Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat

Soodak, Robert E.; Shapley, Robert; Kaplan, Ehud

doi:10.1152/jn.1987.58.2.267

Cited by 107 publications

(119 citation statements)

References 23 publications

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“…In species of carnivores and primates, the transformation driving orientation selectivity occurs in visual cortex, although some selectivity in cat and primate is observed in the retina and LGN. Recordings along the visual pathway from macaque (Hubel and Wiesel, 1968;Essen and Zeki, 1978;Schall et al, 1986;Smith et al, 1990;Ts'o et al, 1990;Gur et al, 2005), tree shrew (Fitzpatrick, 1996;Bosking et al, 1997;Chisum et al, 2003), mouse (Dräger, 1975;Métin et al, 1988;Ohki et al, 2005;Weng et al, 2005;Ohki and Reid, 2007;Elstrott et al, 2008;Marshel et al, 2012;Piscopo et al, 2013), rabbit (Barlow et al, 1964;Levick, 1967;Levick et al, 1969;Murphy and Berman, 1979;Taylor et al, 2000;Venkataramani and Taylor, 2010), and cat (Hubel and Wiesel, 1959, 1961, 1962, 1963Boycott and Wässle, 1974;Cleland and Levick, 1974;Hammond, 1974;Levay and Gilbert, 1976;Levick and Thibos, 1980;Leventhal and Schall, 1983;Vidyasagar and Heide, 1984;Soodak et al, 1987;Shou and Leventhal, 1989;Reid and Alonso, 1995;Shou et al, 1995;Ferster et al, 1996;Chung and Ferster, 1998;Usrey et al, 1999;Alonso et al, 2001;Kuhlmann and Vidyasagar, 2011;…”

Section: Discussionmentioning

confidence: 99%

“…We measured the responses of cat LGN relay cells extracellularly (n ϭ 35), as well as the subthreshold membrane potential and suprathreshold spiking responses of cat V1 simple cells (n ϭ 41), which are predominately found in layer 4 and receive direct thalamocortical excitatory input (LeVay and Gilbert, 1976;Reid and Alonso, 1995;Ferster et al, 1996;Chung and Ferster, 1998;Usrey et al, 1999;Alonso et al, 2001). Cat LGN relay cells are known to show subtle orientation selectivity (Vidyasagar and Heide, 1984;Soodak et al, 1987;Shou and Leventhal, 1989;, attributed to an orientation bias in retinal ganglion cells (Boycott and Wässle, 1974;Cleland and Levick, 1974;Hammond, 1974;Levick and Thibos, 1980;Leventhal and Schall, 1983;Shou et al, 1995), and this was evident in our extracellular records (mean OSI ϭ 0.09 Ϯ 0.08, median ϭ 0.07; Fig. 4A, bottom).…”

Section: Comparison Of Orientation Selectivity Across Visual Processimentioning

confidence: 99%

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Emergence of Orientation Selectivity in the Mammalian Visual Pathway

Scholl

Tan

Corey

et al. 2013

Journal of Neuroscience

174

112

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Orientation selectivity is a property of mammalian primary visual cortex (V1) neurons, yet its emergence along the visual pathway varies across species. In carnivores and primates, elongated receptive fields first appear in V1, whereas in lagomorphs such receptive fields emerge earlier, in the retina. Here we examine the mouse visual pathway and reveal the existence of orientation selectivity in lateral geniculate nucleus (LGN) relay cells. Cortical inactivation does not reduce this orientation selectivity, indicating that cortical feedback is not its source. Orientation selectivity is similar for LGN relay cells spiking and subthreshold input to V1 neurons, suggesting that cortical orientation selectivity is inherited from the LGN in mouse. In contrast, orientation selectivity of cat LGN relay cells is small relative to subthresholdinputsontoV1simplecells.Together,thesedifferencesshowthatalthoughorientationselectivityexistsinvisualneuronsofbothrodentsand carnivores, its emergence along the visual pathway, and thus its underlying neuronal circuitry, is fundamentally different.

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Section: Discussionmentioning

confidence: 99%

Section: Comparison Of Orientation Selectivity Across Visual Processimentioning

confidence: 99%

Emergence of Orientation Selectivity in the Mammalian Visual Pathway

Scholl

Tan

Corey

et al. 2013

Journal of Neuroscience

174

112

View full text Add to dashboard Cite

show abstract

“…By comparison, the receptive field often shows consistent biases for orientation (Fig. 8 E) (Vidyasagar and Urbas, 1982;Soodak et al, 1987;Shou and Leventhal, 1989;Sun et al, 2004), which reach significance (ANOVA, p Ͻ 0.05) in 20 of 30 neurons. This bias had no consistent relationship with that seen occasionally in the suppressive field: aligning responses with the orientation that gave the peak receptive field response (Fig.…”

Section: Visual Preferencesmentioning

confidence: 92%

The Suppressive Field of Neurons in Lateral Geniculate Nucleus

Bonin¹,

Mante²,

Carandini³

2005

J. Neurosci.

212

244

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The responses of neurons in lateral geniculate nucleus (LGN) exhibit powerful suppressive phenomena such as contrast saturation, size tuning, and masking. These phenomena cannot be explained by the classical center-surround receptive field and have been ascribed to a variety of mechanisms, including feedback from cortex. We asked whether these phenomena might all be explained by a single mechanism, contrast gain control, which is inherited from retina and possibly strengthened in thalamus. We formalized an intuitive model of retinal contrast gain control that explicitly predicts gain as a function of local contrast. In the model, the output of the receptive field is divided by the output of a suppressive field, which computes the local root-mean-square contrast. The model provides good fits to LGN responses to a variety of stimuli; with a single set of parameters, it captures saturation, size tuning, and masking. It also correctly predicts that responses to small stimuli grow proportionally with contrast: were it not for the suppressive field, LGN responses would be linear. We characterized the suppressive field and found that it is similar in size to the surround of the classical receptive field (which is eight times larger than commonly estimated), it is not selective for stimulus orientation, and it responds to a wide range of frequencies, including very low spatial frequencies and high temporal frequencies. The latter property is hardly consistent with feedback from cortex. These measurements thoroughly describe the visual properties of contrast gain control in LGN and provide a parsimonious explanation for disparate suppressive phenomena.

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“…The differences in the responses of cortical cells to bars and sinusoidal gratings must also be taken into account in any attempt to understand cortical function since the orientation and direction sensitivities of cells throughout the retinogeniculocortical pathways are spatial frequency dependent (Hammond 1973(Hammond , 1974Thibos, 1980, 1982;Shou and Leventhal, 1989; Smith et al, 1990;Soodak et al, 1987;Hawken et al, 1988;Hammond and Pomfret, 1990). Deciding subjectively which stimulus is the one of choice in order to test selectivity and infer function seems inappropriate since a cell's selectivity can appear quite different depending upon which stimulus is employed.…”

Section: Technical Considerationsmentioning

confidence: 99%

Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex

et al. 1995

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The receptive field properties of cells in layers 2, 3, and 4 of area 17 (V1) of the monkey were studied quantitatively using colored and broad-band gratings, bars, and spots. Many cells in all regions studied responded selectively to stimulus orientation, direction, and color. Nearly all cells (95%) in layers 2 and 3 exhibited statistically significant orientation preferences (biases), most exhibited at least some color sensitivity, and many were direction sensitive. The degree of selectivity of cells in layers 2 and 3 varied continuously among cells; we did not find discrete regions containing cells sensitive to orientation and direction but not color, and vice versa. There was no relationship between the degree of orientation sensitivity of the cells studied and their degree of color sensitivity. There was also no obvious relationship between the receptive field properties studied and the cells' location relative to cytochrome oxidase-rich regions. Our findings are difficult to reconcile with the hypothesis that there is a strict segregation of cells sensitive to orientation, direction, and color in layers 2 and 3. In fact, the present results suggest the opposite since most cells in these layers are selective for a number of stimulus attributes.

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Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat

Cited by 107 publications

References 23 publications

Emergence of Orientation Selectivity in the Mammalian Visual Pathway

Emergence of Orientation Selectivity in the Mammalian Visual Pathway

The Suppressive Field of Neurons in Lateral Geniculate Nucleus

Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex

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