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Mechanisms of Zero-Lag Synchronization in Cortical Motifs  [PDF]
Leonardo L. Gollo ,Claudio Mirasso,Olaf Sporns,Michael Breakspear
PLOS Computational Biology , 2014, DOI: doi/10.1371/journal.pcbi.1003548
Abstract: Zero-lag synchronization between distant cortical areas has been observed in a diversity of experimental data sets and between many different regions of the brain. Several computational mechanisms have been proposed to account for such isochronous synchronization in the presence of long conduction delays: Of these, the phenomenon of “dynamical relaying” – a mechanism that relies on a specific network motif – has proven to be the most robust with respect to parameter mismatch and system noise. Surprisingly, despite a contrary belief in the community, the common driving motif is an unreliable means of establishing zero-lag synchrony. Although dynamical relaying has been validated in empirical and computational studies, the deeper dynamical mechanisms and comparison to dynamics on other motifs is lacking. By systematically comparing synchronization on a variety of small motifs, we establish that the presence of a single reciprocally connected pair – a “resonance pair” – plays a crucial role in disambiguating those motifs that foster zero-lag synchrony in the presence of conduction delays (such as dynamical relaying) from those that do not (such as the common driving triad). Remarkably, minor structural changes to the common driving motif that incorporate a reciprocal pair recover robust zero-lag synchrony. The findings are observed in computational models of spiking neurons, populations of spiking neurons and neural mass models, and arise whether the oscillatory systems are periodic, chaotic, noise-free or driven by stochastic inputs. The influence of the resonance pair is also robust to parameter mismatch and asymmetrical time delays amongst the elements of the motif. We call this manner of facilitating zero-lag synchrony resonance-induced synchronization, outline the conditions for its occurrence, and propose that it may be a general mechanism to promote zero-lag synchrony in the brain.
Mechanisms of Zero-Lag Synchronization in Cortical Motifs  [PDF]
Leonardo L. Gollo,Claudio Mirasso,Olaf Sporns,Michael Breakspear
Physics , 2013, DOI: 10.1371/journal.pcbi.1003548
Abstract: Zero-lag synchronization between distant cortical areas has been observed in a diversity of experimental data sets and between many different regions of the brain. Several computational mechanisms have been proposed to account for such isochronous synchronization in the presence of long conduction delays: Of these, the phenomenon of "dynamical relaying" - a mechanism that relies on a specific network motif - has proven to be the most robust with respect to parameter mismatch and system noise. Surprisingly, despite a contrary belief in the community, the common driving motif is an unreliable means of establishing zero-lag synchrony. Although dynamical relaying has been validated in empirical and computational studies, the deeper dynamical mechanisms and comparison to dynamics on other motifs is lacking. By systematically comparing synchronization on a variety of small motifs, we establish that the presence of a single reciprocally connected pair - a "resonance pair" - plays a crucial role in disambiguating those motifs that foster zero-lag synchrony in the presence of conduction delays (such as dynamical relaying) from those that do not (such as the common driving triad). Remarkably, minor structural changes to the common driving motif that incorporate a reciprocal pair recover robust zero-lag synchrony. The findings are observed in computational models of spiking neurons, populations of spiking neurons and neural mass models, and arise whether the oscillatory systems are periodic, chaotic, noise-free or driven by stochastic inputs. The influence of the resonance pair is also robust to parameter mismatch and asymmetrical time delays amongst the elements of the motif. We call this manner of facilitating zero-lag synchrony resonance-induced synchronization, outline the conditions for its occurrence, and propose that it may be a general mechanism to promote zero-lag synchrony in the brain.
Directional Theta Coherence in Prefrontal Cortical to Amygdalo-Hippocampal Pathways Signals Fear Extinction  [PDF]
J?rg Lesting, Thiemo Daldrup, Venu Narayanan, Christian Himpe, Thomas Seidenbecher, Hans-Christian Pape
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0077707
Abstract: Theta oscillations are considered crucial mechanisms in neuronal communication across brain areas, required for consolidation and retrieval of fear memories. One form of inhibitory learning allowing adaptive control of fear memory is extinction, a deficit of which leads to maladaptive fear expression potentially leading to anxiety disorders. Behavioral responses after extinction training are thought to reflect a balance of recall from extinction memory and initial fear memory traces. Therefore, we hypothesized that the initial fear memory circuits impact behavioral fear after extinction, and more specifically, that the dynamics of theta synchrony in these pathways signal the individual fear response. Simultaneous multi-channel local field and unit recordings were obtained from the infralimbic prefrontal cortex, the hippocampal CA1 and the lateral amygdala in mice. Data revealed that the pattern of theta coherence and directionality within and across regions correlated with individual behavioral responses. Upon conditioned freezing, units were phase-locked to synchronized theta oscillations in these pathways, characterizing states of fear memory retrieval. When the conditioned stimulus evoked no fear during extinction recall, theta interactions were directional with prefrontal cortical spike firing leading hippocampal and amygdalar theta oscillations. These results indicate that the directional dynamics of theta-entrained activity across these areas guide changes in appraisal of threatening stimuli during fear memory and extinction retrieval. Given that exposure therapy involves procedures and pathways similar to those during extinction of conditioned fear, one therapeutical extension might be useful that imposes artificial theta activity to prefrontal cortical-amygdalo-hippocampal pathways that mimics the directionality signaling successful extinction recall.
Zero-lag long-range synchronization via dynamical relaying  [PDF]
Ingo Fischer,Raul Vicente,Javier M. Buldu,Michael Peil,Claudio R. Mirasso,M. C. Torrent,Jordi Garcia-Ojalvo
Physics , 2006, DOI: 10.1103/PhysRevLett.97.123902
Abstract: We show that simultaneous synchronization between two delay-coupled oscillators can be achieved by relaying the dynamics via a third mediating element, which surprisingly lags behind the synchronized outer elements. The zero-lag synchronization thus obtained is robust over a considerable parameter range. We substantiate our claims with experimental and numerical evidence of these synchronization solutions in a chain of three coupled semiconductor lasers with long inter-element coupling delays. The generality of the mechanism is validated in a neuronal model with the same coupling architecture. Thus, our results show that synchronized dynamical states can occur over long distances through relaying, without restriction by the amount of delay.
Properties of Zero-Lag Long-Range Synchronization via Dynamical Relaying  [PDF]
Maria de Sousa Vieira
Physics , 2007,
Abstract: In a recent letter, Fisher et al. reported the phenomenon of zero-lag long range isochronous synchronization via dynamical relaying in systems with delay [Phys. Rev. Lett. bf 97, 123902 (2006)]. They reported that when one has two coupled systems A and C, with delay between them, then the introduction of a third element B between A and C will allow them to synchronize even in regions of the parameter space where this was not possible without the presence of B. Here we study in detail the phenomenon and verify that in all the cases studied (including the ones reported by Fisher et al.) this occurs due to the tendency of A and B and B and C to be in antiphase synchronization and if A is in antiphase with B and B is in antiphase with C, it will imply that A and C are inphase. We show this in coupled quadratic maps, Kuramoto and R\"ossler oscillators. We also report that there is a simpler configuration where the same phenomenon occurs and has nearly the same features of the cases studied by Fisher et al.
Decomposing Neural Synchrony: Toward an Explanation for Near-Zero Phase-Lag in Cortical Oscillatory Networks  [PDF]
Rajasimhan Rajagovindan, Mingzhou Ding
PLOS ONE , 2008, DOI: 10.1371/journal.pone.0003649
Abstract: Background Synchronized oscillation in cortical networks has been suggested as a mechanism for diverse functions ranging from perceptual binding to memory formation to sensorimotor integration. Concomitant with synchronization is the occurrence of near-zero phase-lag often observed between network components. Recent theories have considered the importance of this phenomenon in establishing an effective communication framework among neuronal ensembles. Methodology/Principal Findings Two factors, among possibly others, can be hypothesized to contribute to the near-zero phase-lag relationship: (1) positively correlated common input with no significant relative time delay and (2) bidirectional interaction. Thus far, no empirical test of these hypotheses has been possible for lack of means to tease apart the specific causes underlying the observed synchrony. In this work simulation examples were first used to illustrate the ideas. A quantitative method that decomposes the statistical interdependence between two cortical areas into a feed-forward, a feed-back and a common-input component was then introduced and applied to test the hypotheses on multichannel local field potential recordings from two behaving monkeys. Conclusion/Significance The near-zero phase-lag phenomenon is important in the study of large-scale oscillatory networks. A rigorous mathematical theorem is used for the first time to empirically examine the factors that contribute to this phenomenon. Given the critical role that oscillatory activity is likely to play in the regulation of biological processes at all levels, the significance of the proposed method may extend beyond systems neuroscience, the level at which the present analysis is conceived and performed.
Gap junction involvement in hippocampal theta rhythm generation  [PDF]
Renata Bocian,Tomasz Kowalczyk
Post?py Higieny i Medycyny Do?wiadczalnej , 2012,
Abstract: Hippocampal theta rhythm is probably the best example of oscillations and synchrony phenomena occurring in neuronal networks of the central nervous system. It is well known that intraneuronal communication via chemical and electrical synapses underlies these oscillatory processes. Despite well-documented knowledge concerning the participation of chemical transmission in production of theta activity, the role of much faster gap junction communication is still not fully understood. This paper provides an overview of current research data concerning the involvement of electrical transmission in generation of the best synchronized EEG pattern recorded from the mammalian brain – theta rhythm.
Patterns of Coupled Theta Activity in Amygdala-Hippocampal-Prefrontal Cortical Circuits during Fear Extinction  [PDF]
J?rg Lesting, Rajeevan T. Narayanan, Christian Kluge, Susan Sangha, Thomas Seidenbecher, Hans-Christian Pape
PLOS ONE , 2011, DOI: 10.1371/journal.pone.0021714
Abstract: Signals related to fear memory and extinction are processed within brain pathways involving the lateral amygdala (LA) for formation of aversive stimulus associations, the CA1 area of the hippocampus for context-dependent modulation of these associations, and the infralimbic region of the medial prefrontal cortex (mPFC) for extinction processes. While many studies have addressed the contribution of each of these modules individually, little is known about their interactions and how they function as an integrated system. Here we show, by combining multiple site local field potential (LFP) and unit recordings in freely behaving mice in a fear conditioning paradigm, that theta oscillations may provide a means for temporally and functionally connecting these modules. Theta oscillations occurred with high specificity in the CA1-LA-mPFC network. Theta coupling increased between all areas during retrieval of conditioned fear, and declined during extinction learning. During extinction recall, theta coupling partly rebounded in LA-mPFC and CA1-mPFC, and remained at a low level in CA1-LA. Interfering with theta coupling through local electrical microstimulation in CA1-LA affected conditioned fear and extinction recall depending on theta phase. These results support the hypothesis that theta coupling provides a means for inter-areal coordination in conditioned behavioral responsiveness. More specifically, theta oscillations seem to contribute to a population code indicating conditioned stimuli during recall of fear memory before and after extinction.
When Long-Range Zero-Lag Synchronization is Feasible in Cortical Networks  [PDF]
Atthaphon Viriyopase,Ingo Bojak,Magteld Zeitler,Stan Gielen
Frontiers in Computational Neuroscience , 2012, DOI: 10.3389/fncom.2012.00049
Abstract: Many studies have reported long-range synchronization of neuronal activity between brain areas, in particular in the beta and gamma bands with frequencies in the range of 14–30 and 40–80 Hz, respectively. Several studies have reported synchrony with zero phase lag, which is remarkable considering the synaptic and conduction delays inherent in the connections between distant brain areas. This result has led to many speculations about the possible functional role of zero-lag synchrony, such as for neuronal communication, attention, memory, and feature binding. However, recent studies using recordings of single-unit activity and local field potentials report that neuronal synchronization may occur with non-zero phase lags. This raises the questions whether zero-lag synchrony can occur in the brain and, if so, under which conditions. We used analytical methods and computer simulations to investigate which connectivity between neuronal populations allows or prohibits zero-lag synchrony. We did so for a model where two oscillators interact via a relay oscillator. Analytical results and computer simulations were obtained for both type I Mirollo–Strogatz neurons and type II Hodgkin–Huxley neurons. We have investigated the dynamics of the model for various types of synaptic coupling and importantly considered the potential impact of Spike-Timing Dependent Plasticity (STDP) and its learning window. We confirm previous results that zero-lag synchrony can be achieved in this configuration. This is much easier to achieve with Hodgkin–Huxley neurons, which have a biphasic phase response curve, than for type I neurons. STDP facilitates zero-lag synchrony as it adjusts the synaptic strengths such that zero-lag synchrony is feasible for a much larger range of parameters than without STDP.
Auditory Cortical and Hippocampal-System Mismatch Responses to Duration Deviants in Urethane-Anesthetized Rats  [PDF]
Timo Ruusuvirta, Arto Lipponen, Eeva Pellinen, Markku Penttonen, Piia Astikainen
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0054624
Abstract: Any change in the invariant aspects of the auditory environment is of potential importance. The human brain preattentively or automatically detects such changes. The mismatch negativity (MMN) of event-related potentials (ERPs) reflects this initial stage of auditory change detection. The origin of MMN is held to be cortical. The hippocampus is associated with a later generated P3a of ERPs reflecting involuntarily attention switches towards auditory changes that are high in magnitude. The evidence for this cortico-hippocampal dichotomy is scarce, however. To shed further light on this issue, auditory cortical and hippocampal-system (CA1, dentate gyrus, subiculum) local-field potentials were recorded in urethane-anesthetized rats. A rare tone in duration (deviant) was interspersed with a repeated tone (standard). Two standard-to-standard (SSI) and standard-to-deviant (SDI) intervals (200 ms vs. 500 ms) were applied in different combinations to vary the observability of responses resembling MMN (mismatch responses). Mismatch responses were observed at 51.5–89 ms with the 500-ms SSI coupled with the 200-ms SDI but not with the three remaining combinations. Most importantly, the responses appeared in both the auditory-cortical and hippocampal locations. The findings suggest that the hippocampus may play a role in (cortical) manifestation of MMN.
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