Simple and complex cells in the visual wulst of the burrowing owl: two distinct classes or opposite ends of a stimulus-dependent continuum?
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1
Universidade Federal de Minas Gerais, Graduate Program in Electrical Engineering, Brazil
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2
Universidade Federal de Minas Gerais, Graduate Program in Physiology and Pharmacology, Brazil
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3
Universidade Federal de Minas, Department of Electrical Engineering, Brazil
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4
Universidade Federal de Minas Gerais, Department of Physiology and Biophysics, Brazil
The visual wulst is the avian telencephalic target of the retinothalamofugal pathway. In owls, this area is known to have a close functional resemblance with mammalian primary visual cortex (V1). In his pioneering study [1], Pettigrew reports that this resemblance also extends to two basic cell types initially described by Hubel and Wiesel [2]: simple cells, characterized by approximately linear spatial selectivity to stimulus contrast polarity, and a much more diverse population of so-called complex cells, which do not exhibit this response property. Here, we reassess Pettigrew’s finding using a more quantitative classification method derived from linear system theory. The method computes a linearity index of spatial summation based on the spiking response of a cell to moving sinusoidal gratings optimized in terms of spatial as well as temporal frequencies, orientation and direction of motion. The index (F1/F0) is obtained by dividing the amplitude of response oscillation at the fundamental frequency of the stimulus (F1) by the mean response of the cell above spontaneous discharge (F0). Cells yielding a F1/F0 > 1 are classified as simple cells; the others as complex cells. The reliability of this classification method is supported by two lines of evidence: 1) general agreement with other mapping methods; 2) Bimodal distribution of F1/F0 with a pronounced dip close to unity across V1 neurons of most mammalian species investigated to date. We analyzed a total of 338 neurons randomly sampled along different depths of the visual wulst of sixteen awake burrowing owls. Test gratings were typically presented for 4 s (10 repeats), interleaved with a uniform gray of mean luminance for at least 3 s. Unexpectedly, the F1/F0 frequency distribution was found to be unimodal (median F1/F0 = 0.39) with no clear evidence of local minimum at unity (P = 0.94, Hartigan’s dip test). Adopting the classification criterion conventionally used in mammals (see above), 83% of our sampled cells were classified as complex (median F1/F0 = 0.35). The proportion of simple cells (median F1/F0 = 1.37) was however only slightly lower than that reported by Pettigrew in anesthetized barn owls (21%, 126/579). Neurons classified as simple and complex had similar median spontaneous rates (3.53 and 4.08, respectively) and F1/F0 was not significantly correlated with spontaneous activity (rho = − 0.13, p = 0.016; Spearman rank correlation test). According to recent data from our laboratory, most wulst neurons exhibit marked response suppression when a drifting grating is expanded beyond their classical receptive field (CRF). Here, we found that this suppressive effect is actually often accompanied by a significant increase in F1/F0 (about 2/3 of evaluated cells, n = 86). Altogether, our results do not support the existence of two discrete simple/complex cell classes within the visual wulst. They further suggest that the degree with which a wulst neuron operates as a spatiotemporal linear filter dependents on specific combinations of stimulus attributes.
Acknowledgements
Financial Support: Fapemig, FINEP, CNPq, Capes.
References
[1] Pettigrew, J.D. Proc. R. Soc. Lond. B Biol. Sci., 204, 435–454, 1979.
[2] Hubel, D.H. & Wiesel, T.N. J. Physiol., 160, 106–154, 1962.
Keywords:
Burrowing owls,
complex cells,
Simple cells,
Visual wulst
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster Presentation (see alternatives below as well)
Topic:
Sensory: Vision
Citation:
Machado De Sousa
J,
Turchetti Maia
A,
Vieira
P,
Souza De Amorim
C,
Pinto
L,
Tierra Criollo
C and
Baron
J
(2012). Simple and complex cells in the visual wulst of the burrowing owl: two distinct classes or opposite ends of a stimulus-dependent continuum?.
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00256
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Received:
30 Apr 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Prof. Jerome Baron, Universidade Federal de Minas Gerais, Department of Physiology and Biophysics, Belo Horizonte, Minas Gerais, CEP 31270-901, Brazil, jbaron@icb.ufmg.br