Network Adaptation Improves Temporal Representation of Naturalistic Stimuli in Drosophila Eye: II Mechanisms
Publication Date
January 30, 2009
Anton Nikolaev, Lei Zheng, Trevor J. Wardill, Cahir J. O'kane, et al
Publisher URL
PubMed Central
Europe PMC
Web of Science
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  • {"files"=>[""], "description"=>"<p>A. Mean frequency spectra of seven <i>ort<sup>6</sup></i> photoreceptors (left) and a representative LMC (right) to dim, middle and bright naturalistic stimuli (NS). Inset shows the normalized LMC frequency spectra. B. Synaptic gain is the highest with bright stimulation. Corresponding WT synaptic gain (dotted lines) is given for comparison, from <a href=\"\" target=\"_blank\">[4]</a>. C. Changes in <i>ort<sup>6</sup></i> photoreceptor (left) and LMC (right) frequency spectra for 20 seconds of repeated bright stimulation. The 1<sup>st</sup> (black), 2<sup>nd</sup> (red) and 20<sup>th</sup> (green) frequency spectra, respectively. D. The frequency range of <i>ort<sup>6</sup></i> synaptic gain, dominated by high frequencies, spreads only marginally over time in comparison to the average WT Oregon-R synaptic gain (dotted lines) for the same experiment <a href=\"\" target=\"_blank\">[4]</a>. Error bars are SDs.</p>", "links"=>[], "tags"=>["r-lmc-r", "lacks", "adaptational", "enhancement"], "article_id"=>579866, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"", "title"=>"The <i>ort<sup>6</sup></i> R-LMC-R system lacks adaptational enhancement of low frequency signals.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 02:44:26"}
  • {"files"=>[""], "description"=>"<p>Statistical characterization of adaptive trends is for 4-days-old <i>L2-shi<sup>TS1</sup></i>, WT and control flies (<i>UAS-shi<sup>TS1</sup></i>; <i>L2-Gal4</i>), all having Canton-S (<i>CS</i>) red genetic association. The recordings are at 19°C (blue) and 30°C (orange). A. Typical high-quality voltage response of a LMC to a bright repetitive naturalistic stimulation (NS) at 19°C. This data is from a <i>UAS-shi<sup>TS1</sup></i> fly. Sensitivity, <i>i.e.</i> change in LMC output (gray circles) is defined as the mean of the standard deviations of consecutive response segments to a second long naturalistic stimulus (NS) pattern, from the 2<sup>nd</sup> to 20<sup>th</sup> s (dotted box, each data point is calculated from 800-ms data sections as in <a href=\"\" target=\"_blank\">Fig. 2</a>). This change is then plotted as a percentage, in respect to the 1<sup>st</sup> response, showing 75% increase in the LMC output in 20 seconds. B. Voltage response of the same LMC, but at 30°C. Notice the faster adapting trend. LMC output increases 30% in 3 seconds before settling to 10%, due to faster bioreactions at the higher temperature <a href=\"\" target=\"_blank\">[18]</a>. Accordingly, the voltage responses at 30°C are often smaller than at 19°C. C–F. Changes in the mean LMC output of all recordings (with adequate stability) plotted against their maximum responses at 19°C (left) and at 30°C (right) for different flies as probability distributions. The left hemi-field indicates decaying and the right increasing LMC output. The fits show the mean correspondence between the adapting trends and maximum responses. At 19°C, the fits lie to the right, <i>i.e.</i> the larger the response the larger is its adaptational boosting over the duration of the recording. C. WT Canton-S LMC output is boosted in 33/36 recordings (92%) at 19°C and 27/34 recordings (79%) at 30°C. D. <i>L2-shi<sup>TS1</sup></i> LMC output is boosted in 21/27 recordings (78%) at 19°C, but only 6/29 recordings (21%) show a small increase at 30°C (when L2-R-feedback is reduced). These population means differ significantly (p = 0.00004, ANOVA, one-way Bonferoni test). Thus, LMC output of <i>L2-shi<sup>TS1</sup></i> decreases at 30°C (gray highlight), in contrast to all other genotypes that show an increase over time. E. <i>UAS-shi<sup>TS1</sup></i> LMC output is boosted 11/14 recordings (78%) at 19°C and 20/27 recording (74%). F. <i>GAL4-L2</i> LMC output is boosted in 25/33 recordings (76%) at 19°C and 25/27 recordings (93%) at 30°C.</p>", "links"=>[], "tags"=>["controls", "shows", "adaptation", "lmc", "dampened", "reducing", "l2-r"], "article_id"=>580040, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"", "title"=>"Genetic controls shows that adaptation in LMC output is dampened by reducing L2-R feedback.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:00:40"}
  • {"files"=>[""], "description"=>"<p>Throughput of the feedforward pathway from R1–R6 photoreceptors to LMCs is compromised by ort<sup>6</sup> receptors, which reduce histamine sensitivity by >10-fold <a href=\"\" target=\"_blank\">[8]</a>. A. Voltage responses of <i>ort<sup>6</sup></i> photoreceptors (mean±SD, gray, n = 7) and a representative LMC to a second long naturalistic stimulus (NS), during the first stimulus repetitions at different luminance levels at 25°C. B. The corresponding probability density functions (PDFs) for R1–R6s (top) and LMCs (left) and the joint probability density functions of the first 20 responses. In contour plots of jPDFs, hot colors denote high probability. The jPDFs quantify the input-output transformations, characterizing the synaptic gain for the given luminance of stimulation. The most probable synaptic gain, <i>i.e.</i> the slopes of the white lines, is quite invariable. C. The photoreceptor and LMC PDFs and jPDFs shown at the 1<sup>st</sup>, 2<sup>nd</sup> and 20<sup>th</sup> s of bright stimulation. Note that the synaptic gain (white lines) varies little over time unlike in the WT system <a href=\"\" target=\"_blank\">[4]</a>. D. The normalized responses of <i>ort<sup>6</sup></i> (blue) and WT Oregon-R LMCs (black) to dim (thin traces) and bright stimuli (thick traces). Ort<sup>6</sup> receptors mimic extreme “light adaptation”, making the speed (time course) of the LMC output invariable at different intensities. E. High resolution PDFs of photoreceptor (left) and LMC (right) outputs shown at different times during bright stimulation. The PDFs of <i>ort<sup>6</sup></i> photoreceptors show a gradual compression in voltage range, whilst the PDFs of <i>ort<sup>6</sup></i> LMCs remain unchanged after the first second of stimulation. F. The SDs of voltage responses indicate that the adaptive trends in the photoreceptor or LMC outputs are quite similar for each luminance level. Thus, sensitivity of these cells either remains the same or reduces gradually during repetitive stimulation, unlike in WT LMCs, in which the sensitivity increases over stimulation <a href=\"\" target=\"_blank\">[4]</a>. WT LMC output has an increasing trend, similar to <a href=\"\" target=\"_blank\">Fig. 1C</a>. SDs are from the boxed data (201–1000 ms) in A.</p>", "links"=>[], "tags"=>["r-lmc-r", "adaptation", "naturalistic", "stimuli"], "article_id"=>579750, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"", "title"=>"The <i>ort<sup>6</sup></i> R-LMC-R system show limited adaptation to naturalistic stimuli (NS).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 02:42:30"}
  • {"files"=>[""], "description"=>"<p>A. R1–R6 photoreceptor and B LMC mean frequency spectra for the 1<sup>st</sup> (left), 2<sup>nd</sup> (middle) and 20<sup>th</sup> (right) voltage response of <i>L2-shi<sup>TS1</sup></i> (blue, orange, green) and WT Canton-S (gray) flies at 30°C. The recordings show mean±SEM (photoreceptors: n = 7–9, LMCs: n = 5–12). C. The relative difference in the frequency spectra between WT and <i>L2-shi<sup>TS1</sup></i> LMC (gray areas) and photoreceptors (transparent areas under dotted lines). L2-R feedback “whitens” and extends the frequency range of LMCs over time by boosting mostly high-frequency signals (50–100 Hz). D–E. The panels show the mean±SEM of the relative differences in C for R1–R6 and LMCs, respectively, at 19°C (white) and 30°C (gray). Gray bars differ significantly from white bars in all comparisons. L2-R feedback increases photoreceptor and LMC output by ∼15% and ∼40%, respectively, over time.</p>", "links"=>[], "tags"=>["acting", "l2-r", "helps", "lmc"], "article_id"=>580244, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"", "title"=>"Adaptation acting through L2-R feedback helps to “whiten” LMC output.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:04:04"}
  • {"files"=>[""], "description"=>"<p>At this permissive temperature, photoreceptor and LMC outputs to a repeated naturalistic stimulation (NS) in <i>L2-shi<sup>TS1</sup></i> cells are similar to the corresponding outputs of WT Canton-S cells. A. The 1<sup>st</sup>, 2<sup>nd</sup> and 20<sup>th</sup> voltage responses of R1–R6 photoreceptors (mean±SD, gray, n = 6, above) and LMCs (mean±SD, gray, n = 6, below) to middle intensity stimulation. B. The corresponding photoreceptor and LMC PDFs and jPDFs during bright stimulation. The most probable synaptic gain (the slope of white lines) increases over time, similar to WT <a href=\"\" target=\"_blank\">[4]</a>. C. The adaptive trends of photoreceptor (left) and LMC (right) output, measured as SD the boxed data in A (201–1000 ms) to repeated stimulation. Adaptation dynamics are similar in the <i>L2-shi<sup>TS1</sup></i> (black) and WT (gray) R-LMC-R systems.</p>", "links"=>[], "tags"=>["happens", "r-lmc-r"], "article_id"=>579953, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"", "title"=>"Adaptation happens normally in the <i>L2-shi<sup>TS1</sup></i> R-LMC-R system at 19°C.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 02:45:53"}
  • {"files"=>[""], "description"=>"<p>A–B. The panels show the signal-to-noise ratio in <i>L2-shi<sup>TS1</sup></i> (blue) and WT (black) photoreceptors and LMCs, respectively, to the same middle intensity naturalistic stimulation (NS) at 19°C (permissive temperature). C–D. The panels show the signal-to-noise ratio in <i>L2-shi<sup>TS1</sup></i> (red) and WT (black) photoreceptors and LMC, respectively, to the same stimulus at 30°C (restrictive temperature). Notice that the signal-to-noise ratio of <i>L2-shi<sup>TS1</sup></i> LMCs collapses at the restrictive temperature. Notice also that <i>L2-Gal4</i> and <i>UAS-shi<sup>TS1</sup></i> LMCs have similar signal-to-noise ratios to WT LMCs, indicating that Gal4 and the UAS lines themselves did not influence signaling performance of the R-LMC-R system. Mean±SEM are shown, n is the number of cells in each group.</p>", "links"=>[], "tags"=>["improves", "signal-to-noise", "lmc"], "article_id"=>580354, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"", "title"=>"L2-R feedback improves the signal-to-noise ratio (SNR) of LMC output.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:05:54"}
  • {"files"=>[""], "description"=>"<div><p>Retinal networks must adapt constantly to best present the ever changing visual world to the brain. Here we test the hypothesis that adaptation is a result of different mechanisms at several synaptic connections within the network. In a companion paper (Part I), we showed that adaptation in the photoreceptors (R1–R6) and large monopolar cells (LMC) of the <em>Drosophila</em> eye improves sensitivity to under-represented signals in seconds by enhancing both the amplitude and frequency distribution of LMCs' voltage responses to repeated naturalistic contrast series. In this paper, we show that such adaptation needs both the light-mediated conductance and feedback-mediated synaptic conductance. A faulty feedforward pathway in histamine receptor mutant flies speeds up the LMC output, mimicking extreme light adaptation. A faulty feedback pathway from L2 LMCs to photoreceptors slows down the LMC output, mimicking dark adaptation. These results underline the importance of network adaptation for efficient coding, and as a mechanism for selectively regulating the size and speed of signals in neurons. We suggest that concert action of many different mechanisms and neural connections are responsible for adaptation to visual stimuli. Further, our results demonstrate the need for detailed circuit reconstructions like that of the <em>Drosophila</em> lamina, to understand how networks process information.</p></div>", "links"=>[], "tags"=>["adaptation", "improves", "temporal", "naturalistic", "stimuli", "ii", "mechanisms"], "article_id"=>148655, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"", "title"=>"Network Adaptation Improves Temporal Representation of Naturalistic Stimuli in <em>Drosophila</em> Eye: II Mechanisms", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 02:24:15"}
  • {"files"=>[""], "description"=>"<p>In the WT R-LMC-R system (top), LMC output increases with naturalistic stimulus (NS) repetitions by network adaptation (increasing sensitivity) set by a dynamic equilibrium between light-mediated conductance and feedback-mediated synaptic conductances. In the <i>ort<sup>6</sup></i> R-LMC-R system (middle), mutated ort<sup>6</sup> histamine receptors act as a strict high-pass filter <a href=\"\" target=\"_blank\">[8]</a>, reducing throughput of the feedforward pathway and depolarizing LMCs and AC. This amplifies the feedback connections to photoreceptors, pushing the dynamic equilibrium toward extreme “light adaptation” in all luminance levels. Thus, LMC output contains predominantly high-frequency signals and cannot be improved over time (decreasing sensitivity). In the <i>L2-shi<sup>TS1</sup></i> R-LMC-R system at 30°C (bottom), L2-R feedback is reduced and the dynamic equilibrium shifts toward dark adaptation. As less information is returning to photoreceptors, their output is modified less efficiently and the LMC output desensitizes, tracking mostly the photoreceptor adaptation (decreasing sensitivity).</p>", "links"=>[], "tags"=>["pathways", "components"], "article_id"=>580444, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"", "title"=>"Feedforward and feedback pathways are necessary components for network adaptation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:07:24"}
  • {"files"=>[""], "description"=>"<p>At this restrictive temperature, <i>Shibire<sup>TS1</sup></i>-proteins should block endocytosis <a href=\"\" target=\"_blank\">[16]</a> in L2s, reducing their feedback to R1–R6 photoreceptors in <i>L2-shi<sup>TS1</sup></i> flies. A. The 1<sup>st</sup>, 2<sup>nd</sup> and 20<sup>th</sup> voltage responses of R1–R6 photoreceptors (mean±SD, gray, n = 6, above) and LMCs (mean±SD, gray, n = 4, below) to middle intensity naturalistic stimulation (NS) at 30°C (light yellow panels). The responses are somewhat smaller than at 19°C, <i>cf. </i><a href=\"\" target=\"_blank\">Fig. 4A</a>. B. The corresponding probability density functions, PDFs, and joint probability density functions, jPDFs, during bright stimulation at 30°C. The most probable synaptic gain (white lines) remains invariable over time. C. SD of photoreceptor (left) and LMC (right) output at different times to repeated stimulation at 30°C. The <i>L2-shi<sup>TS1</sup></i> photoreceptor and LMC outputs lack the adaptational boosting of WT controls (gray). D. The difference: 100*[WT(output)-<i>L2-shi<sup>TS1</sup></i>(output)]/ <i>L2-shi<sup>TS1</sup></i>(output) in restrictive temperature (30°C, red) is calculated for 19°C and 30°C data separately. At 30°C, L2-R feedback in <i>L2-shi<sup>TS1</sup></i> flies is reduced, but WT flies have functional L2-R feedback. The difference in the corresponding LMC outputs shows that L2-feedback boosts WT LMC output to repeated stimulation by ∼40%. L2-feedback seems also to boost WT R1–R6 output by ∼15%. The control experiments at 19°C show that L2-feedback functions normally in both <i>L2-shi<sup>TS1</sup></i> and WT cells, with only little differences in their relative strengths (<i>cf.</i>, <a href=\"\" target=\"_blank\">Fig. 4</a>).</p>", "links"=>[], "tags"=>["r-lmc-r", "reduced"], "article_id"=>580147, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"", "title"=>"Adaptation in the <i>L2-shi<sup>TS1</sup></i> R-LMC-R system is reduced at 30°C.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 00:02:27"}
  • {"files"=>[""], "description"=>"<p>A. Color-coded electron-micrograph shows a cross-section of the neurons and synapses in a single lamina cartridge of the <i>Drosophila</i> optic lobe. R1–R6 are terminals of photoreceptors. Monopolar cells, L1 and L2, are situated in the centre of the cartridge together with a terminal of a C3-cell from the 2<sup>nd</sup> visual neuropile, the medulla. Other monopolar cells, L3–L5 lie more peripherally. C2 is a second medulla cell, whereas α indicates an amacrine cell (AC) and β indicate a T1 cell. Only L1–3 and AC receive direct inputs from R1–R6 (green arrows). L4 receive inputs from AC and L4, L5 from AC and Tan (not shown), and T1 from AC <a href=\"\" target=\"_blank\">[1]</a>. L2 (blue arrows) and AC (brown arrows) are the only direct feedbacks to R1–R6 terminals <a href=\"\" target=\"_blank\">[1]</a>. Higher-order feedback to the lamina from C2 and C3 fibers is indicated by gray arrows. The figure is based on a modified EM image from Ian Meinertzhagen (<a href=\"\" target=\"_blank\"></a>). The arrowheads highlight only some of the complex interactions between the neurons in this network. B. <i>In vivo</i> intracellular recordings from intact Oregon-R <i>Drosophila</i> at 25°C. A R1–R6 photoreceptor depolarizes (due to opening of light-gated cation-channels, trp(l)) <a href=\"\" target=\"_blank\">[36]</a> and a LMC hyperpolarizes (due to opening of histamine-gated Cl-channels hclA) <a href=\"\" target=\"_blank\">[9]</a> to light pulses, generating complex response waveforms. Here the saturating bright pulse is 1,000 times more intense than the dim pulse, yet these cells can reliably respond to both of them. The LMC's voltage response to the dim pulse is larger than its response to the bright pulse, in contrast to the photoreceptor output. Note that the responses of LMCs reach their peak well before those of photoreceptors. C. A block-diagram representing the feedforward (R-LMC) and direct feedback (L2/AC-R) pathways in which visual information flows in the R-LMC-R system. In this paper, we perturbate these connections to work out whether they play a role in improving the neural representation in the LMC output to repeated naturalistic contrast patterns <a href=\"\" target=\"_blank\">[4]</a>.</p>", "links"=>[], "tags"=>["connections", "lamina"], "article_id"=>579649, "categories"=>["Neuroscience"], "users"=>["Anton Nikolaev", "Lei Zheng", "Trevor J. Wardill", "Cahir J. O'Kane", "Gonzalo G. de Polavieja", "Mikko Juusola"], "doi"=>"", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"", "title"=>"Feedforward and feedback connections in the lamina are complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-30 02:40:49"}

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Relative Metric

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