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Featured ArticleArticles, Systems/Circuits

Emergence of Orientation Selectivity in the Mammalian Visual Pathway

Benjamin Scholl, Andrew Y. Y. Tan, Joseph Corey and Nicholas J. Priebe
Journal of Neuroscience 26 June 2013, 33 (26) 10616-10624; DOI: https://doi.org/10.1523/JNEUROSCI.0404-13.2013
Benjamin Scholl
Center for Perceptual Systems, Section of Neurobiology, School of Biological Sciences, College of Natural Sciences, The University of Texas at Austin, Austin, Texas 78712
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Andrew Y. Y. Tan
Center for Perceptual Systems, Section of Neurobiology, School of Biological Sciences, College of Natural Sciences, The University of Texas at Austin, Austin, Texas 78712
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Joseph Corey
Center for Perceptual Systems, Section of Neurobiology, School of Biological Sciences, College of Natural Sciences, The University of Texas at Austin, Austin, Texas 78712
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Nicholas J. Priebe
Center for Perceptual Systems, Section of Neurobiology, School of Biological Sciences, College of Natural Sciences, The University of Texas at Austin, Austin, Texas 78712
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Abstract

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 subthreshold inputs onto V1 simple cells. Together, these differences show that although orientation selectivity exists in visual neurons of both rodents and carnivores, its emergence along the visual pathway, and thus its underlying neuronal circuitry, is fundamentally different.

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The Journal of Neuroscience: 33 (26)
Journal of Neuroscience
Vol. 33, Issue 26
26 Jun 2013
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Emergence of Orientation Selectivity in the Mammalian Visual Pathway
Benjamin Scholl, Andrew Y. Y. Tan, Joseph Corey, Nicholas J. Priebe
Journal of Neuroscience 26 June 2013, 33 (26) 10616-10624; DOI: 10.1523/JNEUROSCI.0404-13.2013

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Emergence of Orientation Selectivity in the Mammalian Visual Pathway
Benjamin Scholl, Andrew Y. Y. Tan, Joseph Corey, Nicholas J. Priebe
Journal of Neuroscience 26 June 2013, 33 (26) 10616-10624; DOI: 10.1523/JNEUROSCI.0404-13.2013
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  • Response to Cang and Zhao
    Nicholoas J. Priebe
    Published on: 19 July 2013
  • Orientation Selectivity Is NOT Similar in LGN and V1 of Mice
    Jianhua Cang
    Published on: 08 July 2013
  • Published on: (19 July 2013)
    Page navigation anchor for Response to Cang and Zhao
    Response to Cang and Zhao
    • Nicholoas J. Priebe, Assistant Professor
    • Other Contributors:
      • Benjamin Scholl and Andrew Tan

    Cang and Zhao raise interesting issues with regard to the emergence of orientation selectivity in mice. Their points do not contradict our interpretation of the data.

    The first issue raised is that because multiple LGN neurons converge onto a target V1 neuron, any diversity of orientation preference in those LGN inputs will reduce the orientation selectivity of the aggregate input. We agree with this, because ou...

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    Cang and Zhao raise interesting issues with regard to the emergence of orientation selectivity in mice. Their points do not contradict our interpretation of the data.

    The first issue raised is that because multiple LGN neurons converge onto a target V1 neuron, any diversity of orientation preference in those LGN inputs will reduce the orientation selectivity of the aggregate input. We agree with this, because our data suggest that subthreshold cortical orientation selectivity is slightly broader than thalamic orientation selectivity.

    The second issue raised is that if one examines parameters other than orientation selectivity, for example the spatial segregation of ON and OFF subfields, a dramatic transformation between the thalamus and cortex is observed. Indeed, it appears that there are many response selectivities that are distinct between the LGN and V1, including the size of receptive fields and the degree of surround suppression (Grubb and Thompson, 2003; Marshel et al., 2012; Piscopo et al., 2013). Furthermore, even without considering these other parameters, evidence exists for orientation selective processing in mouse V1. For example, neurons with similar preferred orientation are more likely to be connected (Atallah et al., 2012, Ko et al., 2011; Liu et al., 2011, Li et al., 2012; Tan et al., 2011).

    These interesting considerations do not affect our result that cat and mouse are different because the latter lacks a marked increase in orientation selectivity from thalamus to the subthreshold responses found in cortex.

    References:

    Atallah BV, Bruns W, Carandini M, Scanziani M (2012) Parvalbumin- expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159-170.

    Grubb MS, Thompson ID (2003) Quantitative characterization of visual response properties in the mouse dorsal lateral geniculate nucleus. J Neurophysiol 90:3594 -3607.

    Ko H, Hofer SB, Pichler B, Buchanan KA, Sjostrom PJ, Mrsic-Flogel TD (2011) Functional specificity of local synaptic connections in neocortical networks. Nature 473:87-91.

    Li YT, Ma WP, Pan CJ, Zhang LI, Tao HW (2012) Broadening of cortical inhibition mediates developmental sharpening of orientation selectivity. J Neurosci 32:3981-3991.

    Liu BH, Li YT, Ma WP, Pan CJ, Zhang LI, Tao HW (2011) Broad inhibition sharpens orientation selectivity by expanding input dynamic range in mouse simple cells. Neuron 71:542-554.

    Marshel JH, Kaye AP, Nauhaus I, Callaway EM (2012) Anterior-posterior direction opponency in the superficial mouse lateral geniculate nucleus. Neuron 76:713-720.

    Piscopo DM, El-Danaf RN, Huberman AD, Niell CM (2013) Diverse visual features encoded in mouse lateral geniculate nucleus. J Neurosci 33:4642- 4656.

    Tan AY, Brown BD, Scholl B, Mohanty D, Priebe NJ (2011) Orientation selectivity of synaptic input to neurons in mouse and cat primary visual cortex. J Neurosci 31:12339-12350.

    Conflict of Interest:

    None declared

    Show Less
    Competing Interests: None declared.
  • Published on: (8 July 2013)
    Page navigation anchor for Orientation Selectivity Is NOT Similar in LGN and V1 of Mice
    Orientation Selectivity Is NOT Similar in LGN and V1 of Mice
    • Jianhua Cang, Associate Professor
    • Other Contributors:
      • Xinyu Zhao

    In this paper, Scholl et al. reported that the orientation selectivity of spiking responses in the mouse dLGN and the subthreshold membrane potential responses in V1 simple cells (the first stage of cortical processing) were similar, and suggested that cortical orientation selectivity could be inherited from the dLGN in mice. However, for this to be true, all the presynaptic dLGN neurons to a given simple cell have to be...

    Show More

    In this paper, Scholl et al. reported that the orientation selectivity of spiking responses in the mouse dLGN and the subthreshold membrane potential responses in V1 simple cells (the first stage of cortical processing) were similar, and suggested that cortical orientation selectivity could be inherited from the dLGN in mice. However, for this to be true, all the presynaptic dLGN neurons to a given simple cell have to be tuned to the same orientation, including the many dLGN neurons that only show very small orientation bias. Short of such a perfect alignment, the "inherited" dLGN orientation selectivity would be blurred and weakened in simple cells due to the large convergence ratio in thalamocortical connections. Although some orientation-specific convergence may exist, given its unavoidable imprecision, the finding of similar selectivity between dLGN spiking and simple cell membrane potential is actually a clue for the presence, rather than absence, of additional cortical computation.

    The receptive field (RF) basis of orientation selectivity is in fact different for the dLGN and V1 simple cells in mice. The summary schematics of Scholl et al. (Figure 5), which depict simple-cell-like RFs (i.e., segregated and elongated ON/OFF subregions) throughout all stages of mouse visual pathway, ignored the findings that most dLGN neurons have the classic center-surround RFs (Grubb and Thompson, 2003; Piscopo et al., 2013). Even for orientation-selective dLGN cells, the vast majority of them still have single polarity RF centers (either circular or elongated) (Piscopo et al., 2013; Zhao et al., 2013). Simple cell-like RFs are rare in mouse retina and dLGN but prominent in V1, which reveals a dramatic transformation of visual processing in the cortex, just like in cats and primates.

    The mouse dLGN clearly encodes more diverse features than previously thought (Marshel et al., 2012; Piscopo et al., 2013; Zhao et al., 2013), but the difference in visual transformation across mammalian species may not be as fundamental as Scholl et al. suggest.

    References:

    Grubb MS, Thompson ID (2003) Quantitative characterization of visual response properties in the mouse dorsal lateral geniculate nucleus. J Neurophysiol 90:3594 -3607.

    Marshel JH, Kaye AP, Nauhaus I, Callaway EM (2012) Anterior-posterior direction opponency in the superficial mouse lateral geniculate nucleus. Neuron 76:713-720.

    Piscopo DM, El-Danaf RN, Huberman AD, Niell CM (2013) Diverse visual features encoded in mouse lateral geniculate nucleus. J Neurosci 33:4642- 4656.

    Zhao X, Chen H, Liu X, and Cang J (2013) Orientation-selective responses in the mouse lateral geniculate nucleus. J Neurosci In Press.

    Conflict of Interest:

    We have a paper in press in The Journal of Neuroscience, also on orientation selectivity in the mouse dLGN: Zhao X, Chen H, Liu X, and Cang J (2013) Orientation-selective responses in the mouse lateral geniculate nucleus. J Neurosci In Press.

    Show Less
    Competing Interests: None declared.

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