scholarly journals Neural sensitization improves encoding fidelity in the primate retina

2018 ◽  
Author(s):  
Todd R. Appleby ◽  
Michael B. Manookin

ABSTRACTAn animal’s motion through the environment can induce large and frequent fluctuations in light intensity on the retina. These fluctuations pose a major challenge to neural circuits tasked with encoding visual information, as they can cause cells to adapt and lose sensitivity. Here, we report that sensitization, a short-term plasticity mechanism, solves this difficult computational problem by maintaining neuronal sensitivity in the face of these fluctuations. The numerically dominant output pathway in the macaque monkey retina, the midget (parvocellular-projecting) pathway, undergoes sensitization under specific conditions, including simulated eye movements. Sensitization is present in the excitatory synaptic inputs from midget bipolar cells and is mediated by presynaptic disinhibition from wide-field amacrine cells. Direct physiological recordings and a computational model indicate that sensitization in the midget pathway supports accurate sensory encoding and prevents a loss of responsiveness during dynamic visual processing.

1993 ◽  
Vol 10 (3) ◽  
pp. 511-522 ◽  
Author(s):  
William J. Brunken ◽  
Xiao-Tao Jin

AbstractWe investigated the role of 5HT3 receptors in the mammalian retina using electrophysiological techniques to monitor ganglion cell activity. Activation of 5HT3 receptors with the selective agonist 1-phenylbiguanide (PBG) increased the ON responses of ON-center ganglion cells, while decreasing the OFF responses of OFF-center cells. The application of a selective 5HT3 antagonist had a reciprocal effect, namely it reduced the center response in ON-center cells and concomitantly increased the center responses in OFF-center cells. Since putative serotoninergic amacrine cells in the retina are connected specifically to the rod bipolar cell, these agents most likely affect the rod bipolar terminal. These data, together with previous studies, suggest that both 5HT2 and 5HT3 receptors mediate an excitatory influence which serves to facilitate the output from rod bipolar cells, the former via a phosphatidyl inositol second-messenger system, and the latter via a direction channel.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Jen-Chun Hsiang ◽  
Keith P Johnson ◽  
Linda Madisen ◽  
Hongkui Zeng ◽  
Daniel Kerschensteiner

Neurons receive synaptic inputs on extensive neurite arbors. How information is organized across arbors and how local processing in neurites contributes to circuit function is mostly unknown. Here, we used two-photon Ca2+ imaging to study visual processing in VGluT3-expressing amacrine cells (VG3-ACs) in the mouse retina. Contrast preferences (ON vs. OFF) varied across VG3-AC arbors depending on the laminar position of neurites, with ON responses preferring larger stimuli than OFF responses. Although arbors of neighboring cells overlap extensively, imaging population activity revealed continuous topographic maps of visual space in the VG3-AC plexus. All VG3-AC neurites responded strongly to object motion, but remained silent during global image motion. Thus, VG3-AC arbors limit vertical and lateral integration of contrast and location information, respectively. We propose that this local processing enables the dense VG3-AC plexus to contribute precise object motion signals to diverse targets without distorting target-specific contrast preferences and spatial receptive fields.


2017 ◽  
Author(s):  
Jen-Chun Hsiang ◽  
Keith Johnson ◽  
Linda Madisen ◽  
Hongkui Zeng ◽  
Daniel Kerschensteiner

AbstractSynaptic inputs to neurons are distributed across extensive neurite arborizations. To what extent arbors process inputs locally or integrate them globally is, for most neurons, unknown. This question is particularly relevant for amacrine cells, a diverse class of retinal interneurons, which receive input and provide output through the same neurites. Here, we used two-photon Ca2+ imaging to analyze visual processing in VGluT3-expressing amacrine cells (VG3-ACs), an important component of object motion sensitive circuits in the retina. VG3-AC neurites differed in their preferred stimulus contrast (ON vs. OFF); and ON and OFF responses varied in transience and preferred stimulus size. Contrast preference changed predictably with the laminar position of neurites in the inner plexiform layer. Yet, neurites at all depths were strongly activated by local but not by global image motion. Thus, VG3-AC neurites process visual information locally, exhibiting diverse responses to contrast steps, but uniform object motion selectivity.


2008 ◽  
Vol 508 (1) ◽  
pp. 13-27 ◽  
Author(s):  
Sriparna Majumdar ◽  
Heinz Wässle ◽  
Patricia R. Jusuf ◽  
Silke Haverkamp

2021 ◽  
Vol 7 (1) ◽  
pp. 181-199
Author(s):  
Anita A. Disney

Visual processing is dynamically controlled by multiple neuromodulatory molecules that modify the responsiveness of neurons and the strength of the connections between them. In particular, modulatory control of processing in the lateral geniculate nucleus of the thalamus, V1, and V2 will alter the outcome of all subsequent processing of visual information, including the extent to and manner in which individual inputs contribute to perception and decision making and are stored in memory. This review addresses five small-molecule neuromodulators—acetylcholine, dopamine, serotonin, noradrenaline, and histamine—considering the structural basis for their action, and the effects of their release, in the early visual pathway of the macaque monkey. Traditionally, neuromodulators are studied in isolation and in discrete circuits; this review makes a case for considering the joint action of modulatory molecules and differences in modulatory effects across brain areas as a better means of understanding the diverse roles that these molecules serve.


2003 ◽  
Vol 89 (4) ◽  
pp. 2159-2166 ◽  
Author(s):  
Cun-Jian Dong ◽  
William A. Hare

We examined function of the feedback pathway from A17 GABAergic amacrine cells to rod bipolar cells (A17 feedback), a critically located inhibitory circuit in the classic rod pathway of the mammalian retina whose role in processing of scotopic visual information is still poorly understood. We show evidence that this A17 feedback has a profound influence on the temporal properties of rod-driven postphotoreceptoral responses (assessed with the scotopic electroretinogram b-wave). Application of a GABAcantagonist prolonged preferentially the decay of the scotopic b-wave. The degree of prolongation increased as the light intensity decreased. Application of selective GABAa antagonists accelerated the kinetics of the scotopic b-wave. This effect was abolished when the GABAc antagonist was coapplied. Selective ablation of A17 cells mimicked the action of the GABAc antagonist. In A17 cell–ablated retinas, the GABAc antagonist was no longer very effective to slow the decay of the scotopic b-wave. Thus the A17 feedback, activated by light stimulation and mediated mainly by the GABAc receptors, makes the scotopic b-wave more transient by accelerating preferentially its decay. The strength of the feedback can be modulated by GABAa receptor–mediated inhibition and by light intensity. Our results also suggest that in the mammalian retina the feedback may be a novel mechanism that contributes postphotoreceptorally to the termination of rod signals, especially those elicited by very dim light stimuli.


2012 ◽  
Vol 29 (1) ◽  
pp. 41-49 ◽  
Author(s):  
WILLIAM N. GRIMES

AbstractFeedback is a ubiquitous feature of neural circuits in the mammalian central nervous system (CNS). Analogous to pure electronic circuits, neuronal feedback provides either a positive or negative influence on the output of upstream components/neurons. Although the particulars (i.e., connectivity, physiological encoding/processing/signaling) of circuits in higher areas of the brain are often unclear, the inner retina proves an excellent model for studying both the anatomy and physiology of feedback circuits within the functional context of visual processing. Inner retinal feedback to bipolar cells is almost entirely mediated by a single class of interneurons, the amacrine cells. Although this might sound like a simple circuit arrangement with an equally simple function, anatomical, molecular, and functional evidence suggest that amacrine cells represent an extremely diverse class of CNS interneurons that contribute to a variety of retinal processes. In this review, I classify the amacrine cells according to their anatomical output synapses and target cell(s) (i.e., bipolar cells, ganglion cells, and/or amacrine cells) and discuss specifically our current understandings of amacrine cell-mediated feedback and output to bipolar cells on the synaptic, cellular, and circuit levels, while drawing connections to visual processing.


2015 ◽  
Vol 114 (3) ◽  
pp. 1606-1616 ◽  
Author(s):  
Michael B. Manookin ◽  
Christian Puller ◽  
Fred Rieke ◽  
Jay Neitz ◽  
Maureen Neitz

At early stages of visual processing, receptive fields are typically described as subtending local regions of space and thus performing computations on a narrow spatial scale. Nevertheless, stimulation well outside of the classical receptive field can exert clear and significant effects on visual processing. Given the distances over which they occur, the retinal mechanisms responsible for these long-range effects would certainly require signal propagation via active membrane properties. Here the physiology of a wide-field amacrine cell—the wiry cell—in macaque monkey retina is explored, revealing receptive fields that represent a striking departure from the classic structure. A single wiry cell integrates signals over wide regions of retina, 5–10 times larger than the classic receptive fields of most retinal ganglion cells. Wiry cells integrate signals over space much more effectively than predicted from passive signal propagation, and spatial integration is strongly attenuated during blockade of NMDA spikes but integration is insensitive to blockade of NaV channels with TTX. Thus these cells appear well suited for contributing to the long-range interactions of visual signals that characterize many aspects of visual perception.


2017 ◽  
Vol 38 (3) ◽  
pp. 723-732 ◽  
Author(s):  
Amanda M. Travis ◽  
Stephanie J. Heflin ◽  
Arlene A. Hirano ◽  
Nicholas C. Brecha ◽  
Vadim Y. Arshavsky

2012 ◽  
Vol 29 (1) ◽  
pp. 51-60 ◽  
Author(s):  
JONATHAN B. DEMB ◽  
JOSHUA H. SINGER

AbstractAmacrine cells represent the most diverse class of retinal neuron, comprising dozens of distinct cell types. Each type exhibits a unique morphology and generates specific visual computations through its synapses with a subset of excitatory interneurons (bipolar cells), other amacrine cells, and output neurons (ganglion cells). Here, we review the intrinsic and network properties that underlie the function of the most common amacrine cell in the mammalian retina, the AII amacrine cell. The AII connects rod and cone photoreceptor pathways, forming an essential link in the circuit for rod-mediated (scotopic) vision. As such, the AII has become known as the rod–amacrine cell. We, however, now understand that AII function extends to cone-mediated (photopic) vision, and AII function in scotopic and photopic conditions utilizes the same underlying circuit: AIIs are electrically coupled to each other and to the terminals of some types of ON cone bipolar cells. The direction of signal flow, however, varies with illumination. Under photopic conditions, the AII network constitutes a crossover inhibition pathway that allows ON signals to inhibit OFF ganglion cells and contributes to motion sensitivity in certain ganglion cell types. We discuss how the AII’s combination of intrinsic and network properties accounts for its unique role in visual processing.


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