Discussion
The aim of the present MEG study was to identify areas in the visual
cortex of the human brain that contribute to an attentional enhancement
of steady state amplitudes with attention. In a typical spatial
attention task, after a baseline period, subjects were given an
instructive cue to shift attention to the left or right visual hemifield
and to perform a task at the to-be-attended side. Different from many
studies, we controlled for the attentional deployment before the cue by
instructing to either attend to central fixation or to both stimuli in
the left and right visual hemifield, respectively. Compliance was
assured by having a task at the respective location during the baseline
as well as in the post-cue period. With this manipulation, we were able
to test SSVEF sensory gain modulations for peripheral stimuli under the
conditions that attentional resources were shifted to this peripheral
stimulus (attend cross) or away from an already attended peripheral
stimulus (attend rings). Behavioral data showed that subjects were
compliant with the task, although the “attend cross” condition seemed
to be more difficult compared to the “attend rings” baseline
condition.
Comparing the baseline conditions, we found a differential activation in
early visual cortex. In particular, when subjects were instructed to
attend to both rings, activation was not just restricted to V1 and V2,
as for the “attend cross” baseline, but also included
occipito-parietal cortex, and hMT+. Given that hMT+ was only activated
in the “attend rings” pre-cue baseline period is in line with previous
reports on hMT+ activation by motion and also by flickering stimuli
(Treue and Martinez-Trujillo 1999, Huk and Heeger 2002, Palomares et al.
2012). Surprising to us was that this additional activation in that
baseline condition was more prominent in the right cortical hemisphere
(but numerically in the left hemisphere as well, see Figure 3B), whereas
V1/V2 activation was clearly located in both hemispheres.
The attentional activation pattern after the cue, relative to pre-cue
baseline across all areas, was different for the two pre-cue conditions.
When subjects first attended to both rings in the left and right visual
hemifield, cortical activation slightly increased for the side for which
attention was maintained, but significantly decreased for the side for
which attention was withdrawn. If, however, participants first attended
to central fixation, cortical activation was significantly increased for
the to-be-attended stimulus, and data revealed a trend for this
activation boost to be even bigger compared to when subjects attended to
both rings first. For the to-be-ignored side, activation remained
basically on the pre-cue baseline level.
However, a closer inspection on the individual activation pattern of the
respective cortical areas resembled an interactive activation pattern
that not only depended on the pre-cue condition but also on the visual
area. When subjects attended to both rings first, we observed a
reduction in activity in areas V1, V2, pre-cuneus, occipital parietal
and inferior-temporal cortex for the to-be-ignored stimulus, whereas for
the to-be-attended ring activity basically remained at the pre-cue
level. Thus, all areas followed the pattern we observed in the test
across all areas (see above). Critically, when subjects attended to the
fixation cross first, the SSVEF modulation patterns differed
significantly between the cortical areas within the visual cortex. In
V1, V2, pre-cuneus and occipital parietal cortex SSVEF power followed a
similar pattern as during the pre-cue attend to both rings baseline. The
SSVEF amplitudes elicited by the to-be-ignored hemifield flickers were
suppressed. However, the to-be-attended flickers generated a greater
SSVEF power boost after participants attended the central fixation cross
than after having split their attention between both hemifields during
the ring pre-cue baseline task. On the contrary, hMT+ and
inferior-temporal cortex did not show a further reduction in activity
for the to-be-ignored ring and no enhanced boost of SSVEF amplitudes for
the to-be-attended hemifield after the fixate central cross pre-cue
task.
The present observations nicely match our very simple previous source
reconstructions of EEG data in feature-based attention (Andersen et al.
2008, Andersen and Müller 2010). When subjects attended to red or blue
spatially superimposed random dot kinematograms (RDKs) we also found the
sources of the attention effect in early visual cortex only, including
V1/V2. While it is quite clear that V1/V2 show prominent responses to
flicker stimuli in the respective stimulation frequency plus its
harmonics (Rager and Singer 1998) it is still unknown how far flicker
responses propagate in the visual processing hierarchy. A number of
physiological restrictions suggest that propagation is restricted to
areas of early visual cortex, due to dendritic low-pass filtering, in
particular for higher flicker frequencies (Fortune and Rose 1997, Vaidya
and Johnston 2013), increase in receptive field size (Hubel and Wiesel
1968), or synaptic input from cells that respond to different flicker
frequencies, resulting in so-called intermodulation frequencies (Zemon
and Ratcliff 1984). The idea that propagation of the respective driving
frequencies is limited to early processing stages was also demonstrated
in fMRI (Di Russo et al. 2007, Palomares et al. 2012).
The activation pattern in early visual cortex when subjects first
attended central fixation nicely resembles the pattern of SSVEP
amplitude time courses in spatial shifting designs (Müller et al. 1998,
Müller 2008). In these studies, SSVEP amplitude for the to-be-ignored
side remained on pre-cue baseline level, whereas SSVEP amplitude for the
to-be-attended side exhibited a significant increase. However, the
pattern of amplitude modulations differed in study by Gundlach and
colleagues (2020) that used the same design as in the present study. In
this study, when subjects first attended to the fixation cross, an
increase in SSVEP amplitudes for both, the to-be-attended and unattended
side was found, of course with a significantly greater increase for the
to-be-attended side. When subjects attended to both rings first, we
found no change in amplitude for the side that needed to be ignored
after the cue, but only a significant increase for the then selected
side. The difference between the more recent and the previous studies
may lie in the fact that in the most recent study we used a very broad
range of posterior electrodes including midline electrodes, whereas in
the two older studies we only used one posterior-temporal electrode
left/right, respectively for SSVEP time course analysis. This broader
cluster might have picked-up activity from many more cortical areas. In
previous studies we have shown that the pattern of SSVEP amplitude
modulation is not identical over a broader range of electrodes as used
in the 2020 study (Andersen et al. 2012, Müller et al. 2018), and
therefore, it might be of interest to reanalyze this data with a more
temporal and much smaller electrode cluster, or even single electrodes.
In addition, as the focus of the work by Gundlach and colleagues (2020)
focused on the relationship between SSVEP and alpha-band modulations in
a spatial cueing paradigm, the SSVEP amplitudes were derived from
single-trial FFT spectra. With such an analysis, induced activity of
non-phase locked ongoing neural oscillatory activity is not averaged out
and may contribute to the SSVEP amplitude estimates in the same
frequency range. In the current study, however, SSVEP amplitude values
were derived from trial-averaged FFT spectra promoting evoked signals
such as SSVEPs while minimizing induced signals such as endogenous
neural activity not phase locked to the stimulation. While the relative
amplitude patterns (attended > unattended) are comparable,
differences in the absolute amplitude may stem from differences in
foundations of the signals revealed by different analysis approaches.
To summarize: The present study replicated previous studies that located
cortical sources of SSVEPs driven by flickering (frequency-tagged)
stimuli in early visual cortex. Our results complement and extend these
studies showing that early visual cortex also drives attentional
modulations of SSVEP amplitudes. While the activation pattern in V1/V2
was consistent, the specific modulatory effects differed across
different regions within early visual cortex with a distinct pattern
further up in the processing hierarchy in areas such as hMT+ and
inferior-temporal cortex in the present case. Nevertheless, results
again demonstrate the power of frequency-tagged stimuli to investigate
attentional competitive interactions in multi-element stimulus displays.
To what extent a certain area that is specialized in processing of a
certain feature, such as V4 for color, contributes significantly more to
the observed SSVEP amplitude modulations in color processing, compared
to the other areas that “just” follow the on/off is subject to a
current project and we will report the results in the nearer future.