Field Potential Responses Research Articles

Differential susceptibility of astrocytic and neuronal function to 3‐chloropropanediol in the rat inferior colliculus

We have previously shown that systemic administration of S(+)3-chloropropanediol (3-CPD) produces a morphological loss of astrocytes in specific nuclei of the rodent brain that precedes loss of both neurones and endothelial tight junctions. Here, we have evaluated the differential susceptibility of neuronal and astrocytic function to 3-CPD, in order to see if this parallels the morphological selectivity. To do this, we have developed an in vivo method for monitoring astrocyte function over time by giving hourly 20-min bolus challenge exposures to ammonia via an implanted microdialysis probe and measuring the resulting transient increases in the extracellular glutamine : glutamate ratio. These challenge ammonia exposures evoked a stable response for at least 5 h when the probe was implanted in the rat inferior colliculus, but caused no behavioural response or morphological damage. Although 3-CPD produced a rapid and sustained abolition of the ammonia response within 2 h, the field potential response of inferior collicular neurones to sound fell significantly to 75.0 ± 3.9% pre-dose at up to 8 h but then fell markedly, reaching 20.5 ± 3.7% at 2 days. Blood flow in the inferior colliculus also showed only late changes, increasing substantially at 2 days. Astrocyte damage at the EM level was seen from 3 h, followed by loss of astrocytes from 18 h to a minimum of 7 ± 10% control at 3 days. The rapid abolition of the ammonia response suggests that in addition to selective astrocyte death, 3-CPD also produces an earlier impairment of astrocyte function that precedes loss of neuronal function. This initial functional selectivity of 3-CPD provides a potential investigative tool in neurochemical studies of astrocyte-neuronal interactions.

ANATOMICALLY-CONSTRAINED EFFECTIVE CONNECTIVITY AMONG LAYERS IN A CORTICAL COLUMN MODELED AND ESTIMATED FROM LOCAL FIELD POTENTIALS

We propose a neural mass model for anatomically-constrained effective connectivity among neuronal populations residing in four layers (L2/3, L4, L5 and L6) within a cortical column. Eight neuronal populations in a given column--an excitatory population and an inhibitory population per layer--are assumed to be coupled via effective connections of unknown strengths that need to be estimated. The effective connections are constrained to anatomical connections that have been shown to exist in previous anatomical studies. The neural input to a cortical column is directed into the two populations in L4. The anatomically-constrained effective connectivity is captured by a system of 16 stochastic differential equations. Solving these equations yields the average postsynaptic potentials and transmembrane currents generated in each population. The current source density (CSD) responses in each layer, which serve as the model observations, are equated in the model to the sum of all currents generated within that layer. The model is implemented in a continuous-discrete state-space framework, and the innovation method is used for estimating the model parameters from CSD data. To this end, local field potential (LFP) responses to forepaw stimulation were recorded in rat area S1 using multi-channel linear probes. LFPs were converted to CSD signals, which were averaged within each layer, yielding one CSD response per layer. To estimate the effective strengths of connections between all cortical layers, the model was fitted to these CSD signals. The results show that the pattern of effective interactions is strongly influenced by the pattern of strengths of the anatomical connections; however, these two patterns are not identical. The estimated anatomically-constrained effective connectivity matrix and the anatomical connectivity matrix shared five of their six strongest connections, although rankings according to connection strength differed. The strongest effective connections were from excitatory neurons in layer 4 to excitatory neurons in layer 2/3. Our study shows the feasibility of estimating anatomically-constrained effective connectivity within a cortical column, and indicates that there is a strong influence of anatomical connectivity on effective connectivity between cortical layers.

Physiological effects of enriched environment exposure and LTP induction in the hippocampus in vivo do not transfer faithfully to in vitro slices

A number of experimental paradigms use in vitro brain slices to test for changes in synaptic transmission and plasticity following a behavioral manipulation. For example, a number of previous studies have reported a variety of effects of environmental enrichment (EE) exposure on field potential responses in hippocampal slices, but in no study was is it known what changes had been elicited in vivo. In the present study, we recorded from the hippocampus in vivo while rats underwent a brief period of EE. There was no detectable EE-induced change in synaptic efficacy in the dentate gyrus in vivo, but there was an increase in cellular excitability. In slices prepared from the same animals, we failed to observe any evidence of the excitability increase. We next tested whether LTP induction in vivo was better preserved in vitro. However, when slices from these rats were examined, there was no observable change in perforant path synaptic strength, although there was a modest increase in excitability that correlated with the increased excitability observed in vivo. These findings suggest that synaptic changes induced in vivo either are not preserved faithfully or are difficult to detect in hippocampal slices, while changes in cellular excitability are better preserved.

How Global Are Olfactory Bulb Oscillations?

Previous studies in waking animals have shown that the frequency structure of olfactory bulb (OB) local field potential oscillations is very similar across the OB, but large low-impedance surface electrodes may have favored highly coherent events, averaging out local inhomogeneities. We tested the hypothesis that OB oscillations represent spatially homogeneous phenomena at all scales. We used pairs of concentric electrodes (200 μm outer shaft surrounding an inner 2-3 μm recording site) beginning on the dorsal OB at anterior and medial locations in urethane-anesthetized rats and measured local field potential responses at successive 200 μm depths before and during odor stimulation. Within locations (outer vs. inner lead on a single probe), on the time scale of 0.5 s, coherence in all frequency bands was significant, but on larger time scales (10 s), only respiratory (1-4 Hz) and beta (15-30 Hz) oscillations showed prominent peaks. Across locations, coherence in all frequency bands was significantly lower for both sizes of electrodes at all depths but the most superficial 600 μm. Near the pial surface, coherence across outer (larger) electrodes at different sites was equal to coherence across outer and inner (small) electrodes within a single site and larger than coherence across inner electrodes at different sites. Overall, the beta band showed the largest coherence across bulbar sites and electrodes. Therefore larger electrodes at the surface of the OB favor globally coherent events, and at all depths, coherence depends on the type of oscillation (beta or gamma) and duration of the analysis window.

Regional differences in neurovascular coupling in rat brain as determined by fMRI and electrophysiology

Increases in neuronal activity induce local increases in cerebral perfusion. However, our understanding of the processes underlying this neurovascular coupling remains incomplete and, particularly, how these vary across the brain. Recent work supports an important role for astrocytes in neurovascular coupling, in large part via activation of their metabotropic glutamate receptors (mGluR). Here, using a combination of functional magnetic resonance imaging (fMRI) and electrophysiology we demonstrate regional heterogeneity in the mechanisms underlying neurovascular coupling. Direct electrical stimulation of the rat hindpaw sensorimotor cortex induces blood oxygenation level dependent (BOLD) and cerebral blood volume (CBV) fMRI responses in several anatomically distinct cortical and subcortical structures. Following intraperitoneal administration of the type 5 mGluR antagonist, MPEP, both BOLD and CBV responses to cortical stimulation were significantly reduced, whilst the local field potential (LFP) responses remained largely constant. Spatially, the degree of reduction in fMRI responses varied between cortical and subcortical regions (primary cortex ~ 18% vs. striatum ~ 66%), and also between primary and secondary cortical areas (~ 18% vs. ~ 55%). Similarly, greater decreases in response amplitude were seen in the contralateral secondary cortex (~ 91%) and ipsilateral striatum (~ 70%), compared to the primary cortex (~ 44%). Following MPEP, a negative component of the BOLD and CBV responses became more apparent, suggesting that different mechanisms mediate vasodilatory and vasoconstrictory responses. Interestingly, under baseline conditions the quantitative relationship between fMRI and LFP responses in cortical and subcortical regions was markedly different. Our data indicate that coupling between neuronal and fMRI responses is neither empirically nor mechanistically consistent across the brain.

Neural processing of short-term recurrence in songbird vocal communication.

BackgroundMany situations involving animal communication are dominated by recurring, stereotyped signals. How do receivers optimally distinguish between frequently recurring signals and novel ones? Cortical auditory systems are known to be pre-attentively sensitive to short-term delivery statistics of artificial stimuli, but it is unknown if this phenomenon extends to the level of behaviorally relevant delivery patterns, such as those used during communication.Methodology/Principal FindingsWe recorded and analyzed complete auditory scenes of spontaneously communicating zebra finch (Taeniopygia guttata) pairs over a week-long period, and show that they can produce tens of thousands of short-range contact calls per day. Individual calls recur at time scales (median interval 1.5 s) matching those at which mammalian sensory systems are sensitive to recent stimulus history. Next, we presented to anesthetized birds sequences of frequently recurring calls interspersed with rare ones, and recorded, in parallel, action and local field potential responses in the medio-caudal auditory forebrain at 32 unique sites. Variation in call recurrence rate over natural ranges leads to widespread and significant modulation in strength of neural responses. Such modulation is highly call-specific in secondary auditory areas, but not in the main thalamo-recipient, primary auditory area.Conclusions/SignificanceOur results support the hypothesis that pre-attentive neural sensitivity to short-term stimulus recurrence is involved in the analysis of auditory scenes at the level of delivery patterns of meaningful sounds. This may enable birds to efficiently and automatically distinguish frequently recurring vocalizations from other events in their auditory scene.

Corrigendum

CorrigendumCorrigendumPublished Online:01 Mar 2010https://doi.org/10.1152/jn.z9k-0006-corr.2010Original articleMoreSectionsPDF (539 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Volume 100, July 2008Hirata A, Castro-Alamancos MA, Cortical Transformation of Wide-Field (Multiwhisker) Sensory Responses. J Neurophysiol 100: , 2008. First published May 14, 2008; doi:10.1152/jn.90538.2008; http://jn.physiology.org/cgi/content/full/100/1/358.In Fig. 1B of the original published article, the light gray trace in the 2nd panel from the top (lefthand side) is incorrect (i.e., 2nd panel below the heading “0.2 Hz”). It is supposed to plot the sum of the adjacent whiskers' responses, but what is shown is the sum of all six whiskers (i.e., adjacent whiskers plus the principal whisker). This plot error does not affect any of the conclusions or results. The corrected figure is shown below.Fig. 1.Effect of single and multiwhisker stimulation on single units and field potentials (FPs) in ventroposterior medial (VPM) thalamus and barrel cortex. A: population peristimulus time histograms (PSTHs) and average FP responses evoked by single-whisker stimulation of the principal whisker (PW) or adjacent whiskers (AWs) for VPM cells, Fast-spiking (FS) cells and regular-spiking (RS) cortical cells, and for cortical FPs. Whisker stimulation was applied at 0.2 Hz (left panels) or 10 Hz (right panels). B: population PSTHs and average FP responses, for the cells shown in A, comparing PW and multiwhisker (“ALL 6 wkrs together”) responses. Also shown is the sum of the responses to each of the 5 AWs. Whisker stimulation was applied at 0.2 (left panels) or 10 Hz (right panels).Download figureDownload PowerPointThis article has no references to display. Download PDF Previous Back to Top FiguresReferencesRelatedInformationRelated ArticlesCortical Transformation of Wide-Field (Multiwhisker) Sensory Responses 01 Jul 2008Journal of Neurophysiology More from this issue > Volume 103Issue 3March 2010Pages 1705-1705 Copyright & PermissionsCopyright © 2010 the American Physiological Societyhttps://doi.org/10.1152/jn.z9k-0006-corr.2010History Published online 1 March 2010 Published in print 1 March 2010 Metrics

Computational modeling of GABAA receptor-mediated paired-pulse inhibition in the dentate gyrus

Paired-pulse inhibition (PPI) of the population spike observed in extracellular field recordings is widely used as a read-out of hippocampal network inhibition. PPI reflects GABA(A) receptor-mediated inhibition of principal neurons through local interneurons. However, because of its polysynaptic nature, it is difficult to assign PPI changes to precise synaptic mechanisms. Here we used a detailed network model of the dentate gyrus to simulate PPI of granule cell action potentials and analyze its network properties. Our computational analysis indicates that PPI results mainly from a combination of perisomatic feed-forward and feedback inhibition of granule cells by basket cells. Feed-forward inhibition mediated by basket cells appeared to be the most significant source of PPI. Our simulations suggest that PPI depends more on somatic than on dendritic inhibition of granule cells. Furthermore, PPI was modulated by changes in GABA(A) reversal potential (E(GABA)) and by alterations in intrinsic excitability of granule cells. In summary, computer modeling provides a useful tool for determining the role of synaptic and intrinsic cellular mechanisms in paired-pulse field potential responses.

Detection of Low Salience Whisker Stimuli Requires Synergy of Tectal and Thalamic Sensory Relays

Detection of a sensory stimulus depends on its psychophysical saliency; the higher the saliency, the easier the detection. But it is not known whether sensory relay nuclei differ in their ability to detect low salient whisker stimuli. We found that reversible lesions of either the somatosensory thalamus or superior colliculus blocked detection of a low salience whisker conditioned stimulus (WCS) in an active avoidance task, without affecting detection of a high salience WCS. Thus, thalamic and tectal sensory relays work synergistically to detect low salient stimuli during avoidance behavior, but are redundant during detection of highly salient stimuli. We also recorded electrophysiological responses evoked by high and low salience stimuli in the superior colliculus and barrel cortex of freely behaving animals during active exploration, awake immobility, and sensory detection in the active avoidance task. Field potential (FP) responses evoked in barrel cortex and superior colliculus by high intensity stimuli are larger and adapt more to frequency than those evoked by low-intensity stimuli. FP responses are also more suppressed and adapt less during active exploration, and become further suppressed in barrel cortex during successful detection of either high or low salient stimuli in the active avoidance task. In addition, unit recordings revealed that firing rate increases in superior colliculus during active exploration and especially during successful detection of either high or low salient stimuli in the active avoidance task. We conclude that detection of low salient stimuli is achieved by a sparse neural code distributed through multiple sensory relays.

Serotonin modulates glutamatergic transmission in the rat olfactory tubercle

The olfactory tubercle (OT) is found in the brains of mammals that are highly dependent on their sense of smell. Its human analogue is the poorly understood anterior perforated substance. Previous work on rat brain slices identified two types of field potential responses from the OT. The association fibre (AF) pathway was sensitive to muscarinic modulation, whereas the lateral olfactory tract (LOT) fibre pathway was not. Here, we establish that serotonin (5-hydroxytryptamine; 5-HT) also inhibits field potential excitatory postsynaptic potentials (EPSPs) in the AF, but not in the LOT fibre, pathway. Parallel experiments with adenosine (ADO) excluded ADO mediation of the 5-HT effect. Exogenous 5-HT at 30 microm caused a long-lasting approximately 40% reduction in the amplitude of AF postsynaptic responses, without affecting the time-course of EPSP decline, indicating a fairly restricted disposition of the 5-HT receptors responsible. The 5-HT(1)-preferring, 5-HT(5)-preferring and 5-HT(7)-preferring agonist 5-carboxamidotryptamine caused similar inhibition at approximately 100 nm. The 5-HT(1A)-preferring ligand 8-hydroxy-di-n-propylamino-tetralin at 10 microm, and the 5-HT uptake inhibitor citalopram at 3 microm, caused inhibition of AF-stimulated field potential responses in the 5-10% range. Order-of-potency information suggested a receptor of the 5-HT(1B) or 5-HT(1D) subtype. The 5-HT(1D) agonist L-694,247 (1 microm) suppressed the AF response by approximately 10% when used on its own. After washing out of L-694,427, inhibition by 30 microm 5-HT was reduced to negligible levels. Allowing for a partial agonist action of L-694,427 and complex interactions of 5-HT receptors within the OT, these results support the presence of active 5-HT(1D)-type receptors in the principal cell layer of the OT.

Asymmetries in long‐term and short‐term plasticity at thalamic and cortical inputs to the amygdala in vivo

Converging lines of evidence suggest that synaptic plasticity at auditory inputs to the lateral amygdala (LA) is critical for the formation and storage of auditory fear memories. Auditory information reaches the LA from both thalamic and cortical areas, raising the question of whether they make distinct contributions to fear memory storage. Here we address this by comparing the induction of long-term potentation (LTP) at the two inputs in vivo in anesthetized rats. We first show, using field potential measurements, that different patterns and frequencies of high-frequency stimulation (HFS) consistently elicit stronger LTP at cortical inputs than at thalamic inputs. Field potential responses elicited during HFS of thalamic inputs were also smaller than responses during HFS of cortical inputs, suggesting less effective postsynaptic depolarization. Pronounced differences in the short-term plasticity profiles of the two inputs were also observed: whereas cortical inputs displayed paired-pulse facilitation, thalamic inputs displayed paired-pulse depression. These differences in short- and long-term plasticity were not due to stronger inhibition at thalamic inputs: although removal of inhibition enhanced responses to HFS, it did not enhance thalamic LTP and left paired-pulse depression unaffected. These results highlight the divergent nature of short- and long-term plasticity at thalamic and cortical sensory inputs to the LA, pointing to their different roles in the fear learning system.

Representation of Concurrent Stimuli by Population Activity in Visual Cortex

How do neuronal populations represent concurrent stimuli? We measured population responses in cat primary visual cortex (V1) using electrode arrays. Population responses to two superimposed gratings were weighted sums of the individual grating responses. The weights depended strongly on the relative contrasts of the gratings. When the contrasts were similar, the population performed an approximately equal summation. When the contrasts differed markedly, however, the population performed approximately a winner-take-all competition. Stimuli that were intermediate to these extremes elicited intermediate responses. This entire range of behaviors was explained by a single model of contrast normalization. Normalization captured both the spike responses and the local field potential responses; it even predicted visually evoked currents source-localized to V1 in human subjects. Normalization has profound effects on V1 population responses and is likely to shape the interpretation of these responses by higher cortical areas.

Dose‐dependent effect of isoflurane on neurovascular coupling in rat cerebral cortex

Neurovascular coupling studies are widely conducted in anesthetized animals using functional magnetic resonance imaging (fMRI). In this study, the dose-dependent effects of isoflurane on neurovascular coupling were examined with concurrent recordings of the local field potential (FP) and cerebral blood flow (CBF) in the rat somatosensory cortex. Electrical forepaw stimulation was used, and consisted of either a single pulse or 10 pulses at various frequencies. We observed that the FP response to single-pulse stimulation remained unaffected across the different levels of isoflurane tested (1.1-2.1%), whereas the CBF response to single-pulse stimulation increased dose-dependently (7 +/- 3% to 17 +/- 4%). The isoflurane dose did not affect the vascular reactivity induced by a hypercapnic challenge. These findings suggest that the action of isoflurane affects the neurovascular mechanisms. For 10-pulse stimulation, the summation of the evoked FP responses monotonically decreased with an increase in the isoflurane dose, possibly due to enhancement of the neural adaptation. In contrast, the dose-dependent effect on the CBF response varied with the stimulus frequency; a dose-dependent decrease in the CBF response was observed for high-frequency stimulation, whereas a dose-dependent increase was observed for low-frequency stimulation. Furthermore, a linear time-invariant model consisting of the single-pulse hemodynamic impulse response convoluted with 10-pulse FP recordings showed that the neurovascular transfer function was altered by the isoflurane dose for high-frequency stimulation. These results indicate that careful and consistent maintenance of the depth of anesthesia is required when comparing fMRI data obtained from different animals or physiological and pharmacological manipulations.

Impact of Persistent Cortical Activity (Up States) on Intracortical and Thalamocortical Synaptic Inputs

The neocortex generates short epochs of persistent activity called up states, which are associated with changes in cellular and network excitability. Using somatosensory thalamocortical slices, we studied the impact of persistent cortical activity during spontaneous up states on intrinsic cellular excitability (input resistance) and on excitatory synaptic inputs of cortical cells. At the intrinsic excitability level, we found that the expected decrease in input resistance (high conductance) resulting from synaptic barrages during up states is counteracted by an increase in input resistance due to depolarization per se. The result is a variable but on average relatively small reduction in input resistance during up states. At the synaptic level, up states enhanced a late synaptic component of short-latency thalamocortical field potential responses but suppressed intracortical field potential responses. The thalamocortical enhancement did not reflect an increase in synaptic strength, as determined by measuring the evoked postsynaptic current, but instead an increase in evoked action potential (spike) probability due to depolarization during up states. In contrast, the intracortical suppression was associated with a reduction in synaptic strength, apparently driven by increased presynaptic intracortical activity during up states. In addition, intracortical suppression also reflected a reduction in evoked spike latency caused by depolarization and the abolishment of longer-latency spikes caused by stronger inhibitory drive during up states. In conclusion, depolarization during up states increases the success of excitatory synaptic inputs to reach firing. However, activity-dependent synaptic depression caused by increased presynaptic firing during up states and the enhancement of evoked inhibitory drive caused by depolarization suppress excitatory intracortical synaptic inputs.

Behavioral and Electrophysiological Correlates of Novelty Detection in Mouse Auditory Cortex

Event Abstract Back to Event Behavioral and Electrophysiological Correlates of Novelty Detection in Mouse Auditory Cortex Jose Garcia-Lazaro1*, I. Nelken2 and J. W. Schnupp1 1 Department of Physiology, Anatomy and Genetics, University of Oxford, United Kingdom 2 The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Israel In order to study the interactions between the behavioural and electrophysiological aspects of the processing of novel stimuli, we measured evoked epidural potentials from anesthetized (2-2-2-tribromoethanol/tert-amyl alcohol) C57BL6 mice in the oddball paradigm. Evoked local field potential responses were recorded epidurally from auditory cortex using custom-built low impedance electrodes. Acoustic stimuli consisted on 30 ms tone pips presented once every 300 ms. Two different frequencies, 6.67 kHz and 13.7 kHz, were presented in a randomly interleaved manner. In one condition, one of these frequencies was presented as a standard, with a 90% probability and the other as a deviant, with 10% probability. In a second condition, these probabilities were reversed. We recorded responses to 1000 repeats for each condition. Our preliminary data shows a strong oddball effect. Although this effect was observed for both frequencies, it was significantly stronger for the larger frequency. In order to investigate the potential role of experience, we also measured electrophysiological responses from animals after avoidance training. Training was entirely automated using a simplified version of the Intellicage system (NewBehavior AG, Zurich, Switzerland). The system operates using transponder technology for individual animal recognition and contains an isolated test chamber where mice obtain drinking water by triggering a nose-poke hole. In our paradigm, on 75% of the times an animal visited the chamber, a standard (6.67 kHz) sound stimulus was presented. The stimulus consisted on tone pips presented at intervals of 300 ms for 5 seconds. On the remaining 25% of the visits, a deviant (13.7 kHz) sound stimulus was presented. During a deviant visit animals did not obtain water, but instead a mildly aversive air-puff. Preliminary electrophysiological data from behaviorally trained animals shows that while potentials recorded in response to the standard (non-aversive) stimulus remained largely unchanged, potentials recorded in response to the aversive stimulus exhibited a two-fold increase in amplitude. These differences in the responses following training represent the prima facie evidence for experience induced changes in mouse auditory cortex. Supported by an EU FP6 project grant (LSHM-CT-2006-037378). Conference: MMN 09 Fifth Conference on Mismatch Negativity (MMN) and its Clinical and Scientific Applications, Budapest, Hungary, 4 Apr - 7 Apr, 2009. Presentation Type: Poster Presentation Topic: Poster Presentations Citation: Garcia-Lazaro J, Nelken I and Schnupp JW (2009). Behavioral and Electrophysiological Correlates of Novelty Detection in Mouse Auditory Cortex. Conference Abstract: MMN 09 Fifth Conference on Mismatch Negativity (MMN) and its Clinical and Scientific Applications. doi: 10.3389/conf.neuro.09.2009.05.080 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 25 Mar 2009; Published Online: 25 Mar 2009. * Correspondence: Jose Garcia-Lazaro, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom, jose.garcia-lazaro@dpag.ox.ac.uk Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Jose Garcia-Lazaro I. Nelken J. W Schnupp Google Jose Garcia-Lazaro I. Nelken J. W Schnupp Google Scholar Jose Garcia-Lazaro I. Nelken J. W Schnupp PubMed Jose Garcia-Lazaro I. Nelken J. W Schnupp Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Different Neural Frequency Bands Integrate Faces and Voices Differently in the Superior Temporal Sulcus

The integration of auditory and visual information is required for the default mode of speech-face-to-face communication. As revealed by functional magnetic resonance imaging and electrophysiological studies, the regions in and around the superior temporal sulcus (STS) are implicated in this process. To provide greater insights into the network-level dynamics of the STS during audiovisual integration, we used a macaque model system to analyze the different frequency bands of local field potential (LFP) responses to the auditory and visual components of vocalizations. These vocalizations (like human speech) have a natural time delay between the onset of visible mouth movements and the onset of the voice (the "time-to-voice" or TTV). We show that the LFP responses to faces and voices elicit distinct bands of activity in the theta (4-8 Hz), alpha (8-14 Hz), and gamma (>40 Hz) frequency ranges. Along with single neuron responses, the gamma band activity was greater for face stimuli than voice stimuli. Surprisingly, the opposite was true for the low-frequency bands-auditory responses were of a greater magnitude. Furthermore, gamma band responses in STS were sustained for dynamic faces but not so for voices (the opposite is true for auditory cortex). These data suggest that visual and auditory stimuli are processed in fundamentally different ways in the STS. Finally, we show that the three bands integrate faces and voices differently: theta band activity showed weak multisensory behavior regardless of TTV, the alpha band activity was enhanced for calls with short TTVs but showed little integration for longer TTVs, and finally, the gamma band activity was consistently enhanced for all TTVs. These data demonstrate that LFP activity from the STS can be segregated into distinct frequency bands which integrate audiovisual communication signals in an independent manner. These different bands may reflect different spatial scales of network processing during face-to-face communication.

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Behavioral states regulate how information is processed in local neuronal circuits. Here, we asked whether dendrodendritic synaptic interactions in the olfactory bulb vary with brain and behavioral states. To examine the state-dependent change of the dendrodendritic synaptic transmission, we monitored changes in field potential responses in the olfactory bulb of urethane-anesthetized and freely behaving rats. In urethane-anesthetized rats, granule-to-mitral dendrodendritic synaptic inhibition was larger and longer when slow waves were present in the electroencephalogram (slow-wave state) than during the fast-wave state. The state-dependent alternating change in the granule-to-mitral inhibition was regulated by the cholinergic system. In addition, the frequency of the spontaneous oscillatory activity of local field potentials and periodic discharges of mitral cells in the olfactory bulb shifted in synchrony with shifts in the neocortical brain state. Freely behaving rats showed multilevel changes in dendrodendritic synaptic inhibition that corresponded to diverse behavioral states; the inhibition was the largest during slow-wave sleep state, and successively smaller during light sleep, awake immobility, and awake moving states. These results provide evidence that behavioral state-dependent global changes in cholinergic tone modulate dendrodendritic synaptic inhibition and the information processing mode in the olfactory bulb.

α-Chloralose diminishes γ oscillations in rat hippocampal slices

alpha-Chloralose is an anesthetic characterized by its ability to maintain animals in physiological conditions though immobilized and anesthetized. In addition, alpha-chloralose induces a loss of consciousness with little influence on either pain response or cardiovascular reflexes. The pharmacological mechanisms of alpha-chloralose's actions are poorly understood. In vitro experiments have demonstrated alpha-chloralose enhances GABA(A) receptor function, which may underlie its anesthetic effect. However, how alpha-chloralose affects hippocampal synaptic function and neuronal network synchronization is unknown. In the present study, we performed electrophysiological recordings to examine the effects of alpha-chloralose on synaptic transmission, tetanic stimulation-induced gamma oscillations (30-80 Hz) and neuronal receptor function in rat hippocampal slices and dissociated hippocampal CA1 pyramidal neurons. The results demonstrated that alpha-chloralose (30-100 microM) diminished tetanic stimulation-induced gamma oscillations without affecting single stimulation-induced field potential responses. In single, dissociated hippocampal CA1 pyramidal neurons, alpha-chloralose activated GABA(A) receptors at a high concentration while it potentiated GABA(A) receptor-mediated currents at low concentrations. However, alpha-chloralose did not affect glutamate-, glycine-, or ACh-induced currents. Slice-patch recordings revealed alpha-chloralose enhanced GABAergic leak current and prolonged the decay constant of spontaneous inhibitory postsynaptic currents (sIPSCs). It is concluded that alpha-chloralose suppresses hippocampal gamma oscillations without significantly affecting basic synaptic transmission or ionotropic glutamate, choline and glycine receptor function. Enhancement of GABAergic leak current and prolongation of GABAergic sIPSCs by alpha-chloralose likely underlie its disruption of neuronal network synchronization in the hippocampus.

Synaptic Commitment: Developmentally Regulated Reciprocal Changes in Hippocampal Granule Cell NMDA and AMPA Receptors Over the Lifespan

Synaptic transmission in hippocampal field CA1 is largely N-methyl-d-aspartate receptor (NMDA(R)) dependent during the early postnatal period. It becomes increasingly mediated by alpha-amino-3-hydroxy-5-methylisoxazole-4-proprionate (AMPA) receptors until an adult ratio of AMPA to NMDA receptors is achieved. It is shown here that increases in the AMPA receptor (AMPA(R))-mediated field potential response continue over the life span of the F-344 rat at the perforant path-granule cell synapse in the dentate gyrus. In contrast, the NMDA(R)-dependent component of the response decreases with age between 1 and 27 mo, leading to an increase of AMPA(R)/NMDA(R) ratio with age. One possible explanation of this age difference is that the AMPA(R)/NMDA(R) ratio can be modified by experience. To test the idea that the changed ratio is caused by the old rats' longer lives, an intensive 10-mo period of enrichment treatment was given to a group of animals, beginning at 3 mo of age. Compared with animals housed in standard cages, the enrichment treatment did not alter the glutamatergic response ratio measured with field potential recording methods. These data provide support for the conclusion that the observed change with age is developmentally regulated rather than experience dependent. Given the role of the NMDA(R) in synaptic plasticity, these changes suggest a progressive commitment of perforant path synapses to particular weights over the life span. One possible implication of this effect includes preservation of selected memories, ultimately at the expense of a reduced capacity to store new information.

Temporal envelope processing in the human auditory cortex: Response and interconnections of auditory cortical areas

Temporal envelope processing in the human auditory cortex has an important role in language analysis. In this paper, depth recordings of local field potentials in response to amplitude modulated white noises were used to design maps of activation in primary, secondary and associative auditory areas and to study the propagation of the cortical activity between them. The comparison of activations between auditory areas was based on a signal-to-noise ratio associated with the response to amplitude modulation (AM). The functional connectivity between cortical areas was quantified by the directed coherence (DCOH) applied to auditory evoked potentials. This study shows the following reproducible results on twenty subjects: (1) the primary auditory cortex (PAC), the secondary cortices (secondary auditory cortex (SAC) and planum temporale (PT)), the insular gyrus, the Brodmann area (BA) 22 and the posterior part of T1 gyrus (T1Post) respond to AM in both hemispheres. (2) A stronger response to AM was observed in SAC and T1Post of the left hemisphere independent of the modulation frequency (MF), and in the left BA22 for MFs 8 and 16 Hz, compared to those in the right. (3) The activation and propagation features emphasized at least four different types of temporal processing. (4) A sequential activation of PAC, SAC and BA22 areas was clearly visible at all MFs, while other auditory areas may be more involved in parallel processing upon a stream originating from primary auditory area, which thus acts as a distribution hub. These results suggest that different psychological information is carried by the temporal envelope of sounds relative to the rate of amplitude modulation.