Subthreshold Membrane Depolarization as Memory Trace for Perceptual Learning

2011 ◽  
Vol 23 (12) ◽  
pp. 3205-3231 ◽  
Author(s):  
Osamu Hoshino
Keyword(s):  
Perceptual Learning ◽  
Memory Trace ◽  
Neuronal Response ◽  
Membrane Depolarization ◽  
Spike Timing ◽  
Chemical Agent ◽  
Gabaergic Interneurons ◽  
Dependent Manner ◽  
Gaba Concentration ◽  
Ambient Gaba

Experience-dependent synaptic plasticity characterizes the adaptable brain and is believed to be the cellular substrate for perceptual learning. A chemical agent such as gamma-aminobutyric acid (GABA) is known to affect synaptic alteration, perhaps gating perceptual learning. We examined whether and how ambient (extrasynaptic) GABA affects experience-dependent synaptic alteration. A cortical neural network model was simulated. Transporters on GABAergic interneurons regulate ambient GABA levels around their axonal target neurons by removing GABA from (forward transport) or releasing it into (reverse transport) the extracellular space. The ambient GABA provides neurons with tonic inhibitory currents by activating extrasynaptic GABAa receptors. During repeated exposures to the same stimulus, we modified the synaptic connection strength between principal cells in a spike-timing-dependent manner. This modulated the activity of GABAergic interneurons, and reduced or augmented ambient GABA concentration. Reduction in ambient GABA concentration led to slight depolarization (less than several millivolts) in ongoing-spontaneous membrane potential. This was a subthreshold neuronal behavior because ongoing-spontaneous spiking activity remained almost unchanged. The ongoing-spontaneous subthreshold depolarization improved a suprathreshold neuronal response. If the stimulus was long absent for perceptual learning, augmentation of ambient GABA concentration took place and the ongoing-spontaneous subthreshold depolarization was depressed. We suggest that a perceptual memory trace could be left in neuronal circuitry as an ongoing-spontaneous subthreshold membrane depolarization, which would allow that memory to be accessed easily afterward, whereas a trace of a memory that has not recently been retrieved fades away when the ongoing-spontaneous subthreshold membrane depolarization built by previous perceptual learning is depressed. This would lead that memory to be accessed with some difficulty. In the brain, ambient GABA, whose level could be regulated by transporter may have an important role in leaving memory trace for perceptual learning.

Reduction of Trial-to-Trial Perceptual Variability by Intracortical Tonic Inhibition

2016 ◽  
Vol 28 (1) ◽  
pp. 187-215 ◽  
Author(s):  
Osamu Hoshino ◽  
Meihong Zheng ◽  
Kazuo Watanabe
Keyword(s):  
Neuronal Activity ◽  
Network Model ◽  
Dependent Manner ◽  
Gaba Concentration ◽  
Cell Assemblies ◽  
Principal Cells ◽  
Ambient Gaba ◽  
Spontaneous Neuronal Activity ◽  
Perceptual Variability ◽  
Feature Stimulus

Variability is a prominent characteristic of cognitive brain function. For instance, different trials of presentation of the same stimulus yield higher variability in its perception: subjects sometimes fail in perceiving the same stimulus. Perceptual variability could be attributable to ongoing-spontaneous fluctuation in neuronal activity prior to sensory stimulation. Simulating a cortical neural network model, we investigated the underlying neuronal mechanism of perceptual variability in relation to variability in ongoing-spontaneous neuronal activity. In the network model, populations of principal cells (cell assemblies) encode information about sensory features. Each cell assembly is sensitive to one particular feature stimulus. Transporters on GABAergic interneurons regulate ambient GABA concentration in a neuronal activity-dependent manner. Ambient GABA molecules activate extrasynaptic GABA[Formula: see text] receptors on principal cells and interneurons, and provide them with tonic inhibitory currents. We controlled the variability of ongoing-spontaneous neuronal activity by manipulating the basal level of ambient GABA and assessed the perceptual performance of the network: detection of a feature stimulus. In an erroneous response, stimulus-irrelevant but not stimulus-relevant principal cells were activated, generating trains of action potentials. Perceptual variability, reflected in error rate in detecting the same stimulus that was presented repeatedly to the network, was increased as the variability in ongoing-spontaneous membrane potential among cell assemblies increased. Frequent, transient membrane depolarization below firing threshold was the major cause of the increased neuronal variability, for which a decrease in basal ambient GABA concentration was responsible. We suggest that ambient GABA in the brain may have a role in reducing the variability in ongoing-spontaneous neuronal activity, leading to a decrease in perceptual variability and therefore to reliable sensory perception.

Cortical Representation of Auditory Space: Information-Bearing Features of Spike Patterns

2002 ◽  
Vol 87 (4) ◽  
pp. 1749-1762 ◽  
Author(s):  
Shigeto Furukawa ◽  
John C. Middlebrooks
Keyword(s):  
Sound Source ◽  
Neuronal Response ◽  
Source Location ◽  
Spike Timing ◽  
Spike Count ◽  
Cortical Representation ◽  
Auditory Space ◽  
Transmitted Information ◽  
Related Information ◽  
Spike Patterns

Previous studies have demonstrated that the spike patterns of cortical neurons vary systematically as a function of sound-source location such that the response of a single neuron can signal the location of a sound source throughout 360° of azimuth. The present study examined specific features of spike patterns that might transmit information related to sound-source location. Analysis was based on responses of well-isolated single units recorded from cortical area A2 in α-chloralose-anesthetized cats. Stimuli were 80-ms noise bursts presented from loudspeakers in the horizontal plane; source azimuths ranged through 360° in 20° steps. Spike patterns were averaged across samples of eight trials. A competitive artificial neural network (ANN) identified sound-source locations by recognizing spike patterns; the ANN was trained using the learning vector quantization learning rule. The information about stimulus location that was transmitted by spike patterns was computed from joint stimulus-response probability matrices. Spike patterns were manipulated in various ways to isolate particular features. Full-spike patterns, which contained all spike-count information and spike timing with 100-μs precision, transmitted the most stimulus-related information. Transmitted information was sensitive to disruption of spike timing on a scale of more than ∼4 ms and was reduced by an average of ∼35% when spike-timing information was obliterated entirely. In a condition in which all but the first spike in each pattern were eliminated, transmitted information decreased by an average of only ∼11%. In many cases, that condition showed essentially no loss of transmitted information. Three unidimensional features were extracted from spike patterns. Of those features, spike latency transmitted ∼60% more information than that transmitted either by spike count or by a measure of latency dispersion. Information transmission by spike patterns recorded on single trials was substantially reduced compared with the information transmitted by averages of eight trials. In a comparison of averaged and nonaveraged responses, however, the information transmitted by latencies was reduced by only ∼29%, whereas information transmitted by spike counts was reduced by 79%. Spike counts clearly are sensitive to sound-source location and could transmit information about sound-source locations. Nevertheless, the present results demonstrate that the timing of the first poststimulus spike carries a substantial amount, probably the majority, of the location-related information present in spike patterns. The results indicate that any complete model of the cortical representation of auditory space must incorporate the temporal characteristics of neuronal response patterns.

scholarly journals GABA transporters regulate tonic and synaptic GABAA receptor-mediated currents in the suprachiasmatic nucleus neurons

2017 ◽  
Vol 118 (6) ◽  
pp. 3092-3106 ◽  
Author(s):  
Michael Moldavan ◽  
Olga Cravetchi ◽  
Charles N. Allen
Keyword(s):  
Circadian Clock ◽  
Suprachiasmatic Nucleus ◽  
Dependent Manner ◽  
Circadian Period ◽  
Gaba Concentration ◽  
Gaba Transporter ◽  
Concentration Dependent Manner ◽  
Gaba Transport ◽  
Gaba Transporters ◽  
Tonic Current

GABA is a principal neurotransmitter in the hypothalamic suprachiasmatic nucleus (SCN) that contributes to intercellular communication between individual circadian oscillators within the SCN network and the stability and precision of the circadian rhythms. GABA transporters (GAT) regulate the extracellular GABA concentration and modulate GABAA receptor (GABAAR)-mediated currents. GABA transport inhibitors were applied to study how GABAAR-mediated currents depend on the expression and function of GAT. Nipecotic acid inhibits GABA transport and induced an inward tonic current in concentration-dependent manner during whole cell patch-clamp recordings from SCN neurons. Application of either the selective GABA transporter 1 (GAT1) inhibitors NNC-711 or SKF-89976A, or the GABA transporter 3 (GAT3) inhibitor SNAP-5114, produced only small changes of the baseline current. Coapplication of GAT1 and GAT3 inhibitors induced a significant GABAAR-mediated tonic current that was blocked by gabazine. GAT inhibitors decreased the amplitude and decay time constant and increased the rise time of spontaneous GABAAR-mediated postsynaptic currents. However, inhibition of GAT did not alter the expression of either GAT1 or GAT3 in the hypothalamus. Thus GAT1 and GAT3 functionally complement each other to regulate the extracellular GABA concentration and GABAAR-mediated synaptic and tonic currents in the SCN. Coapplication of SKF-89976A and SNAP-5114 (50 µM each) significantly reduced the circadian period of Per1 expression in the SCN by 1.4 h. Our studies demonstrate that GAT are important regulators of GABAAR-mediated currents and the circadian clock in the SCN. NEW & NOTEWORTHY In the suprachiasmatic nucleus (SCN), the GABA transporters GAT1 and GAT3 are expressed in astrocytes. Inhibition of these GABA transporters increased a tonic GABA current and reduced the circadian period of Per1 expression in SCN neurons. GAT1 and GAT3 showed functional cooperativity: inhibition of one GAT increased the activity but not the expression of the other. Our data demonstrate that GABA transporters are important regulators of GABAA receptor-mediated currents and the circadian clock.

scholarly journals The opposing Chloride Cotransporters KCC and NKCC control locomotor activity in constant light and during long days

2021 ◽  
Author(s):  
Anna Katharina Eick ◽  
Maite Ogueta ◽  
Edgar Buhl ◽  
James J. L. Hodge ◽  
Ralf Stanewsky
Keyword(s):  
Locomotor Activity ◽  
Circadian Clock ◽  
Opposite Effect ◽  
Neuronal Response ◽  
Reversal Potential ◽  
Ion Concentration ◽  
Day Length ◽  
Constant Light ◽  
Behavioral Activity ◽  
Dependent Manner

AbstractCation Chloride Cotransporters (CCC’s) regulate intracellular chloride ion concentration ([Cl−]i) within neurons, which can reverse the direction of the neuronal response to the neurotransmitter GABA. Na+ K+ Cl− (NKCC) and K+ Cl− (KCC) cotransporters transport Cl− into or out of the cell, respectively. When NKCC activity dominates, the resulting high [Cl−]i can lead to an excitatory and depolarizing response of the neuron upon GABAA receptor opening, while KCC dominance has the opposite effect. This inhibitory-to-excitatory GABA switch has been linked to seasonal adaption of circadian clock function to changing day length, and its dysregulation is associated with neurodevelopmental disorders such as epilepsy. Constant light normally disrupts circadian clock function and leads to arrhythmic behavior. Here, we demonstrate a function for KCC in regulating Drosophila locomotor activity and GABA responses in circadian clock neurons because alteration of KCC expression in circadian clock neurons elicits rhythmic behavior in constant light. We observed the same effects after downregulation of the Wnk and Fray kinases, which modulate CCC activity in a [Cl−]i-dependent manner. Patch-clamp recordings from clock neurons show that downregulation of KCC results in a more positive GABA reversal potential, while KCC overexpression has the opposite effect. Finally, KCC downregulation represses morning behavioral activity during long photoperiods, while downregulation of NKCC promotes morning activity. In summary, our results support a model in which the regulation of [Cl−]i by a KCC/NKCC/Wnk/Fray feedback loop determines the response of clock neurons to GABA, which is important for adjusting behavioral activity to constant light and long-day conditions.

Spatial Phase and the Temporal Structure of the Response to Gratings in V1

1998 ◽  
Vol 80 (2) ◽  
pp. 554-571 ◽  
Author(s):  
Jonathan D. Victor ◽  
Keith P. Purpura
Keyword(s):  
Spatial Frequency ◽  
Spike Train ◽  
Temporal Structure ◽  
Spike Timing ◽  
Dependent Manner ◽  
Data Set ◽  
Simple Cells ◽  
Complex Cells ◽  
Spatial Phase ◽  
Contrast Information

Victor, Jonathan D. and Keith P. Purpura. Spatial phase and the temporal structure of the response to gratings in V1. J. Neurophysiol. 80: 554–571, 1998. We recorded single-unit activity of 25 units in the parafoveal representation of macaque V1 to transient appearance of sinusoidal gratings. Gratings were systematically varied in spatial phase and in one or two of the following: contrast, spatial frequency, and orientation. Individual responses were compared based on spike counts, and also according to metrics sensitive to spike timing. For each metric, the extent of stimulus-dependent clustering of individual responses was assessed via the transmitted information, H. In nearly all data sets, stimulus-dependent clustering was maximal for metrics sensitive to the temporal pattern of spikes, typically with a precision of 25–50 ms. To focus on the interaction of spatial phase with other stimulus attributes, each data set was analyzed in two ways. In the “pooled phases” approach, the phase of the stimulus was ignored in the assessment of clustering, to yield an index H pooled. In the “individual phases” approach, clustering was calculated separately for each spatial phase and then averaged across spatial phases to yield an index H indiv. H pooled expresses the extent to which a spike train represents contrast, spatial frequency, or orientation in a manner which is not confounded by spatial phase (phase-independent representation), whereas H indiv expresses the extent to which a spike train represents one of these attributes, provided spatial phase is fixed (phase-dependent representation). Here, representation means that a stimulus attribute has a reproducible and systematic influence on individual responses, not a neural mechanism for decoding this influence. During the initial 100 ms of the response, contrast was represented in a phase-dependent manner by simple cells but primarily in a phase-independent manner by complex cells. As the response evolved, simple cell responses acquired phase-independent contrast information, whereas complex cells acquired phase-dependent contrast information. Simple cells represented orientation and spatial frequency in a primarily phase-dependent manner, but also they contained some phase-independent information in their initial response segment. Complex cells showed primarily phase-independent representation of orientation but primarily phase-dependent representation of spatial frequency. Joint representation of two attributes (contrast and spatial frequency, contrast and orientation, spatial frequency and orientation) was primarily phase dependent for simple cells, and primarily phase independent for complex cells. In simple and complex cells, the variability in the number of spikes elicited on each response was substantially greater than the expectations of a Poisson process. Although some of this variation could be attributed to the dependence of the response on the spatial phase of the grating, variability was still markedly greater than Poisson when the contribution of spatial phase to response variance was removed.

Tonically Balancing Intracortical Excitation and Inhibition by GABAergic Gliotransmission

2014 ◽  
Vol 26 (8) ◽  
pp. 1690-1716 ◽  
Author(s):  
Meihong Zheng ◽  
Takami Matsuo ◽  
Ai Miyamoto ◽  
Osamu Hoshino
Keyword(s):  
Extracellular Space ◽  
Plasma Membranes ◽  
Sensory Information ◽  
Inhibitory Mechanism ◽  
Neuronal Responses ◽  
Gaba Concentration ◽  
Cell Assemblies ◽  
Gaba Transporters ◽  
Ambient Gaba ◽  
P Cells

For sensory cortices to respond reliably to feature stimuli, the balancing of neuronal excitation and inhibition is crucial. A typical example might be the balancing of phasic excitation within cell assemblies and phasic inhibition between cell assemblies. The former controls the gain of and the latter the tuning of neuronal responses. A change in ambient GABA concentration might affect the dynamic behavior of neurons in a tonic manner. For instance, an increase in ambient GABA concentration enhances the activation of extrasynaptic receptors, augments an inhibitory current, and thus inhibits neurons. When a decrease in ambient GABA concentration occurs, the tonic inhibitory current is reduced, and thus the neurons are relatively excited. We simulated a neural network model in order to examine whether and how such a tonic excitatory-inhibitory mechanism could work for sensory information processing. The network consists of cell assemblies. Each cell assembly, comprising principal cells (P), GABAergic interneurons (Ia, Ib), and glial cells (glia), responds to one particular feature stimulus. GABA transporters, embedded in glial plasma membranes, regulate ambient GABA levels. Hypothetical neuron-glia signaling via inhibitory (Ia-to-glia) and excitatory (P-to-glia) synaptic contacts was assumed. The former let transporters import (remove) GABA from the extracellular space and excited stimulus-relevant P cells. The latter let them export GABA into the extracellular space and inhibited stimulus-irrelevant P cells. The main finding was that the glial membrane transporter gave a combinatorial excitatory-inhibitory effect on P cells in a tonic manner, thereby improving the gain and tuning of neuronal responses. Interestingly, it worked cooperatively with the conventional, phasic excitatory-inhibitory mechanism. We suggest that the GABAergic gliotransmission mechanism may provide balanced intracortical excitation and inhibition so that the best perceptual performance of the cortex can be achieved.

scholarly journals Modulation of Synaptic Plasticity by Glutamatergic Gliotransmission: A Modeling Study

2016 ◽  
Vol 2016 ◽  
pp. 1-30 ◽  
Author(s):  
Maurizio De Pittà ◽  
Nicolas Brunel
Keyword(s):  
Synaptic Plasticity ◽  
Glutamate Release ◽  
Spike Timing ◽  
Biophysical Model ◽  
Dependent Manner ◽  
Inward Currents ◽  
Functional Relevance ◽  
And Function ◽  
Activity Dependent

Glutamatergic gliotransmission, that is, the release of glutamate from perisynaptic astrocyte processes in an activity-dependent manner, has emerged as a potentially crucial signaling pathway for regulation of synaptic plasticity, yet its modes of expression and function in vivo remain unclear. Here, we focus on two experimentally well-identified gliotransmitter pathways, (i) modulations of synaptic release and (ii) postsynaptic slow inward currents mediated by glutamate released from astrocytes, and investigate their possible functional relevance on synaptic plasticity in a biophysical model of an astrocyte-regulated synapse. Our model predicts that both pathways could profoundly affect both short- and long-term plasticity. In particular, activity-dependent glutamate release from astrocytes could dramatically change spike-timing-dependent plasticity, turning potentiation into depression (and vice versa) for the same induction protocol.

scholarly journals A Minimum Perturbation Theory of Deep Perceptual Learning

2021 ◽  
Author(s):  
Haozhe Shan ◽  
Haim Sompolinsky
Keyword(s):  
Perceptual Learning ◽  
Network Architecture ◽  
Brain Plasticity ◽  
Deep Structure ◽  
Causal Relation ◽  
Neuronal Response ◽  
Single Layer ◽  
Behavioral Changes ◽  
Large Space ◽  
Deep Network

AbstractPerceptual learning (PL) involves long-lasting improvement in perceptual tasks following extensive training. Such improvement has been found to correlate with modifications in neuronal response properties in early as well as late sensory cortical areas. A major challenge is to dissect the causal relation between modification of the neural circuits and the behavioral changes. Previous theoretical and computational studies of PL have largely focused on single-layer model networks, and thus did not address salient characteristics of PL arising from the multiple-staged “deep” structure of the perceptual system. Here we develop a theory of PL in a deep neuronal network architecture, addressing the questions of how changes induced by PL are distributed across the multiple stages of cortex, and how do the respective changes determine the performance in fine discrimination tasks. We prove that in such tasks, modifications of synaptic weights of early sensory areas are both sufficient and necessary for PL. In addition, optimal synaptic weights in the deep network are not unique but span a large space of solutions. We postulate that, in the brain, plasticity throughout the deep network is distributed such that the resultant perturbation on prior circuit structures is minimized. In contrast to most previous models of PL, the minimum perturbation (MP) learning does not change the network readout weights. Our results provide mechanistic and normative explanations for several important physiological features of PL and reconcile apparently contradictory psychophysical findings.

Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT

2012 ◽  
Vol 108 (8) ◽  
pp. 2101-2114 ◽  
Author(s):  
P. Christiaan Klink ◽  
Anna Oleksiak ◽  
Martin J. M. Lankheet ◽  
Richard J. A. van Wezel
Keyword(s):  
Neuronal Response ◽  
Stimulus Presentation ◽  
Sensory Stimulation ◽  
Response Variability ◽  
Spike Timing ◽  
Response Magnitude ◽  
General Effect ◽  
Neuronal Responses ◽  
Area Mt ◽  
Response Characteristics

Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal adaptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-induced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation.

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