations on the content of perception—that is, whether one or another object is perceived. We recorded neural activity with magnetoencephalography (MEG) before and while participants briefly viewed an ambiguous image, the Rubin face/vase illusion, and required them to report their perceived interpretation in each trial. Using multivariate pattern analysis, we showed robust decoding of the perceptual report during the poststimulus period. Applying source localization to the classifier weights suggested early recruitment of primary visual cortex (V1) and ∼160-ms recruitment of the category-sensitive fusiform face area (FFA). These poststimulus effects were accompanied by stronger oscillatory power in the gamma frequency band for face vs. vase reports. In prestimulus intervals, we found no differences in oscillatory power between face vs. vase reports in V1 or in FFA, indicating similar levels of neural excitability. Despite this, we found stronger connectivity between V1 and FFA before face reports for low-frequency oscillations. Specifically, the strength of prestimulus feedback connectivity (i.e., Granger causality) from FFA to V1 predicted not only the category of the upcoming percept but also the strength of poststimulus neural activity associated with the percept. Our work shows that prestimulus network states can help shape future processing in category-sensitive brain regions and in this way bias the content of visual experiences.

Sign in / Sign up

Export Citation Format

Share Document