Disinhibition Combines with Excitation to Extend the Operating Range of the OFF Visual Pathway in Daylight

Manookin, Michael B.; Beaudoin, Deborah Langrill; Ernst, Zachary Raymond; Flagel, Leigh J.; Demb, Jonathan B.

doi:10.1523/jneurosci.4274-07.2008

Cited by 223 publications

(342 citation statements)

References 85 publications

(135 reference statements)

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“…In this revised scheme, intrinsic oscillations in the AII/ cone ON bipolar cells provide the major drive to both amacrine and ganglion cells. In addition, extending the known AII amacrine cell circuit in wt retina (Manookin et al, 2008;Murphy and Rieke, 2008;Münch et al, 2009), we speculate that oscillations in the AII amacrine cells could carry over to the OFF system through gly- cinergic inhibition of the OFF bipolar cells and ganglion cells (Fig. 10).…”

Section: Discussionsupporting

confidence: 59%

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An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

Borowska¹,

Trenholm²,

Awatramani³

2011

J. Neurosci.

107

171

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The loss of photoreceptors during retinal degeneration (RD) is known to lead to an increase in basal activity in remnant neural networks. To identify the source of activity, we combined two-photon imaging with patch-clamp techniques to examine the physiological properties of morphologically identified retinal neurons in a mouse model of RD (rd1). Analysis of activity in rd1 ganglion cells revealed sustained oscillatory (ϳ10 Hz) synaptic activity in ϳ30% of all classes of cells. Oscillatory activity persisted after putative inputs from residual photoreceptor, rod bipolar cell, and inhibitory amacrine cell synapses were pharmacologically blocked, suggesting that presynaptic cone bipolar cells were intrinsically active. Examination of presynaptic rd1 ON and OFF bipolar cells indicated that they rested at relatively negative potentials (less than Ϫ50 mV). However, in approximately half the cone bipolar cells, low-amplitude membrane oscillation (ϳ5 mV, ϳ10 Hz) were apparent. Such oscillations were also observed in AII amacrine cells. Oscillations in ON cone bipolar and AII amacrine cells exhibited a weak apparent voltage dependence and were resistant to blockade of synaptic receptors, suggesting that, as in wild-type retina, they form an electrically coupled network. In addition, oscillations were insensitive to blockers of voltage-gated Ca 2ϩ channels (0.5 mM Cd 2ϩ and 0.5 mM Ni 2ϩ ), ruling out known mechanisms that underlie oscillatory behavior in bipolar cells. Together, these results indicate that an electrically coupled network of ON cone bipolar/AII amacrine cells constitutes an intrinsic oscillator in the rd1 retina that is likely to drive synaptic activity in downstream circuits.

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Section: Discussionsupporting

confidence: 59%

“…In contrast, oscillations were not observed in wt AII amacrine cells (n ϭ 4) (Fig. 7 B, D) (Manookin et al, 2008;Murphy and Rieke, 2008;Münch et al, 2009) (but see Veruki and Hartveit, 2002). Figure 7B illustrates the relatively stable baseline of a wt AII amacrine cell.…”

Section: Spontaneous Activity In Rd1 Bipolar Cellsmentioning

confidence: 88%

An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

Borowska¹,

Trenholm²,

Awatramani³

2011

J. Neurosci.

107

171

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“…In the guinea pig, pharmacological measurements have suggested that AII amacrine cells carrying signals from cone photoreceptors hyperpolarize to disinhibit Off-type ganglion cells (12). In the salamander retina, disinhibition has been shown in the context of a flash of light (11), where hyperpolarization of GABAergic amacrine cells is thought to delay the truncation of the Off ganglion cell light response.…”

Section: Discussionmentioning

confidence: 99%

“…Inhibitory transmission to ganglion cells is known to have different effects, including reducing activity (6, 10), or increasing activity through disinhibition (11)(12)(13)(14). Thus, to understand how a particular amacrine cell changes the ganglion cell response, measurements of both the response and transmission of the interneuron must be temporally precise.…”

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confidence: 99%

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Disinhibitory gating of retinal output by transmission from an amacrine cell

Manu

Baccus²

2011

Proc. Natl. Acad. Sci. U.S.A.

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Inhibitory interneurons help transform the input of a neural circuit into its output. Such interneurons are diverse, and most have unknown function. To study the function of single amacrine cells in the intact salamander retina, we recorded extracellularly from a population of ganglion cells with a multielectrode array, while simultaneously recording from or injecting current into single Offtype amacrine cells that had linear responses. We measured how visual responses of the amacrine cell interacted both with other visual input to the ganglion cell and with transmission between the two cells. We found that on average, visual responses from Off-type amacrine cells inhibited nearby Off-type ganglion cells. By recording and playing back the light-driven membrane potential fluctuations of amacrine cells during white noise visual stimuli, we found that paradoxically, increasing the light-driven modulations of inhibitory amacrine cells increased the firing rate of nearby Off-type ganglion cells. By measuring the correlations and transmission between amacrine and ganglion cells, we found that, on average, the amacrine cell hyperpolarizes before the ganglion cell fires, generating timed disinhibition just before the ganglion cell spikes. In addition, we found that amacrine to ganglion cell transmission is nonlinear in that increases in ganglion cell activity produced by amacrine hyperpolarization were greater than decreases in activity produced by amacrine depolarization. We conclude that the primary mode of action of this class of amacrine cell is to actively gate the ganglion cell response by a timed release from inhibition.multielectrode recording | computational modeling I n local neural circuits of the brain, interneurons change the output of the circuit by combining their own transmission with inputs to the circuit (1). Inhibitory interneurons throughout the brain have great diversity in their morphology, postsynaptic connections, and biochemistry, but for nearly all of these cells, their functional role in information processing is unknown. In the retina, inhibitory amacrine cells comprise more than 30 classes; most of these cells also have unknown function (2, 3).Compared with a principal neuron, which represents a circuit's output, understanding the functional role of interneurons is a challenge because the effect of an interneuron on the circuit's output is a combination of multiple circuit properties (4, 5). For example, the effect of an amacrine cell on a retinal ganglion cell is a function of the amacrine cell's light response, its effects of transmission on the retinal ganglion cell, and of other visual input to the ganglion cell. Knowledge of all three of these properties is needed to predict how the amacrine cell will affect the ganglion cell's activity.The responses of different cells are precisely timed in the retina, with different amacrine and ganglion cells having distinct temporal responses with respect to light (6-9). Inhibitory transmission to ganglion cells is known to have different effects, i...

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Characterization of small‐field bistratified amacrine cells in macaque retina labeled by antibodies against synaptotagmin‐2

Neumann

Haverkamp

2012

J of Comparative Neurology

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Macaque retinae were immunostained with monoclonal antibodies directed against the protein synaptotagmin-2 (Syt2). Syt2 was localized in a population of small-field amacrine cells, whose cell bodies formed a regular mosaic within the inner nuclear layer, indicating they represent a single amacrine cell type. The labeled amacrine cells had a bistratified appearance with a dense dendritic plexus in the OFF-layer and only a few lobular processes extending into the ON-layer of the inner plexiform layer, similar to A8 amacrine cells described in cat and human retina. Syt2-labeled cells were immunoreactive for glycine but lacked immunoreactivity for γ-aminobutyric acid (GABA), suggesting they use glycine as their neurotransmitter. The density of these cells increases from ∼200/mm(2) in peripheral retina to ∼1,400/mm(2) in central retina. Their bipolar cell input was studied by immunolabeling experiments using various bipolar cell markers combined with CtBP2, a marker of presynaptic ribbons. Our data show that Syt2-labeled amacrine cells receive input from both OFF and ON cone bipolar cells, as well as from rod bipolar cells. The OFF input is dominated by the diffuse bipolar cell DB1 (44%) and the OFF midget bipolar cell (38%). Here we describe a population of bistratified small-field amacrine cells closely resembling A8 amacrine cells and their cone-dominated bipolar cell input. J. Comp. Neurol. 521:709-724, 2013. © 2012 Wiley Periodicals, Inc.

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Disinhibition Combines with Excitation to Extend the Operating Range of the OFF Visual Pathway in Daylight

Cited by 223 publications

References 85 publications

An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

Disinhibitory gating of retinal output by transmission from an amacrine cell

Characterization of small‐field bistratified amacrine cells in macaque retina labeled by antibodies against synaptotagmin‐2

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