An oscillatory circuit underlying the detection of disruptions in temporally-periodic patterns

Gao, Juan; Schwartz, Greg; Berry, Michael; Holmes, Philip

doi:10.1080/09548980902991705

Cited by 10 publications

(11 citation statements)

References 76 publications

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“…Recent evidence suggests that bipolar cells may generate a 10 Hz rhythm in rd1 mouse bipolar cells (Borowska et al, 2010). Indirect evidence from other species [tiger salamander (Gao et al, 2009); goldfish (Protti et al, 2000)] support this hypothesis. Other pacemaker-like interneurons have been reported in the wt retina, such as the starburst amacrine cells (Petit-Jacques et al, 2005) or dopaminergic amacrine cells (Feigenspan et al, 1998).…”

Section: Phenomenology Of the Rhythmic Rgc Activity And The Lfpssupporting

confidence: 63%

Network Oscillations in Rod-Degenerated Mouse Retinas

Menzler¹,

Zeck²

2011

J. Neurosci.

113

169

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In the mammalian retina, excitatory and inhibitory circuitries enable retinal ganglion cells (RGCs) to signal the occurrence of visual features to higher brain areas. This functionality disappears in certain diseases of retinal degeneration because of the progressive loss of photoreceptors. Recent work in a mouse model of retinal degeneration (rd1) found that, although some intraretinal circuitry is preserved and RGCs maintain characteristic physiological properties, they exhibit increased and aberrant rhythmic activity. Here, extracellular recordings were made to assess the degree of aberrant activity in adult rd1 retinas and to investigate the mechanism underlying such behavior. A multi-transistor array with thousands of densely packed sensors allowed for simultaneous recordings of spiking activity in populations of RGCs and of local field potentials (LFPs). The majority of identified RGCs displayed rhythmic (7-10 Hz) but asynchronous activity. The spiking activity correlated with the LFPs, whichreflectanaveragesynchronizedexcitatoryinputtotheRGCs.LFPsinitiatedfromrandompositionsandpropagatedacrosstheretina.They disappeared when ionotrophic glutamate receptors or electrical synapses were blocked. They persisted in the presence of other pharmacological blockers, including TTX and inhibitory receptor antagonists. Our results suggest that excitation-transmitted laterally through a network of electrically coupled interneurons-leads to large-scale retinal network oscillations, reflected in the rhythmic spiking of most rd1 RGCs. This result may explain forms of photopsias reported by blind patients, while the mechanism involved should be considered in future treatment strategies targeting the disease of retinitis pigmentosa.

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Section: Phenomenology Of the Rhythmic Rgc Activity And The Lfpssupporting

confidence: 63%

Network Oscillations in Rod-Degenerated Mouse Retinas

Menzler¹,

Zeck²

2011

J. Neurosci.

113

169

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“…3) suggest that a resonant mechanism may be responsible for the generation of the poststimulus responses. If that is the case, then the amplitude characteristics of the poststimulus responses should be well-described by a mathematical model of a resonant system, such as an LRC circuit that has been used previously to describe resonances in retinal ON bipolar cells (Gao et al, 2009). The response of such a resonant system can be described using the equation for a forced oscillator:

\frac{d^{2} x}{{italicdt}^{2}} + 2 ζ ω_{0} \frac{italicdx}{italicdt} + ω_{0}^{2} x = α \sin (ω_{1} t),

in which the sinusoidal waveform on the right side of eqn.…”

Section: Resultsmentioning

confidence: 99%

“…An LRC resonant circuit model similar to the one used in the present study was employed previously to describe the poststimulus response (i.e., OSR) recorded from RGCs of salamander and mouse (Gao et al, 2009 ). However, in contrast to our simplifi ed resonance model [ eqn.…”

Section: Discussionmentioning

confidence: 99%

“…A second possibility is that the additional poststimulus responses are generated by a resonant mechanism. A resonant system, specifi cally an LRC electrical circuit involving inductance (L), resistance (R), and conductance (C), has been used to model resonances in ON bipolar cells of the salamander retina (Gao et al, 2009 ). If a similar type of resonant mechanism underlies the generation of the multiple poststimulus responses of the human cone fl icker ERG, then the period of the additional responses would not necessarily correspond to the period of the stimulus fl icker train.…”

Section: Introductionmentioning

confidence: 99%

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Poststimulus response characteristics of the human cone flicker electroretinogram

2013

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At certain temporal frequencies, the human cone flicker electroretinogram (ERG) contains multiple additional responses following the termination of a flicker train. The purpose of this study was to determine whether these poststimulus responses are a continuing response to the terminated flicker train or represent the oscillation of a resonant system. ERGs were recorded from 10 visually normal adults in response to full-field sinusoidally modulated flicker trains presented against a short-wavelength rod-saturating adapting field. The amplitude and timing properties of the poststimulus responses were evaluated within the context of a model of a second-order resonant system. At stimulus frequencies between 41.7 and 71.4 Hz, the majority of subjects showed at least three additional ERG responses following the termination of the flicker train. The interval between the poststimulus responses was approximately constant across stimulus frequency, with a mean of 14.4 ms, corresponding to a frequency of 69.4 Hz. The amplitude and timing characteristics of the poststimulus ERG responses were well described by an underdamped second-order system with a resonance frequency of 70.3 Hz. The observed poststimulus ERG responses may represent resonant oscillations of retinal ON bipolar cells, as has been proposed for electrophysiological recordings of poststimulus responses from retinal ganglion cells. However, further investigation is required to determine the types of retinal neurons involved in the generation of the poststimulus responses of the human flicker ERG.

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“…This is also the case for the inclusion of other types of ON/OFF asymmetries seen, e.g., in retina where both onset and offsets of the stimulus can lead to increases of firing rates [41]. The connectivity between primary receptors and the ON and OFF cells considered here is known to determine receptive field properties and needs to be included in the analysis at some point.…”

Section: Resultsmentioning

confidence: 99%

Responses of recurrent nets of asymmetric ON and OFF cells

2010

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A neural field model of ON and OFF cells with all-to-all inhibitory feedback is investigated. External spatiotemporal stimuli drive the ON and OFF cells with, respectively, direct and inverted polarity. The dynamic differences between networks built of ON and OFF cells ("ON/OFF") and those having only ON cells ("ON/ON") are described for the general case where ON and OFF cells can have different spontaneous firing rates; this asymmetric case is generic. Neural responses to nonhomogeneous static and timeperiodic inputs are analyzed in regimes close to and away from self-oscillation. Static stimuli can cause oscillatory behavior for certain asymmetry levels. Time-periodic stimuli expose dynamical differences between ON/OFF and ON/ON nets. Outside the stimulated region, we show that ON/OFF nets exhibit frequency doubling, while ON/ON nets cannot. On the other hand, ON/ON networks show antiphase responses between stimulated and unstimulated regions, an effect that does not rely on specific receptive field circuitry. An analysis of the resonance properties of both net types reveals that ON/OFF nets exhibit larger response amplitude. Numerical simulations of the neural field models agree with theoretical predictions for localized static and time-periodic forcing. This is also the case for simulations of a network of noisy integrate-and-fire neurons. We finally discuss the application of the model to the electrosensory system and to frequency-doubling effects in retina.

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An oscillatory circuit underlying the detection of disruptions in temporally-periodic patterns

Cited by 10 publications

References 76 publications

Network Oscillations in Rod-Degenerated Mouse Retinas

Network Oscillations in Rod-Degenerated Mouse Retinas

Poststimulus response characteristics of the human cone flicker electroretinogram

Responses of recurrent nets of asymmetric ON and OFF cells

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