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Integrating motion and depth via parallel pathways

Abstract

Processing of visual information is both parallel and hierarchical, with each visual area richly interconnected with other visual areas. An example of the parallel architecture of the primate visual system is the existence of two principal pathways providing input to the middle temporal visual area (MT): namely, a direct projection from striate cortex (V1), and a set of indirect projections that also originate in V1 but then relay through V2 and V3. Here we have reversibly inactivated the indirect pathways while recording from MT neurons and measuring eye movements in alert monkeys, a procedure that has enabled us to assess whether the two different input pathways are redundant or whether they carry different kinds of information. We find that this inactivation causes a disproportionate degradation of binocular disparity tuning relative to direction tuning in MT neurons, suggesting that the indirect pathways are important in the recovery of depth in three-dimensional scenes.

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Figure 1: Effects of cooling on visually evoked activity in the anterior lunate bank.
Figure 2: Effects of V2/V3 inactivation on the firing rates of MT neurons.
Figure 3: Changes in direction tuning of MT neurons during V2/V3 inactivation.
Figure 4: Comparison of changes in disparity and direction tuning of MT neurons during V2/V3 inactivation.
Figure 5: Quantitative and qualitative changes in tuning for direction and disparity during V2/V3 inactivation.
Figure 6: Correlation of direction and disparity modulation-amplitude ratio distributions.
Figure 7: Bootstrap test of the global gain hypothesis.
Figure 8: Effects of V2/V3 inactivation on disparity-dependent eye movements.

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Acknowledgements

We thank P. Hendrickson and A. Zaharia for technical assistance, and J.H.R. Maunsell, J.A. Assad, M. Livingstone and N. Price for comments on the manuscript. This work was supported by a grant to C.R.P. from the National Institutes of Neurological Disorders and Stroke (F31NS052926), a grant to S.G.L. from the Natural Sciences and Engineering Research Council of Canada (327442), an R01 grant to R.T.B. (EY11379), a Vision Core Grant (EY12196) and a gift from R. Brandon Fradd.

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R.T.B. conceived the initial inactivation project. C.R.P. performed the experiments and developed the project along with R.T.B. S.G.L. fabricated the cryoloops and, along with R.T.B., implanted them in all monkeys. C.R.P. and R.T.B. wrote the manuscript, and all authors participated in its editing.

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Correspondence to Carlos R Ponce.

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Ponce, C., Lomber, S. & Born, R. Integrating motion and depth via parallel pathways. Nat Neurosci 11, 216–223 (2008). https://doi.org/10.1038/nn2039

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