461
Central neural mechanisms for detecting second-order motion
Curtis L Baker Jr
Single-unit neurophysiology and human psychophysics have
begun to reveal distinct neural mechanisms for processing
visual stimuli defined by differences in contrast or texture
(second-order motion) rather than by luminance (first-order
motion). This processing begins in early visual cortical areas,
with subsequent extrastriate specialization, and may provide a
basis for form-cue invariant analyses of image structure, such as
figure-ground segregation and detection of illusory contours.
Addresses
McGill Vision Research Unit, Department of Ophthalmology, McGill
University, 687 Pine Ave W, H4-14, Montreal, Quebec, Canada
H3A 1 A 1; e-mail: curtis@astra.vision.mcgill.ca
Current Opinion in Neurobiology 1999, 9:461-466
http://biomednet.com/elecref/0959438800900461
© Elsevier Science Ltd ISSN 0959-4388
Abbreviations
A17 primary visual cortex of cat (see V1)
A18 secondary visual cortex of cat (see V2)
fMRI functional magnetic resonance imaging
MT/V5 extrastriate visual area specialized for motion
PET positron emission tomography
V1 primary (striate) visual cortex of primate (see A 17)
V2 secondary (pre-striate) visual cortex of primate (see A 18)
VP upper hemifield counterpart of V3
Introduction
Natural images contain a rich mixture of surfaces and
boundaries of objects that are delineated by local differ-
ences in luminance, contrast, texture, and motion. Much of
our understanding of visual perception has been achieved
using stimuli such as bars, edges, or sinewave gratings,
which are defined by vanat1ons in luminance.
Neurophysiology has demonstrated that single neurons in
the primary and secondary visual cortices can be remarkably
selective for local stimulus orientation, spatial frequency,
and direction of motion, and human psychophysical experi-
ments have provided evidence for the independent early
detection of these luminance-defined (first-order) stimulus
attributes. Recent advances in the experimental analysis of
the detection of borders defined by non-luminance (i.e. sec-
ond-order, or non-Fourier) variations, such as differences of
contrast or texture [1,2], have accelerated our progress in
understanding the underlying mechanisms.
The processing of luminance-defined (first-order) stimu-
lus attributes is conventionally understood in terms of
models in which selectiviry for stimulus properties such as
spatial frequency or orientation is attributed to linear fil-
tering, with subsequent nonlinear gain control and
thresholds affecting the amplitude of response [3"].
Figure la shows an image of a sinewave grating stimulus
upon which the receptive field of a Vl simple cell has been
superimposed. The Vl cell depicted would respond well
to this stimulus because of the linear summation of excita-
tion and inhibition from its ON and OFF zones. However,
stimuli composed of fine-scale texture elements (carrier)
that have a large-scale variation (envelope) in contrast
(Figure lb) or spatial offset (Figure lc) have equal
amounts of dark and light regions in each receptive field
zone, so the linear summation would give no net response.
Thus, these stimuli would be second-order, with respect to
the spatial scale of the neuron's receptive field. (However
stimuli constructed with large texture elements compared
to the size of the receptive field [4"] or with a net lumi-
nance different from the background might still give
first-order responses.) Although complex cells in Vl
behave nonlinearly, they nevertheless exhibit the same
kinds of luminance spatial selectivity as simple cells and
cannot explain response to second-order stimuli; therefore,
an additional kind of nonlinear processing is necessary.
This review will not only highlight some important results
from the past two years, concentrating on the detection of
contrast-modulated pattern motion (such as in Figure lb),
which is the best studied kind of second-order processing,
but also include discussion of some pertinent studies using
second-order texture stimuli lacking contrast modulation
(such as Figure lc).
Separate processing of first- and second-order
stimuli
The detection of second-order stimuli may not necessarily
require a separate processing mechanism from that used for
first-order stimuli. The simplest explanation for detection
of contrast modulation is that small nonlinearities early in
visual processing cause a slightly differing magnitude of
response to dark and light regions of carrier texture, giving
a small net difference between high- and low-contrast
regions that could be detected by subsequent linear filter-
ing. Such an early nonlinearity, possibly occurring in the
photoreceptors or artifactually in the stimulus apparatus,
could plausibly .produce only a very weak signal (if it were
a strong signal, its consequences would preclude the body
of findings that led to the prevalent linear filtering theory).
However, such a 'distortion product' could be a legitimate
concern in view of the very high contrast sensitivity of the
visual system [5]. Artifactual distortions introduced by dis-
play monitors can be compensated with careful calibration,
and a diffusing screen can be used as a spatial low-pass fil-
ter to assess the effectiveness of this correction [6,7""]. The
more serious issue of early visual nonlinearity has been
investigated using a variety of psychophysical methods and
stimuli [7"",8]- these studies concur that such early non-
linear effects, probably arising in photoreceptors [9], are
small in magnitude and only become large enough to affect
psychophysical data at higher temporal frequencies. A
related concern lies in inadvertent activation of first-order
462 Sensory systems

Figure 1

Examples of (a) first-order and (b-f) second·

order visual stimuli. (a) Conventional ( a) Luminance grating ( b) Contrast envelope (c) Illusory contour
luminance-defined sinewave grating. Light
and dark regions of the stimulus are aligned
with excitatory and inhibitory regions of the
superimposed schematic receptive field of a
V1 simple cell, such that linear spatial
summation would give a good response.
(b) One frame of a contrast-modulated
envelope stimulus, constructed with a
stationary high spatial frequency carrier
grating whose contrast is modulated by a (d) Texture-defined bar (e) Dynamic noise bar
moving low spatial frequency envelope.
Because the carrier spatial frequency is
relatively high, the light and dark image
regions cancel one another within excitatory
or inhibitory subzones of the simple receptive
field, giving no response from a linear, first-
order mechanism. (c) Abutting line gratings,
spatially offset where they meet, which give a
percept of an 'illusory contour' (used in
[24,25,29••]). A receptive field responding to
C urrent Opinion in Neurobiology
the vertical contour would represent another
kind of second-order response. (d) Bar·
shaped envelope enclosing a noise texture, envelope enclosing a region of dynamic stimulus, as in (b), but with carrier grating at
whose mean luminance is matched to the noise, against a background of static noise different orientation than envelope (used
backgrou nd (used in [29••]). (e) Bar-shaped (used in [23,26••,38]). (f) Contrast envelope in [1 o••]).

processing - particularly using second-order stimuli con-
structed with relatively large, static texture elements. This
problem can be avoided in neurophysiology by using a car-
rier texture of much finer grain than the measured linear
filter properties of the neuron [6,10""], and in psy-
chophysics by e mploying dynamic carriers [4•].
Distinct mechanisms for processing first- and second-order
stimuli have been implicated in many psychophysical
studies. Nishida eta/. [11""] report that adaptation to one
kind of stimulus does not affect motion thresholds for the
other, and Schofield and Georgeson [1 2.. ] found that
detection thresholds for each can be facilitated in an order-
specific manner. We [13"] found that chromatically defined
motion is directly detected only by second-order motion
mechanisms. Several groups have reported that contrast
envelope stimuli are best detected in a lower range of tem-
poral frequencies than first-order stimuli [14,15",16"];
other kinds of second-order stimuli show slower temporal
dynamics [17- 19]. The two kinds of motion also exhibit
differing degrees or kinds of vulnerability to interference
from other added masking stimuli [20,2 1,22"].
These kinds of evidence, as well as recent neurophysiology
(see below), indicate that first- and second-order stimuli are
processed by separate, early mechanisms, before being
combined into a unitary motion representation.
Responses to second-order stimuli in early
visual cortical areas
Neurons responding to second- as well as first-order stim-
uli are present not only in extrastriate cortex [23], but also
in both simple and complex cells of V 1/A 17 and, more
commonly, V2/A18. Responses are found to illusory con-
tour stimuli (Figure 1c) in monkey V2 [24,25],
noise-defined bars (Figure 1e) in monkey Vl [26""], con-
trast e nvelopes (Figure 1b) in cat A17 and A18
[6,10 .. ,27,28"], and texture -defined bars (Figure 1d) in cat
A18 [29""]. In many of these studies, at least some neurons
respond as strongly to second-order as to luminance-
defined stimuli, making it very unlikely they are mediated
by early nonlinearities.
Construction of second-order stimuli from sinewave grat-
ing components has provided a powerful approach for
analyzing the neural signal processing of second-order
stimuli. Using contrast envelope stimuli (e.g. static, high
spatial frequency sinewave grating carriers modulated by
drifting, low spatial frequency sinewave envelopes; see
Figure 1b), our group has made a detailed analysis of neu-
rons in cat A17 and A18 [6,10"",27,28"], revealing neurons
that respond to both luminance gratings and second-order
envelopes. A very surprising result is that these neurons
are narrowly tuned for quite high values of carrier spatial
freq uency - not only much higher th an the spatial
response range for first-orde r gratings, but approaching the
animal's acuity limit. The lower spatial resolution of visual
neurons in cats compared to monkey makes it an advanta-
geous choice of species for these experime nts. T hese
neurons are also bandpass tuned to the spatial and tempo-
ral frequency of envelope motion, with preferred
frequencies somewhat lower than those for first-orde r
stimuli [28"]. Optimal envelope spatial frequencies are 8-
to 30-fold lower than optimal carrier frequencies, rather
 Central neural mechanisms for detecting second-order motion Baker 463

Figure 2

Model of cortical neuron response, having

separate parallel signal-processing pathways
Linear filter
for first- and second-order stimuli.
Nonlinearities such as output thresholds and
gain controls [3•] are omitted for clarity. In the
top pathway, luminance-defined, first-order 1st order
stimuli are processed conventionally with a
linear spatiotemporal filter. The filter is
depicted as overlaid on a first-order stimulus,

~~
as in Figure 1a. The bottom pathway consists
of a serial 'filter-7rectify-7filter' cascade Response
Stimuli
consisting of early linear filtering subunits, a
nonlinearity (such as rectification), and a late
linear filter; the early and late filters are shown
superimposed on a contrast envelope
stimulus, to indicate the action of their
summation regions. The early filter controls
selectivity to the carrier texture, and the late
filter determines envelope selectivity. Note
that a first-order luminance grating could not
pass both the early and the late filters,
because of their very different spatial
selectivities. The neuron's response reflects a Current Opinion in Neurobiology
combination of both signaling pathways.

than being in a fixed ratio, as suggested by some psy-
chophysical studies of texture perception [30,31]. Optimal
envelope temporal frequencies average about 4 Hz, con-
sistent with human psychophysics [7••].
That the same neuron can show distinct optimal spatial
frequencies for luminance gratings, envelopes, and carriers
of envelopes, is inconsistent with explanations based on
early nonlinearities or other models having only a single
kind of processing for both first- and second-order stimuli.
These and other findings can be understood in terms of a
more elaborate filtering model having two signal-process-
ing pathways (Figure 2), one responding to first- and the
other to second-order stimuli [ l ,27], whose outputs are
combined. One pathway responds conventionally to first-
order stimuli, with a linear filter that determines spatial
and temporal frequency selectivity to luminance gratings.
The other pathway has an early linear filter that deter-
mines carrier spatial frequency selectivity, t hen a
nonlinearity, such as full-wave rectification (giving like-
signed responses to both positive and negative signals),
and a late filter that determines envelope spatial and tem-
poral frequency tuning. Such ' filter-Hectify~filter'
models had previously been proposed in spatial vision for
textural figure-ground segregation [32-34] and for extrac-
tion of contrast modulations contained in plaid stimuli
[35]. In texture segregation models, the first fi lter picks out
the fine grain of a texture, and the second filter responds
to boundaries between texture regions.
Note that in the 'fi lter~rectify~fi lter ' processing scheme
of Figure 2, the early-stage filters are doing a first-order
operation in their response to the carrier; however, their
response does not signal attributes of the e nvelope, such as
its orientation or direction of motion. It is the selectivity
for properties of the envelope that is the essential second-
order response provided by the later-stage filter.
In experiments independently varying carrier and envelope
orientations (Figure lt) [to••], envelope-responsive neurons
showed the same preferred orientations for e nvelopes and for
luminance gratings; however, preferred carrier and envelope
orientations had no systematic relationship to one another.
The carrier orientation tuning suggests that neurons corre-
sponding to the early filter of the filter~rectify~filter
stream (Figure 2) are in the visual cortex.
Some psychophysical studies have supported the neuro-
physiological findings of carrier spatial frequency selectivity
-masking of contrast envelope motion that is specific to
carrier spatial frequency [22•] and a failure of apparent
motion when successive exposures are alternately defined by
first- and second-order patterns [7"•,36]. However, in second-
order apparent motion of grating-like micropatterns [13•,37],
the carrier spatial frequency or orientation can be changed on
successive flashes, suggesting that some second-order mech-
anisms may have broadband early filtering.
Extrastriate specialization for first- and
second-order motion processing
As first- and second-order information could be useful for dif-
ferent visual functions, it would not be surprising if
specialized extrastriate brain areas make differential use of
them. Neurons in primate extrastriate area MT (VS) and
nearby areas show responses to dynamic noise bar stimuli
(Figure le) [23,38], texture-defined stimuli [39], and contrast
envelopes [40], whereas inferior temporal cortex cells respond
to texture-defined stimuli [4 1]. It is difficult to conclude on
464 Sensory systems
the basis of these studies, however, whether extrastriate visu-
al areas are specialized for first- or second-order processing.
Evidence for such specialization has come instead from neu-
ropsychology and neuroimaging approaches.
Because only a fraction of cortical neurons have been found
to respond to second-order stimuli, a nonspecific brain
impairment might appear relatively more damaging to sec-
ond- than to first-order processing [42]. Vaina and
colleagues have reported the particularly striking finding of
two patients, one having a relatively greater deficit for per-
ception of second-order stimuli [43] and the other having a
deficit specific for first-order stimuli ([44•]; see also [45]).
Anatomic MRI showed that these patients have brain
lesions in different extrastriate cortical regions [46••]. This
'double dissociation' lends further support to the notion
that the two kinds of stimuli are processed separately, and
strongly suggests extrastriate specializations for them.
Neuroimaging is a promising approach for exploring
extrastriate specialization. However, a potentially serious
problem is to ensure that a measured response to a second-
order stimulus is not merely attributable to first-order
mechanisms responding to the carrier texture, rather than
to the envelope or texture boundary. While this question is
straightforward to disambiguate for a single, narrowly
tuned neuron [6,10••], it is more challenging for the broad-
band population response of a brain region. Using fMRI to
measure responses to a variety of first- and second-order
motion stimuli in humans, Smith eta/. [4]-•] found that Vl
and most identified extrastriate visual areas respond to
both; however, one area (identified as V3) responded more
to second- than to first-order motion, or to the carrier pat-
tern presented alone, suggesting a degree of relative
specialization. Van Oostende eta/. [48] report that fMRI
responses to motion-defined stimuli selectively activate a
different extrastriate area. Using PET imaging of respons-
es to plaid stimuli, and subtracting the responses to the
grating components, Wenderoth eta/. [49•] obtained a net
response consistent with the contrast modulation compo-
nent of the plaid, which they localized to an extrastriate
visual region.
Function of second-order processing
In natural vision, second-order information (much like
chromatic information) does not usually occur in isolation,
but with correlated luminance information. Thus, it should
nqt be surprising that all neurons found to be responsive to
second-order stimuli are also responsive to first-order stim-
uli. A popular and perhaps related interpretation of this
result is in terms of 'form-cue invariance' [23], the notion of
a mechanism selective for attributes such as contour orien-
tation or direction of motion, regardless of the nature by
which the contour is defined (e.g. by differences of lumi-
nance, contrast, texture, etc). This idea is supported for
envelope orientation and direction of motion
[lo••,26••,27,29••], and roughly, if not exactly, for envelope
spatial frequency [28•]; however, the selectivity of contrast
envelope responsive neurons to carrier spatial frequency
and orientation [10••,27] represents a lack of invariance that
suggests some modification of the concept.
In principle, there are some natural situations in which
second-order information should be particularly useful,
such as disambiguating shadows, handling transparency
[SO], or detecting moving, texture-covered objects whose
constituent texture motion is irrelevant (such as pouncing
predators, fleeing prey, or approaching soccer balls) [51].
The filter-Hectify~filter processing scheme thought to
subserve second-order detection is potentially a very gen-
eral and powerful way to extract image structure not
revealed by conventional linear filtering, such as illusory
contours and other kinds of texture borders. Extraction of
second-order information may be an important element in
subsequent computation of higher-order image structure,
such as plaids [35], terminators [52•], some forms of com-
plex motion [53,54•], and non-Cartesian analysis [Ss••].
A potential problem with this processing scheme is the
very large number of combinations of filters needed to pro-
vide a complete basis set for representing higher-order
image structure. This problem may be less serious than it
seems as a result of constraints such as the limited range of
optimal carrier spatial frequencies and the broad band-
widths of optimal carrier orientations [lo••,27,28•]. Also, in
view of the broadband nature of natural images, a truly
complete representation may not be necessary.
Conclusions
While the scheme of separate signal-processing pathways
for first- and second-order information is now well support-
ed by human psychophysics, single-unit electrophysiology,
and evidence for extrastriate specialization, there have not
been any reports of single neurons that respond exclusively
to second-order stimuli. This discrepancy could be a simple
consequence of the protocols commonly used to search for
visually responsive neurons, in which initial assessments are
performed with simple luminance-defined stimuli.
It has been an implicit assumption throughout this review
that there are common kinds of mechanisms underlying
second-order motion, texture segregation, and perception
of illusory contours [Ss••], though much of the research on
these phenomena has proceeded somewhat independent-
ly. Whether this is so, or to what extent these different
kinds of stimuli are detected by fundamentally different
mechanisms, is an important contemporary research ques-
tion. Indeed, the present distinction of first- and
second-order motion may well stand in need of substantial
revision, as some have already suggested [56], as new
results and insights emerge.
Acknowledgements
My research is supported by Canadian Medical Research Council (MA9685)
and National Science and Engineering Research Council (OGP0001978)
grants. I am grateful to Robert Hess. Fred Kingdom. Tim Ledgeway, and
Nick Scott-Samuel for their comments on the manuscript.
 Central neural mechanisms for detecting second-order motion Baker
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