Direction-Selective Units in Rabbit Retina: Distribution of Preferred Directions

Oyster, Clyde W.; Barlow, H. B.

doi:10.1126/science.155.3764.841

Cited by 244 publications

(148 citation statements)

References 7 publications

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“…2F. It is very obvious that the distribution of LGN DS cell preferred directions (black) forms four groups (anterior, posterior, superior, and inferior), resembling the distribution of ON_OFF DS ganglion cells in the rabbit retina (Oyster and Barlow 1967). In contrast, the preferred directions of cortical simple cells (red) are more homogeneously distributed.…”

Section: D E and F)mentioning

confidence: 90%

“…The representation of the visual streak is located roughly midway along the dorso-ventral axis within the rabbit LGN, whereas the upper visual field is represented dorsally (Holcombe and Guillery 1984;Hughes 1971). We examined the visual response properties of LGN DS neurons and showed that their responses are highly nonlinear, that they consist of highly overlapping ON and OFF subfields, and that their preferred directions are, like their counterparts in the retina (Oyster and Barlow 1967), restricted to the four cardinal directions. Notably, each of these visual response properties are dramatically distinct from those of V1 layer 4 simple cells studied in the same preparation using identical methods (Zhuang et al 2013), suggesting that LGN DS neurons do not contribute strongly to the synthesis of the direction/orientation selectivity seen in V1 simple cells.…”

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confidence: 99%

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Directional selective neurons in the awake LGN: response properties and modulation by brain state

Hei

Stoelzel

Zhuang

et al. 2014

Journal of Neurophysiology

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Directionally selective (DS) neurons are found in the retina and lateral geniculate nucleus (LGN) of rabbits and rodents, and in rabbits, LGN DS cells project to primary visual cortex. Here, we compare visual response properties of LGN DS neurons with those of layer 4 simple cells, most of which show strong direction/orientation selectivity. These populations differed dramatically, suggesting that DS cells may not contribute significantly to the synthesis of simple receptive fields: 1) whereas the first harmonic component (F1)-to-mean firing rate (F0) ratios of LGN DS cells are strongly nonlinear, those of simple cells are strongly linear; 2) whereas LGN DS cells have overlapped ON/OFF subfields, simple cells have either a single ON or OFF subfield or two spatially separate subfields; and 3) whereas the preferred directions of LGN DS cells are closely tied to the four cardinal directions, the directional preferences of simple cells are more evenly distributed. We further show that directional selectivity in LGN DS neurons is strongly enhanced by alertness via two mechanisms, 1) an increase in responses to stimulation in the preferred direction, and 2) an enhanced suppression of responses to stimuli moving in the null direction. Finally, our simulations show that these two consequences of alertness could each serve, in a vector-based population code, to hasten the computation of stimulus direction when rabbits become alert.

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Section: D E and F)mentioning

confidence: 90%

mentioning

confidence: 99%

Directional selective neurons in the awake LGN: response properties and modulation by brain state

Hei

Stoelzel

Zhuang

et al. 2014

Journal of Neurophysiology

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“…Some types of RGCs respond selectively to the direction of motion (Cronly-Dillon, 1964;Barlow and Levick, 1965;Oyster and Barlow, 1967;Pearlman and Hughes, 1976). In the rabbit retina, direction-selective RGCs account for ϳ10% of all RGCs (Vaney, 1994;Vaney et al, 2001;Taylor and Vaney, 2003).…”

Section: Retinal Direction Selectivitymentioning

confidence: 99%

Analysis of Development of Direction Selectivity in Retinotectum by a Neural Circuit Model with Spike Timing-Dependent Plasticity

Honda¹,

Urakubo²,

Tanaka³

et al. 2011

J. Neurosci.

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The development of direction selectivity in the visual system depends on visual experience. In the developing Xenopus retinotectal system, tectal neurons (TNs) become direction selective through spike timing-dependent plasticity (STDP) after repetitive retinal exposure to a moving bar in a specific direction. We investigated the mechanism responsible for the development of direction selectivity in the Xenopus retinotectal system using a neural circuit model with STDP. In this retinotectal circuit model, a moving bar stimulated the retinal ganglion cells (RGCs), which provided feedforward excitation to the TNs and interneurons (INs). The INs provided delayed feedforward inhibition to the TNs. The TNs also received feedback excitation from neighboring TNs. As a synaptic learning rule, a molecular STDP model was used for synapses between the RGCs and TNs. The retinotectal circuit model reproduced experimentally observed features of the development of direction selectivity, such as increase in input to the TN. The peak of feedforward excitation from RGCs to TNs shifted earlier as a result of STDP. Together with the delayed feedforward inhibition, a stronger earlier transient feedforward signal was generated, which exceeded the threshold of the feedback excitation from the neighboring TNs and resulted in amplification of input to the TN. The suppression of the delayed feedforward inhibition resulted in the development of orientation selectivity rather than direction selectivity, indicating the pivotal role of the delayed feedforward inhibition in direction selectivity. We propose a mechanism for the development of direction selectivity involving a delayed feedforward inhibition with STDP and the amplification of feedback excitation.

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“…The ON-OFF DS cell class harbors four vector types (Oyster and Barlow, 1967) and lies in the small-to-medium soma size spectrum (Amthor et al, 1989b). Because vector type might display a well patterned distribution (Vaney, 1994b) and a single class contains two or more vector types, that class might show mixed distribution patterns.…”

Section: On-off Ds Cellsmentioning

confidence: 99%

“…In addition, some patterns might represent mixed "subclasses." For example, we know that ON-OFF direction-selective (DS) ganglion cells exist as four vector subclasses (Oyster and Barlow, 1967) but that they are not morphologically distinguishable (Amthor et al, 1989b). Any class that contains the ON-OFF DS cells should be represented by a mixture of patterns (a "mixed" pattern).…”

Section: Structural Correlates Of Classesmentioning

confidence: 99%

Molecular Phenotyping of Retinal Ganglion Cells

2002

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Classifying all of the ganglion cells in the mammalian retina has long been a goal of anatomists, physiologists, and cell biologists. The rabbit retinal ganglion cell layer was phenotyped using intrinsic small molecule signals (aspartate, glutamate, glycine, glutamine, GABA, and taurine) and glutamate receptorgated 1-amino-4-guanidobutane excitation signals as the clustering dimensions for formal classification. Intrinsic signals alone yielded 7 ganglion cell superclasses and 1 amacrine cell superclass; the addition of excitation signals ultimately resolved 14 natural ganglion cell classes and 3 amacrine cell classes. Ganglion cells comprise two-thirds to three-quarters of the cells in the ganglion cell layer and exhibited distinct metabolic, coupling, and excitation phenotypes, as well as characteristic sizes, population fractions, and patterns. Metabolic signatures (mixtures of glutamate, aspartate, glutamine, and GABA) chemically discriminated ganglion from amacrine cells. Coupling signatures reflected heterologous coupling states across ganglion cells: (1) uncoupled, (2) coupled to GABAergic amacrine cells, and (3) coupled to glycinergic amacrine cells. Excitation signatures reflected differential channel permeation rates across classes after AMPA activation. Extraction of unique size and patterning features from the data sets further validated the robustness of the classification. Because the classifications were explicitly blinded to structure, this is strong evidence that molecular phenotype classes are natural classes. Correspondences of molecular phenotype classes to functional classes were inferred from size, coupling, encounter, and physiological attributes. Ganglion cell classes display markedly different ionotropic drives, which may partly explain the physiological brisk-sluggish spectrum of ganglion cell spiking patterns.

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Direction-Selective Units in Rabbit Retina: Distribution of Preferred Directions

Cited by 244 publications

References 7 publications

Directional selective neurons in the awake LGN: response properties and modulation by brain state

Directional selective neurons in the awake LGN: response properties and modulation by brain state

Analysis of Development of Direction Selectivity in Retinotectum by a Neural Circuit Model with Spike Timing-Dependent Plasticity

Molecular Phenotyping of Retinal Ganglion Cells

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