“moving dot”and a“random dot”(Fig. 4A). The
moving dot stimulus consisted of a small dot
shifting position incrementally along a linear
trajectory through the receptive field of the
neuron (the same type of stimulus as used in
experiments described above). For the random
dot stimulus, the dot positions along the same
trajectory were randomized (Fig. 4A). Except for
the temporal order of the dot positions, the two
stimuli were identical. V1 neurons responded
almost equally well to moving and to random
dots (Fig. 4B) [25.19% (67 of 266) of the units
isolated from V1 responded to moving and/or
random dots; average firing rate ± SEM for mov-
ing dot: 1.62 ± 0.19 Hz; for random dot: 1.13 ±
0.16 Hz;n= 67; 5 mice]. For all responsive V1
neurons, the moving dot produced only a 1.4-fold-
higher average firing response than the random
dot. The response of POR neurons to the same
stimuli, however, showed a marked preference
for the moving dot over the random dot (Fig. 4C).
For all responsive POR neurons, the moving dot
produced a 9.2-fold-higher average firing re-
sponse than the random dot [33.73% (56 of 166)
of the units isolated from POR responded to
either stimulus; average firing rate ± SEM for
moving dot: 2.77 ± 0.5 Hz; for random dot: 0.3 ±
0.05 Hz;P< 0.0001, Wilcoxon signed-rank
test,n= 56; 5 mice]. This was not because POR
neurons responded much more to moving dots
than did V1 neurons, but mainly because POR
neurons responded much less to random dots
than did V1 neurons. Receiver operator char-
acteristics (ROC) analysis showed that an inde-
pendent observer is better at discriminating
moving from random dots based on the response
of POR than the response of V1 neurons (Fig.
4D). Finally, we used moving dots to compare
the sizes of receptive fields of POR and V1 neu-
rons (fig. S12). Neurons in POR had significantly
larger receptive fields than those in V1 (medians ±
interquartile ranges of receptive field area; POR:
735.5 ± 631 square degrees,n= 62, 5 mice; V1:
157 ± 71.25 square degrees,n=31,8mice;P<
0.0001, Wilcoxon rank sum test).
These results show that a cortical area, POR,
is driven by visual information conveyed via the
colliculo-cortical pathway rather than by the
geniculate-V1 pathway. The weak impact of V1
silencing on POR is consistent with the weak
projection of the former onto the latter area ( 14 ).
The superior ability of POR to discriminate
movingobjectscomparedwiththatofV1isin
agreement with previous descriptions of en-
hanced motion selectivity in lateral cortical visual
areas ( 23 , 24 ). However, though this selectivity to
moving objects was believed to result from the
hierarchical cortical processing of geniculate
inputs entering V1 ( 23 , 24 ), our data indicate
that this property of POR depends on collicular
input and could be directly inherited from SC.
Similarly, the expanded representation of the
upper visual hemifield reported in POR ( 24 , 25 )
could also be directly inherited from the equally
biased representation in SC ( 26 ). Because the
colliculo-cortical pathway is believed to be phylo-
genetically older than the geniculate-V1 pathway
( 27 ), it is tempting to regard POR as an ancestral
primary visual area.
Previous reports of SC lesions in cats ( 12 ) and
rodents ( 9 ) described only a slight reduction, if
any, of visually evoked activity in various visual
cortical areas. Furthermore, in rodents, this re-
duction depends on the features of the stimulus
( 9 ). However, none of these recordings was per-
formed in POR. In primates, SC silencing and
lesionsalsohavelittleornoimpactonvisual
response of several visual cortical areas unless
V1 has been ablated first ( 11 ). Although primate
vision may rely less on SC than in other mam-
mals, again, these recordings were not performed
in the parahippocampal cortical areas TF and
TH, the primate areas most similar to POR ( 28 ).
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to the frontal eye fields. Primates can also par-
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some aspect of blindsight depends on the impact
of SC on visual cortex remains to be established.
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segregation of the sensory representation of the
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ACKNOWLEDGMENTS
We thank all the members of the Scanziani lab for discussions
about the project and comments on the manuscript; H. Karten for
advice during the course of the study; L. Frank, R. Nicoll, and
E. Feinberg for critical reading of the manuscript; and M. Mukundan,
J. Evora, N. Kim, and Y. Li for technical support.Funding:This
project was supported by the European Molecular Biology
Organization Long Term Fellowship, the Human Frontier Science
Program Long Term Fellowship, and the Howard Hughes
Medical Institute.Author contributions:R.B. and M.S. designed
the study. R.B. conducted all experiments and analyses. R.B.
and M.S. wrote the paper.Competing interests:The authors
declare no competing interests.Data and materials availability:
All data and analyses necessary to understand and assess the
conclusions of the manuscript are presented in the main text and
in the supplementary materials.SUPPLEMENTARY MATERIALS
http://www.sciencemag.org/content/363/6422/64/suppl/DC1
Materials and Methods
Figs. S1 to S12
References ( 31 – 41 )
3 August 2018; accepted 21 November 2018
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