Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina
TL;DR: Intracellular recordings were made from various types of cells in the isolated goldfish retina, and Procion Yellow was injected from the recording pipette in order to identify histologically the structure recorded.
Abstract: 1. Intracellular recordings were made from various types of cells in the isolated goldfish retina, and Procion Yellow was injected from the recording pipette in order to identify histologically the structure recorded. The dye diffused and stained the cell body and processes down to the fine branches.
2. S-potentials were identified as coming from the external horizontal cells and from the internal horizontal cells. Both L- and C-type S-potentials were found in both regions, and no histological differences were seen in cells giving these two types of responses. S-potentials recorded from the external horizontal cells showed less spatial summation than those recorded from the internal horizontal cells.
3. Bipolar cell responses consisted of sustained potentials associated with an antagonistic centre-surround type receptive field (on-centre, off-surround or vice versa). Spike activity was not observed in bipolar cells.
4. Amacrine cells responded with transient depolarization both at the beginning and at the end of illumination. They sometimes showed spike activity. The amplitude of on- and off-depolarization showed slight dependence on stimulus geometry but a distinct centre-surround organization was not observed.
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05 Jun 1975
TL;DR: Introduction to synaptic circuits, Gordon M.Shepherd and Christof Koch membrane properties and neurotransmitter actions, David A.Brown and Anthony M.Brown.
Abstract: Introduction to synaptic circuits, Gordon M.Shepherd and Christof Koch membrane properties and neurotransmitter actions, David A.McCormick peripheral ganglia, Paul R.Adams and Christof Koch spinal cord - ventral horn, Robert E.Burke olfactory bulb, Gordon M.Shepherd, and Charles A.Greer retina, Peter Sterling cerebellum, Rodolfo R.Llinas and Kerry D.Walton thalamus, S.Murray Sherman and Christof Koch basal ganglia, Charles J.Wilson olfactory cortex, Lewis B.Haberly hippocampus, Thomas H.Brown and Anthony M.Zador neocortex, Rodney J.Douglas and Kevan A.C.Martin Gordon M.Shepherd. Appendix: Dendretic electrotonus and synaptic integration.
3,241 citations
TL;DR: It is suggested that arousal is gated by a chemical transmitter system—for example, norepinephrine—whose relative states of accumulation at antagonistic pairs of on-cells and off-cells through time can shift the spatial pattern of STM activity across a field of feature detectors.
Abstract: Part I of this paper describes a model for the parallel development and adult coding of neural feature detectors. It shows how any set of arbitrary spatial patterns can be recoded, or transformed, into any other spatial patterns (universal recoding), if there are sufficiently many cells in the network's cortex. This code is, however, unstable through time if arbitrarily many patterns can perturb a fixed number of cortical cells. This paper shows how to stabilize the code in the general case using feedback between cellular sites. A biochemically defined critical period is not necessary to stabilize the code, nor is it sufficient to ensure useful coding properties.
We ask how short term memory can be reset in response to temporal sequences of spatial patterns. This leads to a context-dependent code in which no feature detector need uniquely characterize an input pattern; yet unique classification by the pattern of activity across feature detectors is possible. This property uses learned expectation mechanisms whereby unexpected patterns are temporarily suppressed and/or activate nonspecific arousal. The simplest case describes reciprocal interactions via trainable synaptic pathways (long term memory traces) between two recurrent on-center off-surround networks undergoing mass action (shunting) interactions. This unit can establish an adaptive resonance, or reverberation, between two regions if their coded patterns match, and can suppress the reverberation if their patterns do not match. This concept yields a model of olfactory coding within the olfactory bulb and prepyriform cortex. The resonance idea also includes the establishment of reverberation between conditioned reinforcers and generators of contingent negative variation if presently avialable sensory cues are compatible with the network's drive requirements at that time; and a search and lock mechanism whereby the disparity between two patterns can be minimized and the minimal disparity images locked into position. Stabilizing the code uses attentional mechanisms, in particular nonspecific arousal as a tuning and search device. We suggest that arousal is gated by a chemical transmitter system--for example, norepinephrine--whose relative states of accumulation at antagonistic pairs of on-cells and off-cells through time can shift the spatial pattern of STM activity across a field of feature detectors. For example, a sudden arousal increment in response to an un-expected pattern can reverse, or rebound, these relative activities, thereby suppressing incorrectly classified populations. The rebound mechanism has formal properties analogous to negative afterimages and spatial frequency adaptation.
1,132 citations
TL;DR: The fundamental structural principles of the retina give a bottom-up view of the strategies used in the retina's processing of visual information and suggest new questions for physiological experiments and modeling.
Abstract: The retina, like many other central nervous system structures, contains a huge diversity of neuronal types. Mammalian retinas contain approximately 55 distinct cell types, each with a different function. The census of cell types is nearing completion, as the development of quantitative methods makes it possible to be reasonably confident that few additional types exist. Although much remains to be learned, the fundamental structural principles are now becoming clear. They give a bottom-up view of the strategies used in the retina’s processing of visual information and suggest new questions for physiological experiments and modeling.
1,122 citations
TL;DR: Assessing evidence from a wide range of vertebrate and invertebrate examples, it is shown that reducing energy expenditure can account for many of the morphological features of sensory systems and has played a key role in their evolution.
Abstract: Evolution of animal morphology, physiology and behaviour is shaped by the selective pressures to which they are subject Some selective pressures act to increase the benefits accrued whilst others act to reduce the costs incurred, affecting the cost/benefit ratio Selective pressures therefore produce a trade-off between costs and benefits that ultimately influences the fitness of the whole organism The nervous system has a unique position as the interface between morphology, physiology and behaviour; the final output of the nervous system is the behaviour of the animal, which is a product of both its morphology and physiology The nervous system is under selective pressure to generate adaptive behaviour, but at the same time is subject to costs related to the amount of energy that it consumes Characterising this trade-off between costs and benefits is essential to understanding the evolution of nervous systems, including our own Within the nervous system, sensory systems are the most amenable to analysing costs and benefits, not only because their function can be more readily defined than that of many central brain regions and their benefits quantified in terms of their performance, but also because recent studies of sensory systems have begun to directly assess their energetic costs Our review focuses on the visual system in particular, although the principles we discuss are equally applicable throughout the nervous system Examples are taken from a wide range of sensory modalities in both vertebrates and invertebrates We aim to place the studies we review into an evolutionary framework We combine experimentally determined measures of energy consumption from whole retinas of rabbits and flies with intracellular measurements of energy consumption from single fly photoreceptors and recently constructed energy budgets for neural processing in rats to assess the contributions of various components to neuronal energy consumption Taken together, these studies emphasize the high costs of maintaining neurons at rest and whilst signalling A substantial proportion of neuronal energy consumption is related to the movements of ions across the neuronal cell membrane through ion channels, though other processes such as vesicle loading and transmitter recycling also consume energy Many of the energetic costs within neurons are linked to 3Na(+)/2K(+) ATPase activity, which consumes energy to pump Na(+) and K(+) ions across the cell membrane and is essential for the maintenance of the resting potential and its restoration following signalling Furthermore, recent studies in fly photoreceptors show that energetic costs can be related, via basic biophysical relationships, to their function These findings emphasize that neurons are subject to a law of diminishing returns that severely penalizes excess functional capacity with increased energetic costs The high energetic costs associated with neural tissue favour energy efficient coding and wiring schemes, which have been found in numerous sensory systems We discuss the role of these efficient schemes in reducing the costs of information processing Assessing evidence from a wide range of vertebrate and invertebrate examples, we show that reducing energy expenditure can account for many of the morphological features of sensory systems and has played a key role in their evolution
898 citations
Cites background from "Physiological and morphological ide..."
...…into an electrical signal, the transmission of electrical signals within neurons and synaptic transmission of signals between neurons (Barlow, 1956; Katz and Miledi, 1970; Lillywhite and Laughlin, 1979; Aho et al., 1988; Mainen and Sejnowski, 1995; Berry et al., 1997; de Ruyter van Steveninck et…...
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TL;DR: At least half of the encodings sent to the brain (ganglion cell response selectivities) remain to be discovered, indicating that diversity of the retina's outputs has yet to be incorporated into the understanding of higher visual function.
834 citations
Cites background from "Physiological and morphological ide..."
...Bipolar Cells Early physiological recordings suggested that there were four types of bipolar cells: ON, OFF, sustained, and transient (Kaneko, 1970; Werblin and Dowling, 1969)....
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References
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TL;DR: The intracellularly recorded response characteristics of each type of neuron in a vertebrate retina are described, and the response of each neuron to the responses of those neurons to which it is synaptically coupled are related.
Abstract: the optic nerve, it has been possible to specify many of the functions performed bv the vertebrate retina. These include brightness detection (16, 18, 27), centersurround contrast detection (1, 8, 20, 23), and motion detection (3, 4, 26-28). It has not been possible, however, to determine how the retina organizes the visual message recorded at the optic nerve, primarily because intracellular recording from single cells distal to the ganglion cells has been difficult. Detailed structural studies of the vertebrate retina, such as the one in the preceding paper (14), provide a framework within which the functional organization of the retina can be described. The anatomical studies show a limited number of clearly defined synaptic structures at which interaction between specific neurons can take place. In this paper we shall describe the intracellularly recorded response characteristics of each type of neuron in a vertebrate retina, and then relate the response of each neuron to the responses of those neurons to which it is synaptically coupled. By following the responses through the synaptic pathways, we can begin to describe how information from the visual field is abstracted and encoded in the retina. Intracellular recording throughout most retinas has been difficult because even the finest available micropipettes fail to penetrate the small retinal neurons consistently without damage. Bortoff (5-7) showed that this difficulty could be overcome by recording in an animal with larger retinal neurons: the mudpuppy, Nectwus maculosus. As described in the preceding paper (14),
1,356 citations
TL;DR: Repeated injection of the same cells in ganglia from different animals showed that cells have characteristic shapes and that the neuropil is highly structured.
Abstract: In a study of the specificity of neuronal connections in lobster abdominal ganglia, the dye Procion Yellow M4RS was electrophoretically injected into identified cell bodies. This dye spreads into fine branches of cells, survives fixation and routine histological procedures, and permits the reconstruction of cell shapes through examination of serial sections of ganglia. Certain cells were found to have an internal bilateral symmetry. Repeated injection of the same cells in ganglia from different animals showed that cells have characteristic shapes and that the neuropil is highly structured. This method of dye injection should have general applicability in studies where a knowledge of the geometry of specific cells is important.
404 citations
TL;DR: S‐potentials from Luminosity‐units in the excised eye of the tench (Tinca) were excited by white lights of various intensities and spatial distributions.
Abstract: 1. S-potentials from Luminosity-units in the excised eye of the tench (Tinca) were excited by white lights of various intensities and spatial distributions.
2. When a small light spot of fixed size and intensity was presented at various distances from the recording electrode, the S-potential was found to suffer an exponential attenuation with distance (Fig. 3).
3. A circular patch of light centred upon the electrode and varied in radius gave concordant results.
4. The effects at the electrode site of a distant light flash was not due to light scattered to the electrode which acted upon the retina there; the light acted locally and it was the current that spread.
5. With red and blue light stimuli superposed on the retina, it is the potentials not the lights that add.
6. These experimental results seem to indicate that S-potentials can spread laterally across the retina within a thin layer at about the horizontal cell level.
7. The layer is bounded by leaky membranes which appear to be electrogenic, no doubt as a result of transmitters released by light which change the permeability. Electric currents have no demonstrable effect.
8. Two simple results were found. (a) The membrane contains an element whose conductance is proportional to the light intensity. (b) The S-potential is a hyperbolic function of light intensity.
9. All these experimental results can be explained quantitatively in terms of the formal model of Fig. 8F. But the required change of membrane permeability with light has not yet been demonstrated.
362 citations
TL;DR: After impregnation of goldfish retina by the rapid Golgi method, two classes each of photoreceptor, bipolar, and horizontal cells were observed by light microscopy, and some role in information processing therefore appears likely.
Abstract: After impregnation of goldfish retina by the rapid Golgi method, two classes each of photoreceptor, bipolar, and horizontal cells were observed by light microscopy. Interconnections between these elements in the outer plexiform (first synaptic) layer were investigated by electron microscopy of ultrathin sections, in which the processes of impregnated cells are easily distinguished. Dendrites of large bipolar cells (Cajal's “bipolaires destinees aux bâtonnets”) appeared to contact the synaptic endings of both rods and cones, while those of small bipolars (Cajal's “bipolaires destinees aux cones”) appeared to contact only cones. Processes from horizontal cells of the vitread level (Cajal's “cellules horizontaux intermediaires”) appeared to contact only rods, while those from horizontal cells of the sclerad level (Cajal's “cellules horizontaux externes”) appeared to contact only cones. The structures formerly called “synaptic vacuoles” are the terminals of horizontal cell processes in the goldfish, and by analogy they should be so identified in all vertebrates. Teleostean horizontal cells are not typical of neurons or glia cells, but are morphologically intermediate between them. Their most interesting properties are their unique relationship to photoreceptor synaptic endings and their segregation into rod and cone subsystems along with the corresponding photoreceptor and bipolar cells. Although their specific function is not clear, some role in information processing therefore appears likely.
348 citations
TL;DR: In this paper, a new direct and rapid method for filling single and multibarreled drawn glass capillary microelectrodes is described, which can be used for both single and multi-barred drawn glass microelectrometers.
320 citations