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Novel use of matched filtering for synaptic event detection and extraction.

Shi Y, Nenadic Z, Xu X - PLoS ONE (2010)

Bottom Line: This new technique was applied to quantify and compare the EPSCs obtained from excitatory pyramidal cells and fast-spiking interneurons.In addition, our technique has been further applied to the detection and analysis of inhibitory postsynaptic current (IPSC) responses.Given the general purpose of our matched filtering and signal recognition algorithms, we expect that our technique can be appropriately modified and applied to detect and extract other types of electrophysiological and optical imaging signals.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Neurobiology, School of Medicine, University of California Irvine, Irvine, California, USA.

ABSTRACT
Efficient and dependable methods for detection and measurement of synaptic events are important for studies of synaptic physiology and neuronal circuit connectivity. As the published methods with detection algorithms based upon amplitude thresholding and fixed or scaled template comparisons are of limited utility for detection of signals with variable amplitudes and superimposed events that have complex waveforms, previous techniques are not applicable for detection of evoked synaptic events in photostimulation and other similar experimental situations. Here we report on a novel technique that combines the design of a bank of approximate matched filters with the detection and estimation theory to automatically detect and extract photostimluation-evoked excitatory postsynaptic currents (EPSCs) from individually recorded neurons in cortical circuit mapping experiments. The sensitivity and specificity of the method were evaluated on both simulated and experimental data, with its performance comparable to that of visual event detection performed by human operators. This new technique was applied to quantify and compare the EPSCs obtained from excitatory pyramidal cells and fast-spiking interneurons. In addition, our technique has been further applied to the detection and analysis of inhibitory postsynaptic current (IPSC) responses. Given the general purpose of our matched filtering and signal recognition algorithms, we expect that our technique can be appropriately modified and applied to detect and extract other types of electrophysiological and optical imaging signals.

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Laser scanning photostimulation combined with whole cell recordings to map local circuit input to an excitatory pyramidal neuron.A shows a mouse prefrontal cortical slice image with the superimposed photostimulation sites (16×16 cyan stars, spaced at 60 µm×100 µm) across all the cortical layers 1, 2, 3, 5 and 6 (i.e., L1–L6). Note that the prefrontal cortex lacks granular layer 4 found in primary sensory cortex. The glass electrode was recording from an excitatory pyramidal neuron (shown with a scaled reconstruction with major dendrites) in upper layer 5 of the prelimbic area in prefrontal cortex. M denotes medial, and V denotes ventral. B shows an array of photostimulation-evoked response traces from most locations shown in A, with the cell held at −70 mV in voltage clamp mode to detect inward excitatory synaptic currents (EPSCs). The red circle indicates the cell body location. Only the 200 ms of the recorded traces after the onset of laser photostimulation (1 ms, 25 mW) are shown. Different forms of photostimulation responses are illustrated by the traces of 1, 2, 3 and 4, which are expanded and separately shown in C. Trace 1 is an example of the direct response (shown in red) to glutamate uncaging on the cell body. Trace 2 is a typical example of synaptic input responses (blue). Trace 3 shows synaptic responses (blue) over-riding on the relatively small direct response (red) evoked from the cell's proximal dendrites. Trace 4 is another form of direct response (red) evoked from apical dendrites. D shows the pyramidal cell's intrinsic firing pattern with its voltage response traces to current injections at amplitudes of -50, 100, 150 and 200 pA, respectively.
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pone-0015517-g001: Laser scanning photostimulation combined with whole cell recordings to map local circuit input to an excitatory pyramidal neuron.A shows a mouse prefrontal cortical slice image with the superimposed photostimulation sites (16×16 cyan stars, spaced at 60 µm×100 µm) across all the cortical layers 1, 2, 3, 5 and 6 (i.e., L1–L6). Note that the prefrontal cortex lacks granular layer 4 found in primary sensory cortex. The glass electrode was recording from an excitatory pyramidal neuron (shown with a scaled reconstruction with major dendrites) in upper layer 5 of the prelimbic area in prefrontal cortex. M denotes medial, and V denotes ventral. B shows an array of photostimulation-evoked response traces from most locations shown in A, with the cell held at −70 mV in voltage clamp mode to detect inward excitatory synaptic currents (EPSCs). The red circle indicates the cell body location. Only the 200 ms of the recorded traces after the onset of laser photostimulation (1 ms, 25 mW) are shown. Different forms of photostimulation responses are illustrated by the traces of 1, 2, 3 and 4, which are expanded and separately shown in C. Trace 1 is an example of the direct response (shown in red) to glutamate uncaging on the cell body. Trace 2 is a typical example of synaptic input responses (blue). Trace 3 shows synaptic responses (blue) over-riding on the relatively small direct response (red) evoked from the cell's proximal dendrites. Trace 4 is another form of direct response (red) evoked from apical dendrites. D shows the pyramidal cell's intrinsic firing pattern with its voltage response traces to current injections at amplitudes of -50, 100, 150 and 200 pA, respectively.

Mentions: Overall, photostimulation-evoked EPSCs represent a range of complex synaptic events that may be encountered in other studies of synaptic connections using focal electrical stimulation and dual or multiple intracellular recordings in highly localized circuits formed by neurons of high connection probabilities [13], [24], [25]. As illustrated in Figure 1, photostimulation can induce two major forms of excitatory responses: (1) direct glutamate uncaging responses (direct activation of the recorded neuron's glutamate receptors); and (2) synaptically mediated responses (EPSCs) resulting from the suprathreshold activation of presynaptic excitatory neurons. Responses within the 10 ms window from laser onset were considered direct, as they had a distinct shape (longer rise time) and occurred immediately after glutamate uncaging (shorter latency) (Figure 1C). Synaptic currents with such short latencies are not possible because they would have to occur before the generation of action potentials in photostimulated neurons [2], [7], [8], [16]. Therefore, direct responses need to be excluded from local synaptic input analysis. However, at some locations, synaptic responses were over-riding on the relatively small direct responses and they needed to be identified and included in synaptic input analysis (Figure 1C). Detection and extraction of this type of synaptic events actually presents a major challenge for automatic signal detection and extraction using algorithms in previously published techniques. In addition, synaptically-mediated responses have varying amplitudes and frequencies with overlapping EPSC events.


Novel use of matched filtering for synaptic event detection and extraction.

Shi Y, Nenadic Z, Xu X - PLoS ONE (2010)

Laser scanning photostimulation combined with whole cell recordings to map local circuit input to an excitatory pyramidal neuron.A shows a mouse prefrontal cortical slice image with the superimposed photostimulation sites (16×16 cyan stars, spaced at 60 µm×100 µm) across all the cortical layers 1, 2, 3, 5 and 6 (i.e., L1–L6). Note that the prefrontal cortex lacks granular layer 4 found in primary sensory cortex. The glass electrode was recording from an excitatory pyramidal neuron (shown with a scaled reconstruction with major dendrites) in upper layer 5 of the prelimbic area in prefrontal cortex. M denotes medial, and V denotes ventral. B shows an array of photostimulation-evoked response traces from most locations shown in A, with the cell held at −70 mV in voltage clamp mode to detect inward excitatory synaptic currents (EPSCs). The red circle indicates the cell body location. Only the 200 ms of the recorded traces after the onset of laser photostimulation (1 ms, 25 mW) are shown. Different forms of photostimulation responses are illustrated by the traces of 1, 2, 3 and 4, which are expanded and separately shown in C. Trace 1 is an example of the direct response (shown in red) to glutamate uncaging on the cell body. Trace 2 is a typical example of synaptic input responses (blue). Trace 3 shows synaptic responses (blue) over-riding on the relatively small direct response (red) evoked from the cell's proximal dendrites. Trace 4 is another form of direct response (red) evoked from apical dendrites. D shows the pyramidal cell's intrinsic firing pattern with its voltage response traces to current injections at amplitudes of -50, 100, 150 and 200 pA, respectively.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2991367&req=5

pone-0015517-g001: Laser scanning photostimulation combined with whole cell recordings to map local circuit input to an excitatory pyramidal neuron.A shows a mouse prefrontal cortical slice image with the superimposed photostimulation sites (16×16 cyan stars, spaced at 60 µm×100 µm) across all the cortical layers 1, 2, 3, 5 and 6 (i.e., L1–L6). Note that the prefrontal cortex lacks granular layer 4 found in primary sensory cortex. The glass electrode was recording from an excitatory pyramidal neuron (shown with a scaled reconstruction with major dendrites) in upper layer 5 of the prelimbic area in prefrontal cortex. M denotes medial, and V denotes ventral. B shows an array of photostimulation-evoked response traces from most locations shown in A, with the cell held at −70 mV in voltage clamp mode to detect inward excitatory synaptic currents (EPSCs). The red circle indicates the cell body location. Only the 200 ms of the recorded traces after the onset of laser photostimulation (1 ms, 25 mW) are shown. Different forms of photostimulation responses are illustrated by the traces of 1, 2, 3 and 4, which are expanded and separately shown in C. Trace 1 is an example of the direct response (shown in red) to glutamate uncaging on the cell body. Trace 2 is a typical example of synaptic input responses (blue). Trace 3 shows synaptic responses (blue) over-riding on the relatively small direct response (red) evoked from the cell's proximal dendrites. Trace 4 is another form of direct response (red) evoked from apical dendrites. D shows the pyramidal cell's intrinsic firing pattern with its voltage response traces to current injections at amplitudes of -50, 100, 150 and 200 pA, respectively.
Mentions: Overall, photostimulation-evoked EPSCs represent a range of complex synaptic events that may be encountered in other studies of synaptic connections using focal electrical stimulation and dual or multiple intracellular recordings in highly localized circuits formed by neurons of high connection probabilities [13], [24], [25]. As illustrated in Figure 1, photostimulation can induce two major forms of excitatory responses: (1) direct glutamate uncaging responses (direct activation of the recorded neuron's glutamate receptors); and (2) synaptically mediated responses (EPSCs) resulting from the suprathreshold activation of presynaptic excitatory neurons. Responses within the 10 ms window from laser onset were considered direct, as they had a distinct shape (longer rise time) and occurred immediately after glutamate uncaging (shorter latency) (Figure 1C). Synaptic currents with such short latencies are not possible because they would have to occur before the generation of action potentials in photostimulated neurons [2], [7], [8], [16]. Therefore, direct responses need to be excluded from local synaptic input analysis. However, at some locations, synaptic responses were over-riding on the relatively small direct responses and they needed to be identified and included in synaptic input analysis (Figure 1C). Detection and extraction of this type of synaptic events actually presents a major challenge for automatic signal detection and extraction using algorithms in previously published techniques. In addition, synaptically-mediated responses have varying amplitudes and frequencies with overlapping EPSC events.

Bottom Line: This new technique was applied to quantify and compare the EPSCs obtained from excitatory pyramidal cells and fast-spiking interneurons.In addition, our technique has been further applied to the detection and analysis of inhibitory postsynaptic current (IPSC) responses.Given the general purpose of our matched filtering and signal recognition algorithms, we expect that our technique can be appropriately modified and applied to detect and extract other types of electrophysiological and optical imaging signals.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Neurobiology, School of Medicine, University of California Irvine, Irvine, California, USA.

ABSTRACT
Efficient and dependable methods for detection and measurement of synaptic events are important for studies of synaptic physiology and neuronal circuit connectivity. As the published methods with detection algorithms based upon amplitude thresholding and fixed or scaled template comparisons are of limited utility for detection of signals with variable amplitudes and superimposed events that have complex waveforms, previous techniques are not applicable for detection of evoked synaptic events in photostimulation and other similar experimental situations. Here we report on a novel technique that combines the design of a bank of approximate matched filters with the detection and estimation theory to automatically detect and extract photostimluation-evoked excitatory postsynaptic currents (EPSCs) from individually recorded neurons in cortical circuit mapping experiments. The sensitivity and specificity of the method were evaluated on both simulated and experimental data, with its performance comparable to that of visual event detection performed by human operators. This new technique was applied to quantify and compare the EPSCs obtained from excitatory pyramidal cells and fast-spiking interneurons. In addition, our technique has been further applied to the detection and analysis of inhibitory postsynaptic current (IPSC) responses. Given the general purpose of our matched filtering and signal recognition algorithms, we expect that our technique can be appropriately modified and applied to detect and extract other types of electrophysiological and optical imaging signals.

Show MeSH