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Identifying the synaptic origin of ongoing neuronal oscillations through spatial discrimination of electric fields.

Fernández-Ruiz A, Herreras O - Front Comput Neurosci (2013)

Bottom Line: However, multi-site recording devices now provide high-resolution spatial profiles of local field potentials (LFPs) and when coupled to modern mathematical analyses that discriminate signals with distinct but overlapping spatial distributions, they open the door to better understand these potentials.Accordingly, some oscillatory patterns can now be viewed as a periodic succession of synchronous synaptic currents that reflect the time envelope of spiking activity in given presynaptic populations.These analyses modify our concept of brain rhythms as abstract entities, molding them into mechanistic representations of network activity and allowing us to work in the time domain, reducing the loss of information inherent to data-chopping frequency treatment.

View Article: PubMed Central - PubMed

Affiliation: Experimental and Computational Neurophysiology, Department of Systems Neuroscience, Cajal Institute - Consejo Superior de Investigaciones Científicas Madrid, Spain.

ABSTRACT
Although intracerebral field potential oscillations are commonly used to study information processing during cognition and behavior, the cellular and network processes underlying such events remain unclear. The limited spatial resolution of standard single-point recordings does not clarify whether field oscillations reflect the activity of one or many afferent presynaptic populations. However, multi-site recording devices now provide high-resolution spatial profiles of local field potentials (LFPs) and when coupled to modern mathematical analyses that discriminate signals with distinct but overlapping spatial distributions, they open the door to better understand these potentials. Here we review recent insights that help disentangle certain pathway-specific activities. Accordingly, some oscillatory patterns can now be viewed as a periodic succession of synchronous synaptic currents that reflect the time envelope of spiking activity in given presynaptic populations. These analyses modify our concept of brain rhythms as abstract entities, molding them into mechanistic representations of network activity and allowing us to work in the time domain, reducing the loss of information inherent to data-chopping frequency treatment.

No MeSH data available.


Related in: MedlinePlus

CA3 to CA1 gamma input is a succession of elementary μ-fEPSPs that link pre- and postsynaptic units. (A) Representative example of time courses of LFP generators and firing of a CA3 pyramidal cell. The baseline activity of the Schaffer LFP generator (in blue) is formed by a temporal succession of small wavelets or μ-fEPSP (enlargements at the bottom) in a global gamma pattern exclusive for this input. The presence of occasional sharp-waves (SPWs) is highlighted (in cyan). Autocorrelations (ACF) of the time courses of the generators are shown in the right inset. (B) (1) Fragment of Schaffer-LFP. Note the striking non-overlapping succession of wavelets. (2) The CSD analysis reveals a succession of currents with a spatial distribution matching that of Schaffer evoked potentials and SPWs. (3) The Schaffer-LFP in the wavelet domain. High magnitude (color coded from black to yellow) at given time instant and scale (cyan dots mark maxima) corresponds to the presence of μ-fEPSPs. (4) The width and height of the bar codify the duration and amplitude of detected μ-fEPSPs, respectively. (C) Using the excitatory quanta composing the baseline activity of Schaffer-LFPs (μ-fEPSPs) allows discriminating synaptically connected CA3 and CA1 units. The illustration of point processes in the left represents (from top to bottom) the spike train of a presynaptic CA3 pyramidal cell, the temporal series of μ-fEPSP events and a spike train of a postsynaptic CA1 pyramidal cell. Plausible monosynaptic coincidences are color coded as follows: Type I, green (in-cluster spikes); Type II, blue (Schaffer spikes); Type III, magenta (efficient spike transfer). Examples of these correlations are shown in right insets. (A and B) Modified from Fernández-Ruiz et al. (2012a); (C) modified from Fernández-Ruiz et al. (2012b).
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Figure 2: CA3 to CA1 gamma input is a succession of elementary μ-fEPSPs that link pre- and postsynaptic units. (A) Representative example of time courses of LFP generators and firing of a CA3 pyramidal cell. The baseline activity of the Schaffer LFP generator (in blue) is formed by a temporal succession of small wavelets or μ-fEPSP (enlargements at the bottom) in a global gamma pattern exclusive for this input. The presence of occasional sharp-waves (SPWs) is highlighted (in cyan). Autocorrelations (ACF) of the time courses of the generators are shown in the right inset. (B) (1) Fragment of Schaffer-LFP. Note the striking non-overlapping succession of wavelets. (2) The CSD analysis reveals a succession of currents with a spatial distribution matching that of Schaffer evoked potentials and SPWs. (3) The Schaffer-LFP in the wavelet domain. High magnitude (color coded from black to yellow) at given time instant and scale (cyan dots mark maxima) corresponds to the presence of μ-fEPSPs. (4) The width and height of the bar codify the duration and amplitude of detected μ-fEPSPs, respectively. (C) Using the excitatory quanta composing the baseline activity of Schaffer-LFPs (μ-fEPSPs) allows discriminating synaptically connected CA3 and CA1 units. The illustration of point processes in the left represents (from top to bottom) the spike train of a presynaptic CA3 pyramidal cell, the temporal series of μ-fEPSP events and a spike train of a postsynaptic CA1 pyramidal cell. Plausible monosynaptic coincidences are color coded as follows: Type I, green (in-cluster spikes); Type II, blue (Schaffer spikes); Type III, magenta (efficient spike transfer). Examples of these correlations are shown in right insets. (A and B) Modified from Fernández-Ruiz et al. (2012a); (C) modified from Fernández-Ruiz et al. (2012b).

Mentions: Spike activity of a given presynaptic population elicits postsynaptic currents in target regions that if spatially appropriate, may set rhythmic, irregular, and more commonly, behaviorally modulated periods of different LFP patterns. As a case in point, the CA3 input to CA1 pyramidal cells is responsible for (1) low amplitude steady or (2) theta modulated gamma activity, and (3) isolated hyper-synchronous SPWs (Ylinen et al., 1995; Penttonen et al., 1998; Fernández-Ruiz et al., 2012a). The separation of the Schaffer activity from concomitant inputs allowed a detailed study of its time course. A small LFP epoch is presented in Figure 2 to show the independent activity of three different LFP generators. One is very irregular, while another presents high amplitude slow-waves and the third corresponds to the ongoing Schaffer input. In anesthetized animals, whereas epochs of gamma activity can be found in all LFP generators (Makarov et al., 2010) it only has a steady presence in the Schaffer input. Traditionally, gamma activity in the hippocampus was assumed to be mainly inhibitory (Mann and Paulsen, 2007; Buzsáki and Wang, 2012), in compliance with the observations of interneurons firing at that rate. But in phase firing of units to LFPs does not establish cause or effect, as the LFPs may reflect compound synaptic currents generated by spiking in unrecorded distant neurons. In fact, our findings refuted that view, as the gamma activity in the CA1 Schaffer generator is made up of small wave-like LFP events (~120 μV, ~16 ms long) that were specifically time locked with monosynaptic latency to the spikes of CA3 pyramidal cells but not interneurons. Indeed, the CSD analysis of the disentangled Schaffer-specific LFPs returns gamma sequence of current sinks in the CA1 stratum radiatum with a spatial distribution that tightly matched that of SPW events and CA3-evoked fEPSPs (Figure 2B2). These wavelets were blocked by pharmacologically silencing the CA3 or blockade of glutamate receptors in the CA1. Thus, the gamma rhythm recorded in this stratum of the CA1 region is a periodic succession of micro (μ)-fEPSPs triggered in CA1 pyramidal cells by CA3 assemblies firing in gamma sequence. This is probably the clearest demonstration of the cellular nature of a field oscillation in the intact brain presented to date.


Identifying the synaptic origin of ongoing neuronal oscillations through spatial discrimination of electric fields.

Fernández-Ruiz A, Herreras O - Front Comput Neurosci (2013)

CA3 to CA1 gamma input is a succession of elementary μ-fEPSPs that link pre- and postsynaptic units. (A) Representative example of time courses of LFP generators and firing of a CA3 pyramidal cell. The baseline activity of the Schaffer LFP generator (in blue) is formed by a temporal succession of small wavelets or μ-fEPSP (enlargements at the bottom) in a global gamma pattern exclusive for this input. The presence of occasional sharp-waves (SPWs) is highlighted (in cyan). Autocorrelations (ACF) of the time courses of the generators are shown in the right inset. (B) (1) Fragment of Schaffer-LFP. Note the striking non-overlapping succession of wavelets. (2) The CSD analysis reveals a succession of currents with a spatial distribution matching that of Schaffer evoked potentials and SPWs. (3) The Schaffer-LFP in the wavelet domain. High magnitude (color coded from black to yellow) at given time instant and scale (cyan dots mark maxima) corresponds to the presence of μ-fEPSPs. (4) The width and height of the bar codify the duration and amplitude of detected μ-fEPSPs, respectively. (C) Using the excitatory quanta composing the baseline activity of Schaffer-LFPs (μ-fEPSPs) allows discriminating synaptically connected CA3 and CA1 units. The illustration of point processes in the left represents (from top to bottom) the spike train of a presynaptic CA3 pyramidal cell, the temporal series of μ-fEPSP events and a spike train of a postsynaptic CA1 pyramidal cell. Plausible monosynaptic coincidences are color coded as follows: Type I, green (in-cluster spikes); Type II, blue (Schaffer spikes); Type III, magenta (efficient spike transfer). Examples of these correlations are shown in right insets. (A and B) Modified from Fernández-Ruiz et al. (2012a); (C) modified from Fernández-Ruiz et al. (2012b).
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Related In: Results  -  Collection

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Figure 2: CA3 to CA1 gamma input is a succession of elementary μ-fEPSPs that link pre- and postsynaptic units. (A) Representative example of time courses of LFP generators and firing of a CA3 pyramidal cell. The baseline activity of the Schaffer LFP generator (in blue) is formed by a temporal succession of small wavelets or μ-fEPSP (enlargements at the bottom) in a global gamma pattern exclusive for this input. The presence of occasional sharp-waves (SPWs) is highlighted (in cyan). Autocorrelations (ACF) of the time courses of the generators are shown in the right inset. (B) (1) Fragment of Schaffer-LFP. Note the striking non-overlapping succession of wavelets. (2) The CSD analysis reveals a succession of currents with a spatial distribution matching that of Schaffer evoked potentials and SPWs. (3) The Schaffer-LFP in the wavelet domain. High magnitude (color coded from black to yellow) at given time instant and scale (cyan dots mark maxima) corresponds to the presence of μ-fEPSPs. (4) The width and height of the bar codify the duration and amplitude of detected μ-fEPSPs, respectively. (C) Using the excitatory quanta composing the baseline activity of Schaffer-LFPs (μ-fEPSPs) allows discriminating synaptically connected CA3 and CA1 units. The illustration of point processes in the left represents (from top to bottom) the spike train of a presynaptic CA3 pyramidal cell, the temporal series of μ-fEPSP events and a spike train of a postsynaptic CA1 pyramidal cell. Plausible monosynaptic coincidences are color coded as follows: Type I, green (in-cluster spikes); Type II, blue (Schaffer spikes); Type III, magenta (efficient spike transfer). Examples of these correlations are shown in right insets. (A and B) Modified from Fernández-Ruiz et al. (2012a); (C) modified from Fernández-Ruiz et al. (2012b).
Mentions: Spike activity of a given presynaptic population elicits postsynaptic currents in target regions that if spatially appropriate, may set rhythmic, irregular, and more commonly, behaviorally modulated periods of different LFP patterns. As a case in point, the CA3 input to CA1 pyramidal cells is responsible for (1) low amplitude steady or (2) theta modulated gamma activity, and (3) isolated hyper-synchronous SPWs (Ylinen et al., 1995; Penttonen et al., 1998; Fernández-Ruiz et al., 2012a). The separation of the Schaffer activity from concomitant inputs allowed a detailed study of its time course. A small LFP epoch is presented in Figure 2 to show the independent activity of three different LFP generators. One is very irregular, while another presents high amplitude slow-waves and the third corresponds to the ongoing Schaffer input. In anesthetized animals, whereas epochs of gamma activity can be found in all LFP generators (Makarov et al., 2010) it only has a steady presence in the Schaffer input. Traditionally, gamma activity in the hippocampus was assumed to be mainly inhibitory (Mann and Paulsen, 2007; Buzsáki and Wang, 2012), in compliance with the observations of interneurons firing at that rate. But in phase firing of units to LFPs does not establish cause or effect, as the LFPs may reflect compound synaptic currents generated by spiking in unrecorded distant neurons. In fact, our findings refuted that view, as the gamma activity in the CA1 Schaffer generator is made up of small wave-like LFP events (~120 μV, ~16 ms long) that were specifically time locked with monosynaptic latency to the spikes of CA3 pyramidal cells but not interneurons. Indeed, the CSD analysis of the disentangled Schaffer-specific LFPs returns gamma sequence of current sinks in the CA1 stratum radiatum with a spatial distribution that tightly matched that of SPW events and CA3-evoked fEPSPs (Figure 2B2). These wavelets were blocked by pharmacologically silencing the CA3 or blockade of glutamate receptors in the CA1. Thus, the gamma rhythm recorded in this stratum of the CA1 region is a periodic succession of micro (μ)-fEPSPs triggered in CA1 pyramidal cells by CA3 assemblies firing in gamma sequence. This is probably the clearest demonstration of the cellular nature of a field oscillation in the intact brain presented to date.

Bottom Line: However, multi-site recording devices now provide high-resolution spatial profiles of local field potentials (LFPs) and when coupled to modern mathematical analyses that discriminate signals with distinct but overlapping spatial distributions, they open the door to better understand these potentials.Accordingly, some oscillatory patterns can now be viewed as a periodic succession of synchronous synaptic currents that reflect the time envelope of spiking activity in given presynaptic populations.These analyses modify our concept of brain rhythms as abstract entities, molding them into mechanistic representations of network activity and allowing us to work in the time domain, reducing the loss of information inherent to data-chopping frequency treatment.

View Article: PubMed Central - PubMed

Affiliation: Experimental and Computational Neurophysiology, Department of Systems Neuroscience, Cajal Institute - Consejo Superior de Investigaciones Científicas Madrid, Spain.

ABSTRACT
Although intracerebral field potential oscillations are commonly used to study information processing during cognition and behavior, the cellular and network processes underlying such events remain unclear. The limited spatial resolution of standard single-point recordings does not clarify whether field oscillations reflect the activity of one or many afferent presynaptic populations. However, multi-site recording devices now provide high-resolution spatial profiles of local field potentials (LFPs) and when coupled to modern mathematical analyses that discriminate signals with distinct but overlapping spatial distributions, they open the door to better understand these potentials. Here we review recent insights that help disentangle certain pathway-specific activities. Accordingly, some oscillatory patterns can now be viewed as a periodic succession of synchronous synaptic currents that reflect the time envelope of spiking activity in given presynaptic populations. These analyses modify our concept of brain rhythms as abstract entities, molding them into mechanistic representations of network activity and allowing us to work in the time domain, reducing the loss of information inherent to data-chopping frequency treatment.

No MeSH data available.


Related in: MedlinePlus