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Orientation and spatiotemporal tuning of cells in the primary visual cortex of an Australian marsupial, the wallaby Macropus eugenii

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Abstract

The metatherians (marsupials) have been separated from eutherians (placentals) for approximately 135 million years. It might, therefore, be expected that significant independent evolution of the visual system has occurred. The present paper describes for the first time the orientation, direction and spatiotemporal tuning of neurons in the primary visual cortex of an Australian marsupial, the wallaby Macropus eugenii. The stimuli consisted of spatial sinusoidal gratings presented within apertures covering the classical receptive fields of the cells. The neurons can be classified as those with clear ON and OFF zones and those with less well-defined receptive field structures. Seventy-percent of the total cells encountered were strongly orientation selective (tuning functions at half height were less than 45°). The preferred orientations were evenly distributed throughout 360° for cells with uniform receptive fields but biased towards the vertical and horizontal for cells with clear ON-OFF zones. Many neurons gave directional responses but only a small percentage of them (4%) showed motion opponent properties (i.e. they were excited by motion in one direction and actively inhibited by motion in the opposite direction). The median peak temporal tuning for cells with clear ON-OFF zones and those without were 3 Hz and 6 Hz, respectively. The most common peak spatial frequency tuning for the two groups were 2 cycles per degree and 0.5 cycles per degree, respectively. Spatiotemporal tuning was not always the same for preferred and antipreferred direction motion. In general, the physiology of the wallaby cortex was similar to well studied eutherian mammals suggesting either convergent evolution or a highly conserved architecture that stems from a common therian ancestor.

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Fig. 1A,B.
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Abbreviations

cpd:

cycles per degree

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Acknowledgements

We thank Drs. Marotte, Henry and Wimborne for assistance with early experiments. Drs. Ted Maddess and Colin Clifford and two anonymous referees made constructive comments on early drafts, greatly improving the manuscript. All procedures were approved by the Animal Experimentation Ethics Committee of the Australian National University and complied with the Principles of Animal Care (publication no. 86-23, revised 1985) of the National Institute of Health and with the guidelines of the Australian National Health and Medical Research Council.

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Correspondence to M. R. Ibbotson.

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Ibbotson, M.R., Mark, R.F. Orientation and spatiotemporal tuning of cells in the primary visual cortex of an Australian marsupial, the wallaby Macropus eugenii . J Comp Physiol A 189, 115–123 (2003). https://doi.org/10.1007/s00359-002-0379-6

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