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 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 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 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 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.

Sensitivity to interaural intensity differences of neurons in primary auditory cortex of the cat. I. types of sensitivity and effects of variations in sound pressure level

1996 ◽  
Vol 75 (1) ◽  
pp. 75-96 ◽  
Author(s):  
D. R. Irvine ◽  
R. Rajan ◽  
L. M. Aitkin
Keyword(s):  
Auditory Cortex ◽  
High Frequency ◽  
Primary Auditory Cortex ◽  
Mirror Image ◽  
Sensitivity Function ◽  
Maximum Response ◽  
Binaural Interaction ◽  
Sensitivity Functions ◽  
Monaural Stimulation ◽  
Stimulation Of

1. Interaural intensity differences (IIDs) provide the major cue to the azimuthal location of high-frequency narrowband sounds. In recent studies of the azimuthal sensitivity of high-frequency neurons in the primary auditory cortex (field AI) of the cat, a number of different types of azimuthal sensitivity have been described and the azimuthal sensitivity of many neurons was found to vary as a function of changes in stimulus intensity. The extent to which the shape and the intensity dependence of the azimuthal sensitivity of AI neurons reflects features of their IID sensitivity was investigated by obtaining data on IID sensitivity from a large sample of neurons with a characteristic frequency (CF) > 5.5 kHz in AI of anesthetized cats. IID sensitivity functions were classified in a manner that facilitated comparison with previously obtained data on azimuthal sensitivity, and the effects of changes in the base intensity at which IIDs were introduced were examined. 2. IID sensitivity functions for CF tonal stimuli were obtained at one or more intensities for a total of 294 neurons, in most cases by a method of generating IIDs that kept the average binaural intensity (ABI) of the stimuli at the two ears constant. In the standard ABI range at which a function was obtained for each unit, five types of IID sensitivity were distinguished. Contra-max neurons (50% of the sample) had maximum response (a peak or a plateau) at IIDs corresponding to contralateral azimuths, whereas ipsi-max neurons (17%) had the mirror-image form of sensitivity. Near-zero-max neurons (18%) had a clearly defined maximum response (peak) in the range of +/- 10 dB IID, whereas a small group of tough neurons (2%) had a restricted range of minimal responsiveness with near-maximal responses at IIDs on either side. A final 18% of AI neurons were classified as insensitive to IIDs. The proportions of neurons exhibiting the various types of sensitivity corresponded closely to the proportions found to exhibit corresponding types of azimuthal sensitivity in a previous study. 3. There was a strong correlation between a neuron's binaural interaction characteristics and the form of its IID sensitivity function. Thus, neurons excited by monaural stimulation of only one ear but with either inhibitory, facilitatory, or mixed facilitatory-inhibitory effects of stimulation of the other ear had predominantly contra-max IID sensitivity (if contralateral monaural stimulation was excitatory) or ipsi-max sensitivity (if ipsilateral monaural stimulation was excitatory). Neurons driven weakly or not at all by monaural stimulation but facilitated binaurally almost all exhibited near-zero-max IID sensitivity. The exception to this tight association between binaural input and IID sensitivity was provided by neurons excited by monaural stimulation of either ear (EE neurons). Although EE neurons have frequently been considered to be insensitive to IIDs, our data were in agreement with two recent reports indicating that they can exhibit various forms of IID sensitivity: only 23 of 75 EE neurons were classified as insensitive and the remainder exhibited diverse types of sensitivity. 4. IID sensitivity was examined at two or more intensities (3-5 in most cases) for 84 neurons. The form of the IID sensitivity function (defined in terms of both shape and position along the IID axis) was invariant with changes in ABI for only a small proportion of IID-sensitive neurons (approximately 15% if a strict criterion of invariance was employed), and for many of these neurons the spike counts associated with a given IID varied with ABI, particularly at near-threshold levels. When the patterns of variation in the form of IID sensitivity produced by changes in ABI were classified in a manner equivalent to that used previously to classify the effects of intensity on azimuthal sensitivity, there was a close correspondence between the effects of intensity on corresponding types of azimuthal and IID sensitivity

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 Sensory Input Directs Spatial and Temporal Plasticity in Primary Auditory Cortex

2001 ◽  
Vol 86 (1) ◽  
pp. 326-338 ◽  
Author(s):  
Michael P. Kilgard ◽  
Pritesh K. Pandya ◽  
Jessica Vazquez ◽  
Anil Gehi ◽  
Christoph E. Schreiner ◽  
...  
Keyword(s):  
Receptive Field ◽  
Auditory Cortex ◽  
Carrier Frequency ◽  
Basal Forebrain ◽  
Sensory Input ◽  
Cortical Plasticity ◽  
Primary Auditory Cortex ◽  
Cortical Response ◽  
Modulation Rate ◽  
A1 Neurons

The cortical representation of the sensory environment is continuously modified by experience. Changes in spatial (receptive field) and temporal response properties of cortical neurons underlie many forms of natural learning. The scale and direction of these changes appear to be determined by specific features of the behavioral tasks that evoke cortical plasticity. The neural mechanisms responsible for this differential plasticity remain unclear partly because important sensory and cognitive parameters differ among these tasks. In this report, we demonstrate that differential sensory experience directs differential plasticity using a single paradigm that eliminates the task-specific variables that have confounded direct comparison of previous studies. Electrical activation of the basal forebrain (BF) was used to gate cortical plasticity mechanisms. The auditory stimulus paired with BF stimulation was systematically varied to determine how several basic features of the sensory input direct plasticity in primary auditory cortex (A1) of adult rats. The distributed cortical response was reconstructed from a dense sampling of A1 neurons after 4 wk of BF-sound pairing. We have previously used this method to show that when a tone is paired with BF activation, the region of the cortical map responding to that tone frequency is specifically expanded. In this report, we demonstrate that receptive-field size is determined by features of the stimulus paired with BF activation. Specifically, receptive fields were narrowed or broadened as a systematic function of both carrier-frequency variability and the temporal modulation rate of paired acoustic stimuli. For example, the mean bandwidth of A1 neurons was increased (+60%) after pairing BF stimulation with a rapid train of tones and decreased (−25%) after pairing unmodulated tones of different frequencies. These effects are consistent with previous reports of receptive-field plasticity evoked by natural learning. The maximum cortical following rate and minimum response latency were also modified as a function of stimulus modulation rate and carrier-frequency variability. The cortical response to a rapid train of tones was nearly doubled if BF stimulation was paired with rapid trains of random carrier frequency, while no following rate plasticity was observed if a single carrier frequency was used. Finally, we observed significant increases in response strength and total area of functionally defined A1 following BF activation paired with certain classes of stimuli and not others. These results indicate that the degree and direction of cortical plasticity of temporal and receptive-field selectivity are specified by the structure and schedule of inputs that co-occur with basal forebrain activation and suggest that the rules of cortical plasticity do not operate on each elemental stimulus feature independently of others.

Sign in / Sign up

Export Citation Format

Share Document