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1.  Rapid mapping of visual receptive fields by filtered back projection: application to multi-neuronal electrophysiology and imaging 
The Journal of Physiology  2014;592(Pt 22):4839-4854.
Neurons in the visual system vary widely in the spatiotemporal properties of their receptive fields (RFs), and understanding these variations is key to elucidating how visual information is processed. We present a new approach for mapping RFs based on the filtered back projection (FBP), an algorithm used for tomographic reconstructions. To estimate RFs, a series of bars were flashed across the retina at pseudo-random positions and at a minimum of five orientations. We apply this method to retinal neurons and show that it can accurately recover the spatial RF and impulse response of ganglion cells recorded on a multi-electrode array. We also demonstrate its utility for in vivo imaging by mapping the RFs of an array of bipolar cell synapses expressing a genetically encoded Ca2+ indicator. We find that FBP offers several advantages over the commonly used spike-triggered average (STA): (i) ON and OFF components of a RF can be separated; (ii) the impulse response can be reconstructed at sample rates of 125 Hz, rather than the refresh rate of a monitor; (iii) FBP reveals the response properties of neurons that are not evident using STA, including those that display orientation selectivity, or fire at low mean spike rates; and (iv) the FBP method is fast, allowing the RFs of all the bipolar cell synaptic terminals in a field of view to be reconstructed in under 4 min. Use of the FBP will benefit investigations of the visual system that employ electrophysiology or optical reporters to measure activity across populations of neurons.
doi:10.1113/jphysiol.2014.276642
PMCID: PMC4259530  PMID: 25172952
2.  Rapid mapping of visual receptive fields by filtered back projection: application to multi-neuronal electrophysiology and imaging 
The Journal of Physiology  2014;592(22):4839-4854.
Key points
To understand vision, we must measure the spatio-temporal receptive field of neurons in the visual system. We describe how the filtered back projection can be used to map the receptive fields of many neurons simultaneously, within a few minutes. This method can also reveal complex features of visual receptive fields such as the tuning of orientation selective neurons and the contributions from separate ON and OFF components. We demonstrate that the filtered back projection is suited to mapping receptive fields from populations of neurons recorded with imaging or electrophysiology and should therefore prove useful for investigations of visual processing throughout the visual pathway.
Abstract
Neurons in the visual system vary widely in the spatiotemporal properties of their receptive fields (RFs), and understanding these variations is key to elucidating how visual information is processed. We present a new approach for mapping RFs based on the filtered back projection (FBP), an algorithm used for tomographic reconstructions. To estimate RFs, a series of bars were flashed across the retina at pseudo-random positions and at a minimum of five orientations. We apply this method to retinal neurons and show that it can accurately recover the spatial RF and impulse response of ganglion cells recorded on a multi-electrode array. We also demonstrate its utility for in vivo imaging by mapping the RFs of an array of bipolar cell synapses expressing a genetically encoded Ca2+ indicator. We find that FBP offers several advantages over the commonly used spike-triggered average (STA): (i) ON and OFF components of a RF can be separated; (ii) the impulse response can be reconstructed at sample rates of 125 Hz, rather than the refresh rate of a monitor; (iii) FBP reveals the response properties of neurons that are not evident using STA, including those that display orientation selectivity, or fire at low mean spike rates; and (iv) the FBP method is fast, allowing the RFs of all the bipolar cell synaptic terminals in a field of view to be reconstructed in under 4 min. Use of the FBP will benefit investigations of the visual system that employ electrophysiology or optical reporters to measure activity across populations of neurons.
doi:10.1113/jphysiol.2014.276642
PMCID: PMC4259530  PMID: 25172952
3.  A Synaptic Mechanism for Temporal Filtering of Visual Signals 
PLoS Biology  2014;12(10):e1001972.
Synaptic volume matters! The size of the presynaptic compartment of retinal bipolar cells controls the amplitude, speed, and adaptation of synaptic transmission.
The visual system transmits information about fast and slow changes in light intensity through separate neural pathways. We used in vivo imaging to investigate how bipolar cells transmit these signals to the inner retina. We found that the volume of the synaptic terminal is an intrinsic property that contributes to different temporal filters. Individual cells transmit through multiple terminals varying in size, but smaller terminals generate faster and larger calcium transients to trigger vesicle release with higher initial gain, followed by more profound adaptation. Smaller terminals transmitted higher stimulus frequencies more effectively. Modeling global calcium dynamics triggering vesicle release indicated that variations in the volume of presynaptic compartments contribute directly to all these differences in response dynamics. These results indicate how one neuron can transmit different temporal components in the visual signal through synaptic terminals of varying geometries with different adaptational properties.
Author Summary
The process of neurotransmission involves the conversion of electrical signals into the release of a chemical neurotransmitter from the neurons synaptic terminal, and the key trigger for this release is a rise in calcium concentration. Accordingly, the amplitude and speed of this calcium signal controls the amplitude and time-course of synaptic communication. Working on the synaptic terminals of fish retinal bipolar cells, we show that the presynaptic calcium signal and the subsequent neurotransmitter release are shaped by the basic property of synapse volume. Using a combination of experimental approaches and computational models, we found that large synapses are slow and adapt little during ongoing stimulation, while small synapses are fast and show more profound adaptation. This observation leads to a second key concept: since neurons usually have several presynaptic terminals that may vary in volume, a single neuron can, in principle, forward different synaptic signals to different postsynaptic partners. We provide direct evidence that this is the case for bipolar cells of the fish retina.
doi:10.1371/journal.pbio.1001972
PMCID: PMC4205119  PMID: 25333637
5.  Olfactory Stimulation Selectively Modulates the OFF Pathway in the Retina of Zebrafish 
Neuron  2013;79(1):97-110.
Summary
Cross-modal regulation of visual performance by olfactory stimuli begins in the retina, where dopaminergic interneurons receive projections from the olfactory bulb. However, we do not understand how olfactory stimuli alter the processing of visual signals within the retina. We investigated this question by in vivo imaging activity in transgenic zebrafish expressing SyGCaMP2 in bipolar cell terminals and GCaMP3.5 in ganglion cells. The food-related amino acid methionine reduced the gain and increased sensitivity of responses to luminance and contrast transmitted through OFF bipolar cells but not ON. The effects of olfactory stimulus were blocked by inhibiting dopamine uptake and release. Activation of dopamine receptors increased the gain of synaptic transmission in vivo and potentiated synaptic calcium currents in isolated bipolar cells. These results indicate that olfactory stimuli alter the sensitivity of the retina through the dopaminergic regulation of presynaptic calcium channels that control the gain of synaptic transmission through OFF bipolar cells.
Highlights
•Olfactory stimuli regulate transmission of signals through retinal bipolar cells•Modulation of synaptic gain and sensitivity occur in OFF bipolar cells but not ON•An inhibitor of dopamine uptake blocks odor-induced changes in synaptic gain•Dopamine potentiates presynaptic calcium channels in isolated bipolar cells
Esposti et al. show that olfactory stimulation selectively modulates synaptic transmission from retinal OFF bipolar cells in zebrafish. Dopamine plays a key role in this cross modal interaction by acting on the presynaptic calcium channels.
doi:10.1016/j.neuron.2013.05.001
PMCID: PMC3710973  PMID: 23849198
6.  Optimization of a GCaMP calcium indicator for neural activity imaging 
Genetically encoded calcium indicators (GECIs) are powerful tools for systems neuroscience. Recent efforts in protein engineering have significantly increased the performance of GECIs. The state-of-the art single-wavelength GECI, GCaMP3, has been deployed in a number of model organisms and can reliably detect three or more action potentials (APs) in short bursts in several systems in vivo. Through protein structure determination, targeted mutagenesis, high-throughput screening, and a battery of in vitro assays, we have increased the dynamic range of GCaMP3 by several-fold, creating a family of “GCaMP5” sensors. We tested GCaMP5s in several systems: cultured neurons and astrocytes, mouse retina, and in vivo in Caenorhabditis chemosensory neurons, Drosophila larval neuromuscular junction and adult antennal lobe, zebrafish retina and tectum, and mouse visual cortex. Signal-to-noise ratio was improved by at least 2–3-fold. In the visual cortex, two GCaMP5 variants detected twice as many visual stimulus-responsive cells as GCaMP3. By combining in vivo imaging with electrophysiology we show that GCaMP5 fluorescence provides a more reliable measure of neuronal activity than its predecessor GCaMP3. GCaMP5 allows more sensitive detection of neural activity in vivo and may find widespread applications for cellular imaging in general.
doi:10.1523/JNEUROSCI.2601-12.2012
PMCID: PMC3482105  PMID: 23035093
GCaMP5; GCaMP3; GECI; genetically encoded calcium indicator; functional imaging
7.  In vivo evidence that retinal bipolar cells generate spikes modulated by light 
Nature neuroscience  2011;14(8):951-952.
Retinal bipolar cells have been assumed to generate purely graded responses to light. To test this idea we imaged the presynaptic calcium transient in live zebrafish. We found that ON, OFF, transient and sustained bipolar cells are all capable of generating fast “all-or-none” calcium transients modulated by visual stimulation.
doi:10.1038/nn.2841
PMCID: PMC3232443  PMID: 21706020
8.  Spikes in Retinal Bipolar Cells Phase-Lock to Visual Stimuli with Millisecond Precision 
Current Biology  2011;21(22):1859-1869.
Summary
Background
The conversion of an analog stimulus into the digital form of spikes is a fundamental step in encoding sensory information. Here, we investigate this transformation in the visual system of fish by in vivo calcium imaging and electrophysiology of retinal bipolar cells, which have been assumed to be purely graded neurons.
Results
Synapses of all major classes of retinal bipolar cell encode visual information by using a combination of spikes and graded signals. Spikes are triggered within the synaptic terminal and, although sparse, phase-lock to a stimulus with a jitter as low as 2–3 ms. Spikes in bipolar cells encode a visual stimulus less reliably than spikes in ganglion cells but with similar temporal precision. The spike-generating mechanism does not alter the temporal filtering of a stimulus compared with the generator potential. The amplitude of the graded component of the presynaptic calcium signal can vary in time, and small fluctuations in resting membrane potential alter spike frequency and even switch spiking on and off.
Conclusions
In the retina of fish, the millisecond precision of spike coding begins in the synaptic terminal of bipolar cells. This neural compartment regulates the frequency of digital signals transmitted to the inner retina as well as the strength of graded signals.
Graphical Abstract
Highlights
► The spike code of vision begins in retinal bipolar cells ► Spikes in bipolar cells phase-lock to visual stimuli with millisecond precision ► Spiking and graded calcium signals can switch on and off at individual synapses ► Spikes in bipolar cells encode a stimulus less reliably than spikes in ganglion cells
doi:10.1016/j.cub.2011.09.042
PMCID: PMC3235547  PMID: 22055291

Results 1-8 (8)