Functional MRI in the Awake Monkey: The Missing Link
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Functional MRI in the Awake Monkey: The Missing Link
Guy A. Orban
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Functional imaging in humans, first with positron emis- tizing the monkey and administering a muscle relaxant
sion tomography and now using functional magnetic and increased the BOLD signal by using a high-field
resonance imaging (fMRI), has become a major tool of magnet (4.7 T). This allowed them to produce ‘‘focal,
neuroscientists in the study of cerebral systems. It allows reproducible stimulus-induced MR changes’’ (Logothetis,
in vivo mapping of human cerebral regions engaged in Guggenberger, Peled, & Pauls, 1999). Rotating checker-
an endless variety of sensory, motor, and cognitive boards alternating on and off evoked activity that could
conditions. Because these imaging techniques provide be attributed to the lateral geniculate nucleus, primary
indirect measurements of the activities of large popula- visual cortex, and extrastriate areas, including V4 and
tions of neurons, their interpretation can benefit tre- MT/ V5. Comparing faces to scrambled versions of the
mendously from links to the wealth of information same images evoked activity in the superior temporal
obtained in nonhuman primates using more invasive sulcus and amygdala. The same anesthetized prepara-
techniques such as the properties of single neurons, tion was also used in two somatosensory studies using
anatomical connections, and behavioral effects of con- 1.5-T magnets (Disbrow, Slutsky, Roberts, & Krubitzer,
trolled lesions or temporary inactivations. Unfortunately, 2000; Hayashi, Konishi, Hasegawa, & Miyashita, 1999).
this comparison has been hampered by the confound The Hayashi study revealed that face and hand repre-
between differences in species and in techniques. sentations in somatosensory cortex (SI and SII) can be
Because it is difficult to record from single neurons in distinguished at 1.5 T. The second study compared in
humans, the most logical step has been to develop fMRI the same animals the single-cell- and fMRI-defined so-
in the monkey. The first to realize the importance of this matotopic maps. In some cases, the match between the
approach were Stefanacci et al. (1998), who showed that two types of maps was good, but mislocalization of the
blood oxygenation level-dependent (BOLD) fMRI was fMRI signal up to 1 cm from the actual single-cell activity
feasible in the awake monkey. Activity in voxels tenta- was observed. Directional asymmetries in the mislocal-
tively identified as belonging to the extrastriate cortex izations suggested that the BOLD signal likely originated
(V2) correlated with the visual stimulus presentation: near the draining veins rather than the neuronal source.
a video presentation alternating with total darkness. Draining veins, particularly the sagittal sinus, were also
Without their impetus, we, like others (E. DeYoe and the likely source of the dominant signal in the reports of
C. Olson, cited in Stefanacci et al., 1998) who failed to Dubowitz et al. (1998) and Stefanacci et al. (1998).
obtain fMRI signals in anesthetized monkeys, would One potential benefit of developing fMRI in monkeys
have abandoned the effort. A heavily attended historic is that it will allow one to directly compare neuronal
session at the 1998 Society for Neuroscience meeting in activity and MR activity, which should provide the
Los Angeles revealed that three vision laboratories, at much needed information about the physiological basis
Caltech, Max-Planck-Institut Tübingen, and Katholieke of the functional MR signal. There are at least three
Universiteit Leuven, were following suit. In a brief unanswered questions about the functional MR (BOLD
report, researchers from Caltech (Dubowitz et al., or other) signals (for the first two, see also Heeger &
1998) confirmed that a blocked ‘‘on – off’’ paradigm Rees, 2002): (1) Where is the neuronal activity giving
(25-sec movie alternating with complete darkness) rise to the functional MR signal localized to? (2) What
evoked correlated fMRI activity, measurable with a type of activity (single-unit, multiple-unit, or local field
standard 1.5-T magnet and a knee coil, in discrete areas potentials) underlies the MR signal? (3) How does the
of the visual cortex of a single awake monkey. activity level in a population measured by fMRI relate
In addition to the low signal-to-noise ratio of the to the selectivity and tuning curves revealed in single-
BOLD signal and an absence of retinal position control, unit studies? Regarding the first two questions, only
the main problem revealed by these two preliminary one study published thus far has simultaneously meas-
reports was brain motion during scanning. The ured neural activity and BOLD signal. Logothetis, Pauls,
Tübingen group eliminated motion artifact by anesthe- Augath, Trinath, and Oeltermann (2001) demonstrated
that at high field (4.7 T), the MR activity is colocalized
with neuronal activity (although it is difficult to avoid a
small susceptibility artifact at the very tip of the
Katholieke Universiteit Leuven, Belgium electrode). The BOLD signal was more closely correlated
D 2002 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 14:6, pp. 965 – 969
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902760191171 by guest on 15 October 2021with the local field potential than with multiunit or Overcoming brain motion during scanning is neces-
single-cell activity. The third question involving the sary for successful awake behaving monkey fMRI studies.
relationship between fMRI activity and neuronal selec- In addition, for monkey fMRI to gain widespread use,
tivity is more difficult to answer. For example, neurons in one needs to find a way to increase the signal-to-noise
area MT/ V5 are tuned to direction (Albright, 1984), ratio without resorting to expensive vertical high-field
where the neuronal response varies from zero to a scanners. Our laboratory has achieved this using the
maximum (200 spikes/sec or so) when direction is following approach ( Vanduffel et al., 2001). First, we
varied. The average population, however, will respond train monkeys to remain immobile in the adverse MR
equally well to all directions since equal proportions of environment so that standard motion correction algo-
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neurons are tuned to different directions (provided one rithms are sufficient to correct for brain motion, as is
averages over regions exceeding columnar width). routinely done in humans. Second, to obtain adequate
Hence, the BOLD signals recorded from MT/ V5 will MR signal at 1.5 T, we use a contrast agent administered
not depend on direction, a result that could, however, intravenously: monocrystalline iron oxide nanoparticle
equally well reflect a neuronal population that does not (MION), developed at Massachusetts General Hospital
code direction. Thus, at present, a given BOLD signal (Weissleder et al., 1990). MION measures blood volume,
may arise from selective or nonselective neuronal pop- rather than a mixture of flow, volume, and oxygenation.
ulations. One way to make this distinction has been to This type of imaging has two advantages over BOLD
use adaptation paradigms in monkeys (Tolias, Smirnakis, fMRI: The sensitivity of the measurement is increased by
Augath, Trinath, & Logothetis, 2001) as in humans (Huk, a factor of 5 and the MR signal is localized more clearly
Rees, & Heeger, 2001; Kourtzi & Kanwisher, 2001; Grill- to the brain parenchyma and is less affected by draining
Spector et al., 1999). The basic tenet of the adaptation veins (see also Leite et al., 2002). Currently, it is possible
paradigm is that if neurons are tuned for a given to obtain functional images with a spatial resolution of
parameter, adapting them with a fixed value of this 2-mm isotropic voxels. The MION contrast agent is also
parameter will decrease the response in a subset of superior to magnetite dextran nanoparticles, which was
neurons (those tuned to that value) and the average used in the Dubowitz, Bernheim, Chen, Bradley, and
response, and hence the fMRI signal, will be larger for a Andersen (2001) study, since it has increased sensitivity
nonadapted than the adapted value of the parameter. (fivefold compared to threefold) and has a faster time
Full realization of the potential of monkey fMRI course. The slow time course of magnetite dextran
studies is unlikely to occur in the anesthetized prepa- nanoparticles (maximum at 40 sec compared to 5 sec
ration given its limitations (Rainer, Augath, Trinath, & for MION) allows measurement of only a small number
Logothetis, 2001; Tolias et al., 2001). First, it is impos- of functional volumes in a single session. This makes it
sible to use motor and cognitive paradigms in the difficult to reach statistical significance in more subtle
anesthetized preparation, restricting its use to the behavioral paradigms that are not simply presenting
exploration of sensory systems. Second, even in sen- stimuli on and off.
sory experiments the stimuli drive mainly the early Thus, we have now reached the fortunate stage where
stages of a sensory pathway. In vision, for example, this all three experiments can be run in parallel: fMRI in
includes V1, V2, V3, MT/ V5, and perhaps V4 (Rainer humans, fMRI in awake monkeys, and single-cell record-
et al., 2001; Tolias et al., 2001, but see Logothetis et al., ings in awake monkeys ( Vanduffel et al., 2000; Orban,
1999). Recently, MR activity in higher visual regions Sunaert, Todd, Van Hecke, & Marchal, 1999; Xiao,
was reported in the anesthetized monkey (Sereno, Marcar, Raiguel, & Orban, 1997). This should open the
Trinath, Augath, & Logothetis, 2002) but the signals door to major progress in systems and cognitive neuro-
were too weak for differences in ‘‘subtle’’ comparisons science. For example, one can now directly compare
(e.g., between different types of visual stimuli rather visual cortex in human and nonhuman primates using
than between a visual stimulus and nonstimulus) to fMRI, addressing homology questions directly. It is likely
reach statistical significance. Third, even if BOLD activ- that further differences will appear, although one such
ity is detected in a cortical area of the anesthetized difference is already known. fMRI studies have demon-
preparation it may reflect neuronal properties altered strated that human V3A (Tootell et al., 1997) occupies
by the anesthesia ( Vanduffel, Tootell, Schoups, & the same location in the cortex (anterior to V3) and has
Orban, 2002; Pack, Berezovskii, & Born, 2001) or an a similar retinotopic organization in the two species, yet
altered set of anatomical inputs, because some of the it is motion sensitive in humans, while monkey V3A is
afferent areas are silenced by the anesthesia. Finally, not ( Vanduffel et al., 2001). How many differences one
any comparison of human studies with fMRI and fMRI can tolerate and still consider regions as homologous in
in anesthetized monkey will be difficult. Hence, obtain- the two species is a subject for future debate. It is useful
ing focal, stimulus-induced MR signal changes in the to remember that in monkey, cortical areas are defined
awake monkey, where the same wide variety of para- by convergent evidence of four criteria: architectonics,
digms can be used as in humans, would represent connections, topographic organization (e.g., retinotopy),
considerable progress. and functional properties. The latter two criteria can be
966 Journal of Cognitive Neuroscience Volume 14, Number 6
Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892902760191171 by guest on 15 October 2021addressed by fMRI, with some restrictions upon the signal will allow the derivation of appropriate paradigms
properties as noted above. Connections may be ascer- for unmasking neuronal selectivity in MR signal, that is,
tained indirectly with human imaging using diffusion the MR signal level reflects activity of neurons tuned to
tensor imaging and multivariate methods that assess the dimension manipulated. In this case, all regions
functional and effective connectivity (Friston & Büchel, activated in a given fMRI paradigm will be characterized
2000). Furthermore, in vivo tracing of anatomical con- by large proportions of selective neurons. Clearly, that
nections with MRI has been demonstrated in monkeys was not the case for the kinetic grating paradigm
(Saleem et al., 2001). Cyto- and myeloarchitectonics mentioned above: Kinetic gratings of different orienta-
are increasingly used to parcel human cortex (e.g., Zilles tions were presented but this stimulation activated
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et al., 1995). regions such as MT/ V5, which contains no neurons
In addition to addressing possible homologies be- tuned to kinetic grating orientation. The adaptation
tween cortical organization in human and nonhuman paradigm mentioned above is an example of an appro-
primates (Nakahara, Hayashi, Konishi, & Miyashita, priate paradigm, but others should follow.
2002), one can now compare, in the same awake The development of such appropriate paradigms will
monkey, single-cell recordings and fMRI maps. This further enhance the use of fMRI in the awake monkey
approach allows one to clarify the relationship between for scouting monkey cerebral cortex with new stimuli
single-cell activity and population activity measured by and/or tasks. The progress in understanding extrastriate
fMRI. For example, when BOLD signal increases with cortex and other cerebral systems has been slow,
increased attention during a visual paradigm, as is because of the lack of such an exploratory tool. Indeed,
frequently observed, at least two scenarios can apply it takes about a year to complete a monkey single-cell
at the single-cell level. Either all neurons increase their study in a given cortical region with a given set of stimuli
firing rate or only a subset of neurons fire more strongly. and to decide whether that region is involved in the
Similarly, a decrease in activation can be due to a processing of that particular feature or a given cognitive
general decrease in activity throughout the population operation. Hence, the approach has been very con-
or it can be restricted to a subset of neurons that might servative. Since the early days following its discovery
actually become more selective (and thus fire for fewer (Dubner & Zeki, 1971), area MT/ V5 has been associated
stimuli). Another example illustrates the question of the with motion perception, because of the prevalence of
relationship between functional MR signals and neuro- direction selective neurons. As witnessed by the number
nal selectivity. Kinetic boundaries can, under certain of articles on MT/ V5 neurons, a young student starting
circumstances, activate monkey MT/ V5 as observed by out to address an aspect of motion processing will be
fMRI (Fize et al., 2001). Yet single-cell studies (Marcar, tempted to begin in MT/ V5, thus fueling the circular
Xiao, Raiguel, Maes, & Orban, 1995) have shown that reasoning that MT/ V5 is involved only in motion pro-
MT/ V5 neurons do not encode kinetic boundary orien- cessing. The pace of progress will change dramatically, if
tation or position. Furthermore, lesions of MT/ V5 do in one or two afternoons, one can test a new set of
not impair orientation judgments of kinetic contours stimuli, as we have been able to do recently. Multiple
(Lauwers, Saunders, Vogels, Vandenbussche, & Orban, new stimuli can then be tested easily and new avenues
2000). Thus, the MT/ V5 activation by kinetic contours explored. Furthermore, the same monkey can be tested
observed in the fMRI must be nonspecific, probably repeatedly so that many functional maps can be com-
reflecting the antagonistic surrounds that are ubiquitous pared in the same individual, eliminating effects of
in this area (Raiguel, Van Hulle, Xiao, Marcar, & Orban, interindividual and experimental differences. This
1995; Tanaka et al., 1986; Allman, Miezen, & McGuin- should provide a much clearer picture of the functional
ness, 1985). Due to these surrounds, a number of MT specialization of the cortical regions and help define
neurons will respond better to the kinetic boundary different cortical areas more precisely.
stimulus than to the transparent stimulus, because the fMRI in the awake monkey is the technique we have
kinetic boundary happens to be aligned with the border been waiting for since the discovery of the anatomical
separating the surround from their receptive field. Thus, organization of extrastriate cortex in the 1970s and 1980s
the activation of area MT/ V5, and by inference that of (for a review, see Felleman & Van Essen, 1991). Indeed, it
hMT/ V5+, by kinetic gratings does not reflect activity of addresses the system at the level of its components, the
neurons selective for the orientation of the kinetic functional maps (Churchland & Sejnowski, 1988), which
gratings. Hence, it is nonspecific: The difference in MR complements the single-cell approach. The advent of
signal in the two conditions compared reflects a mod- monkey fMRI will not remove the need for single-cell
ulation of activity of a given group of neurons (some recording, on the contrary. Even if the MR signal were to
neurons with surround) unspecific for the stimulus used reflect neuronal selectivity perfectly, which is certainly
and it does not reflect the recruitment of neurons not the case at present, we will need to know the latency
specifically devoted to the analysis of the kinetic stim- and time course of the response, because fMRI will never
ulus (cells tuned to the orientation of the boundary). achieve the temporal resolution of electrophysiology.
Systematic, parallel studies of single-cell activity and MR Furthermore, one needs to investigate the precision of
Orban 967
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Orban 969
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