The extracellular matrix regulates cortical layer dynamics and cross-columnar frequency integration in the auditory cortex.
Ontology highlight
ABSTRACT:
SUBMITTER: El-Tabbal M
PROVIDER: S-EPMC7946889 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Corticofugal projections outnumber subcortical input projections by far. However, the specific role for signal processing of corticofugal feedback is still less well understood in comparisonto the feedforward projection. Here, we lesioned corticothalamic (CT) neurons in layers V and/or VI of the auditory cortex of Mongolian gerbils by laser-induced photolysis to investigate their contribution to cortical activation patterns. We have used laminar current-source density (CSD) recordings of tone-evoked responses and could show that, particularly, lesion of CT neurons in layer VI affected cortical frequency processing. Specifically, we found a decreased gain of best-frequency input in thalamocortical (TC)-recipient input layers that correlated with the relative lesion of layer VI neurons, but not layer V neurons. Using cortical silencing with the GABA a -agonist muscimol and layer-specific intracortical microstimulation (ICMS), we found that direct activation of infragranular layers recruited a local recurrent cortico-thalamo-cortical loop of synaptic input. This recurrent feedback was also only interrupted when lesioning layer VI neurons, but not cells in layer V. Our study thereby shows distinct roles of these two types of CT neurons suggesting a particular impact of CT feedback from layer VI to affect the local feedforward frequency processing in auditory cortex.
| S-EPMC8311662 | biostudies-literature
Project description:The mammalian neocortex mediates complex cognitive behaviors, such as sensory perception, decision making, and language. The evolutionary history of the cortex, and the cells and circuitry underlying similar capabilities in nonmammals, are poorly understood, however. Two distinct features of the mammalian neocortex are lamination and radially arrayed columns that form functional modules, characterized by defined neuronal types and unique intrinsic connections. The seeming inability to identify these characteristic features in nonmammalian forebrains with earlier methods has often led to the assumption of uniqueness of neocortical cells and circuits in mammals. Using contemporary methods, we demonstrate the existence of comparable columnar functional modules in laminated auditory telencephalon of an avian species (Gallus gallus). A highly sensitive tracer was placed into individual layers of the telencephalon within the cortical region that is similar to mammalian auditory cortex. Distribution of anterograde and retrograde transportable markers revealed extensive interconnections across layers and between neurons within narrow radial columns perpendicular to the laminae. This columnar organization was further confirmed by visualization of radially oriented axonal collaterals of individual intracellularly filled neurons. Common cell types in birds and mammals that provide the cellular substrate of columnar functional modules were identified. These findings indicate that laminar and columnar properties of the neocortex are not unique to mammals and may have evolved from cells and circuits found in more ancient vertebrates. Specific functional pathways in the brain can be analyzed in regard to their common phylogenetic origins, which introduces a previously underutilized level of analysis to components involved in higher cognitive functions.
| S-EPMC2906560 | biostudies-literature
Project description:Integrating information across sensory domains to construct a unified representation of multi-sensory signals is a fundamental characteristic of perception in ecological contexts. One provocative hypothesis deriving from neurophysiology suggests that there exists early and direct cross-modal phase modulation. We provide evidence, based on magnetoencephalography (MEG) recordings from participants viewing audiovisual movies, that low-frequency neuronal information lies at the basis of the synergistic coordination of information across auditory and visual streams. In particular, the phase of the 2-7 Hz delta and theta band responses carries robust (in single trials) and usable information (for parsing the temporal structure) about stimulus dynamics in both sensory modalities concurrently. These experiments are the first to show in humans that a particular cortical mechanism, delta-theta phase modulation across early sensory areas, plays an important "active" role in continuously tracking naturalistic audio-visual streams, carrying dynamic multi-sensory information, and reflecting cross-sensory interaction in real time.
| S-EPMC2919416 | biostudies-literature
Project description:Columnar arrangements of neurons with similar preference have been suggested as the fundamental processing units of the cerebral cortex. Within these columnar arrangements, feed-forward information enters at middle cortical layers whereas feedback information arrives at superficial and deep layers. This interplay of feed-forward and feedback processing is at the core of perception and behavior. Here we provide in vivo evidence consistent with a columnar organization of the processing of sound frequency in the human auditory cortex. We measure submillimeter functional responses to sound frequency sweeps at high magnetic fields (7 tesla) and show that frequency preference is stable through cortical depth in primary auditory cortex. Furthermore, we demonstrate that-in this highly columnar cortex-task demands sharpen the frequency tuning in superficial cortical layers more than in middle or deep layers. These findings are pivotal to understanding mechanisms of neural information processing and flow during the active perception of sounds.
| S-EPMC4702984 | biostudies-literature
Project description:Recent studies have challenged the traditional notion of modality-dedicated cortical systems by showing that audition and touch evoke responses in the same sensory brain regions. While much of this work has focused on somatosensory responses in auditory regions, fewer studies have investigated sound responses and representations in somatosensory regions. In this functional magnetic resonance imaging (fMRI) study, we measured BOLD signal changes in participants performing an auditory frequency discrimination task and characterized activation patterns related to stimulus frequency using both univariate and multivariate analysis approaches. Outside of bilateral temporal lobe regions, we observed robust and frequency-specific responses to auditory stimulation in classically defined somatosensory areas. Moreover, using representational similarity analysis to define the relationships between multi-voxel activation patterns for all sound pairs, we found clear similarity patterns for auditory responses in the parietal lobe that correlated significantly with perceptual similarity judgments. Our results demonstrate that auditory frequency representations can be distributed over brain regions traditionally considered to be dedicated to somatosensation. The broad distribution of auditory and tactile responses over parietal and temporal regions reveals a number of candidate brain areas that could support general temporal frequency processing and mediate the extensive and robust perceptual interactions between audition and touch.
| S-EPMC6188539 | biostudies-literature
Project description:Despite numerous studies of auditory cortical processing in the ferret (Mustela putorius), very little is known about the connections between the different regions of the auditory cortex that have been characterized cytoarchitectonically and physiologically. We examined the distribution of retrograde and anterograde labeling after injecting tracers into one or more regions of ferret auditory cortex. Injections of different tracers at frequency-matched locations in the core areas, the primary auditory cortex (A1) and anterior auditory field (AAF), of the same animal revealed the presence of reciprocal connections with overlapping projections to and from discrete regions within the posterior pseudosylvian and suprasylvian fields (PPF and PSF), suggesting that these connections are frequency specific. In contrast, projections from the primary areas to the anterior dorsal field (ADF) on the anterior ectosylvian gyrus were scattered and non-overlapping, consistent with the non-tonotopic organization of this field. The relative strength of the projections originating in each of the primary fields differed, with A1 predominantly targeting the posterior bank fields PPF and PSF, which in turn project to the ventral posterior field, whereas AAF projects more heavily to the ADF, which then projects to the anteroventral field and the pseudosylvian sulcal cortex. These findings suggest that parallel anterior and posterior processing networks may exist, although the connections between different areas often overlap and interactions were present at all levels.
| S-EPMC4737260 | biostudies-literature
Project description:A canonical feedforward circuit is proposed to underlie sensory cortical responses with balanced excitation and inhibition in layer 4 (L4). However, in another input layer, L6, sensory responses and the underlying synaptic circuits remain largely unclear. Here, cell-attached recordings in rat primary auditory cortex revealed that for the majority of L6 excitatory neurons, tonal stimuli did not drive spike responses, but suppressed spontaneous firings. Whole-cell recordings further revealed that the silencing resulted from tone-evoked strong inhibition arriving earlier than excitation. This pattern of inputs can be attributed to a parallel feedforward circuit with both excitatory and inhibitory inputs disynaptically relayed. In contrast, in the other neurons directly driven by thalamic input, stimuli evoked excitation preceding relatively weak inhibition, resulting in robust spike responses. Thus, the dichotomy of L6 response properties arises from two distinct patterns of excitatory-inhibitory interplay. The parallel circuit module generating preceding inhibition may provide a gating mechanism for conditional corticothalamic feedback.
| S-EPMC2904750 | biostudies-literature
Project description:Lateral inhibition is a fundamental circuit operation that sharpens the tuning properties of cortical neurons. This operation is classically attributed to an increase in GABAergic synaptic input triggered by non-preferred stimuli. Here we use in vivo whole-cell recording and two-photon Ca2+ imaging in awake mice to show that lateral inhibition shapes frequency tuning in primary auditory cortex via an unconventional mechanism: non-preferred tones suppress both excitatory and inhibitory synaptic inputs onto layer 2/3 cells ("network suppression"). Moreover, optogenetic inactivation of inhibitory interneurons elicits a paradoxical increase in inhibitory synaptic input. These results indicate that GABAergic interneurons regulate cortical activity indirectly via the suppression of recurrent excitation. Furthermore, the network suppression underlying lateral inhibition was blocked by inactivation of somatostatin-expressing interneurons (SOM cells), but not parvalbumin-expressing interneurons (PV cells). Together, these findings reveal that SOM cells govern lateral inhibition and control cortical frequency tuning through the regulation of reverberating recurrent circuits.
| S-EPMC5705232 | biostudies-literature
Project description:The sensory cortices of the brain exhibit large-scale functional topographic organization, such as the tonotopic organization of the primary auditory cortex (A1) according to sound frequency. However, at the level of individual neurons, layer 2/3 (L2/3) A1 appears functionally heterogeneous. To identify if there exists a higher-order functional organization of meso-scale neuronal networks within L2/3 that bridges order and disorder, we used in vivo two-photon calcium imaging of pyramidal neurons to identify networks in three-dimensional volumes of L2/3 A1 in awake mice. Using tonal stimuli, we found diverse receptive fields with measurable colocalization of similarly tuned neurons across depth but less so across L2/3 sublayers. These results indicate a fractured microcolumnar organization with a column radius of ∼50 µm, with a more random organization of the receptive field over larger radii. We further characterized the functional networks formed within L2/3 by analyzing the spatial distribution of signal correlations (SCs). Networks show evidence of Rentian scaling in physical space, suggesting effective spatial embedding of subnetworks. Indeed, functional networks have characteristics of small-world topology, implying that there are clusters of functionally similar neurons with sparse connections between differently tuned neurons. These results indicate that underlying the regularity of the tonotopic map on large scales in L2/3 is significant tuning diversity arranged in a hybrid organization with microcolumnar structures and efficient network topologies.
| S-EPMC10898513 | biostudies-literature
Project description:During brain maturation, the occurrence of the extracellular matrix (ECM) terminates juvenile plasticity by mediating structural stability. Interestingly, enzymatic removal of the ECM restores juvenile forms of plasticity, as for instance demonstrated by topographical reconnectivity in sensory pathways. However, to which degree the mature ECM is a compromise between stability and flexibility in the adult brain impacting synaptic plasticity as a fundamental basis for learning, lifelong memory formation, and higher cognitive functions is largely unknown. In this study, we removed the ECM in the auditory cortex of adult Mongolian gerbils during specific phases of cortex-dependent auditory relearning, which was induced by the contingency reversal of a frequency-modulated tone discrimination, a task requiring high behavioral flexibility. We found that ECM removal promoted a significant increase in relearning performance, without erasing already established-that is, learned-capacities when continuing discrimination training. The cognitive flexibility required for reversal learning of previously acquired behavioral habits, commonly understood to mainly rely on frontostriatal circuits, was enhanced by promoting synaptic plasticity via ECM removal within the sensory cortex. Our findings further suggest experimental modulation of the cortical ECM as a tool to open short-term windows of enhanced activity-dependent reorganization allowing for guided neuroplasticity.
| S-EPMC3932855 | biostudies-other