Monkey Cortex through fMRI Glasses
2014; Cell Press; Volume: 83; Issue: 3 Linguagem: Inglês
10.1016/j.neuron.2014.07.015
ISSN1097-4199
AutoresWim Vanduffel, Qi Zhu, Guy A. Orban,
Tópico(s)Face Recognition and Perception
ResumoIn 1998 several groups reported the feasibility of fMRI experiments in monkeys, with the goal to bridge the gap between invasive nonhuman primate studies and human functional imaging. These studies yielded critical insights in the neuronal underpinnings of the BOLD signal. Furthermore, the technology has been successful in guiding electrophysiological recordings and identifying focal perturbation targets. Finally, invaluable information was obtained concerning human brain evolution. We here provide a comprehensive overview of awake monkey fMRI studies mainly confined to the visual system. We review the latest insights about the topographic organization of monkey visual cortex and discuss the spatial relationships between retinotopy and category- and feature-selective clusters. We briefly discuss the functional layout of parietal and frontal cortex and continue with a summary of some fascinating functional and effective connectivity studies. Finally, we review recent comparative fMRI experiments and speculate about the future of nonhuman primate imaging. In 1998 several groups reported the feasibility of fMRI experiments in monkeys, with the goal to bridge the gap between invasive nonhuman primate studies and human functional imaging. These studies yielded critical insights in the neuronal underpinnings of the BOLD signal. Furthermore, the technology has been successful in guiding electrophysiological recordings and identifying focal perturbation targets. Finally, invaluable information was obtained concerning human brain evolution. We here provide a comprehensive overview of awake monkey fMRI studies mainly confined to the visual system. We review the latest insights about the topographic organization of monkey visual cortex and discuss the spatial relationships between retinotopy and category- and feature-selective clusters. We briefly discuss the functional layout of parietal and frontal cortex and continue with a summary of some fascinating functional and effective connectivity studies. Finally, we review recent comparative fMRI experiments and speculate about the future of nonhuman primate imaging. Following the introduction of human fMRI in the early 90s, four groups independently reported the feasibility of monkey fMRI in 1998 (Dubowitz et al., 1998Dubowitz D.J. Chen D.Y. Atkinson D.J. Grieve K.L. Gillikin B. Bradley Jr., W.G. Andersen R.A. Functional magnetic resonance imaging in macaque cortex.Neuroreport. 1998; 9: 2213-2218Crossref PubMed Google Scholar; N.K. Logothetis et al., 1998, Soc. Neurosci., abstract; Stefanacci et al., 1998Stefanacci L. Reber P. Costanza J. Wong E. Buxton R. Zola S. Squire L. Albright T. fMRI of monkey visual cortex.Neuron. 1998; 20: 1051-1057Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar; W. Vanduffel et al., 1998, Soc. Neurosci., abstract). Initially, disparate strategies were used, including high-field (4.7 T) blood-oxygen level-dependent (BOLD) imaging with dedicated vertical scanner bores (Logothetis et al., 2001Logothetis N.K. Pauls J. Augath M. Trinath T. Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal.Nature. 2001; 412: 150-157Crossref PubMed Scopus (2703) Google Scholar), BOLD imaging using clinical, low-field (1.5 T) MR scanners (Stefanacci et al., 1998Stefanacci L. Reber P. Costanza J. Wong E. Buxton R. Zola S. Squire L. Albright T. fMRI of monkey visual cortex.Neuron. 1998; 20: 1051-1057Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar), and cerebral blood volume fMRI using exogenous contrast agents at low field (Vanduffel et al., 2001Vanduffel W. Fize D. Mandeville J.B. Nelissen K. Van Hecke P. Rosen B.R. Tootell R.B. Orban G.A. Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys.Neuron. 2001; 32: 565-577Abstract Full Text Full Text PDF PubMed Scopus (214) Google Scholar). Since high-field MR scanning is more susceptible to motion-induced imaging artifacts, the initial studies in vertical scanners were primarily performed in anesthetized animals (Hayashi et al., 1999Hayashi T. Konishi S. Hasegawa I. Miyashita Y. Short communication: mapping of somatosensory cortices with functional magnetic resonance imaging in anaesthetized macaque monkeys.Eur. J. Neurosci. 1999; 11: 4451-4456Crossref PubMed Scopus (25) Google Scholar, Logothetis et al., 2001Logothetis N.K. Pauls J. Augath M. Trinath T. Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal.Nature. 2001; 412: 150-157Crossref PubMed Scopus (2703) Google Scholar, Sereno et al., 2002Sereno M.E. Trinath T. Augath M. Logothetis N.K. Three-dimensional shape representation in monkey cortex.Neuron. 2002; 33: 635-652Abstract Full Text Full Text PDF PubMed Scopus (101) Google Scholar). This motion issue could be largely mitigated by using contrast agents at low field, increasing the contrast-to-noise ratio by ∼5 at 1.5 T and ∼3 at 3 T (Vanduffel et al., 2001Vanduffel W. Fize D. Mandeville J.B. Nelissen K. Van Hecke P. Rosen B.R. Tootell R.B. Orban G.A. Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys.Neuron. 2001; 32: 565-577Abstract Full Text Full Text PDF PubMed Scopus (214) Google Scholar). Later improvements included developments of implanted focal single loop coils (Logothetis et al., 2002Logothetis N. Merkle H. Augath M. Trinath T. Ugurbil K. Ultra high-resolution fMRI in monkeys with implanted RF coils.Neuron. 2002; 35: 227-242Abstract Full Text Full Text PDF PubMed Scopus (94) Google Scholar), external phased array coils (Ekstrom et al., 2008Ekstrom L.B. Roelfsema P.R. Arsenault J.T. Bonmassar G. Vanduffel W. Bottom-up dependent gating of frontal signals in early visual cortex.Science. 2008; 321: 414-417Crossref PubMed Scopus (115) Google Scholar), spin-echo imaging (Ku et al., 2011Ku S.P. Tolias A.S. Logothetis N.K. Goense J. fMRI of the face-processing network in the ventral temporal lobe of awake and anesthetized macaques.Neuron. 2011; 70: 352-362Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar), and implanted phased array coils (Janssens et al., 2012Janssens T. Keil B. Farivar R. McNab J.A. Polimeni J.R. Gerits A. Arsenault J.T. Wald L.L. Vanduffel W. An implanted 8-channel array coil for high-resolution macaque MRI at 3T.Neuroimage. 2012; 62: 1529-1536Crossref PubMed Scopus (7) Google Scholar). Here we provide an overview of what has been achieved using fMRI in alert monkeys over the past 15 years, focusing on the visual system, by far the most investigated modality. We shall argue that functional imaging in animals is highly complementary to traditional invasive methods and may vastly increase the "yield" of such methods in future investigations by guiding large-scale electrophysiological recordings and focal reversible perturbation experiments. The role of nonhuman primate fMRI in systems neuroscience will only increase as sensitivity and spatiotemporal resolution are further refined. Moreover, comparative imaging will provide crucial insights into brain evolution and will prove essential for integrating the wealth of invasive animal results with the ever-expanding human imaging data sets. In this Review, we will first describe how fMRI provides a parcellation of visual cortex in individual, living subjects, using retinotopic mapping, paving the way for further characterization of cortical areas and functional networks. We will also show how monkey fMRI reconciled human imaging with single-cell studies by mapping category-selective regions, including cortical patches preferentially processing faces, bodies, or places, and by guiding recordings from these patches. Next, we will briefly describe the efforts to use fMRI in active subjects performing motor and cognitive tasks, which reveal the functional properties of parietal and (pre)frontal monkey cortex. Following a brief evaluation of a burgeoning human imaging field, i.c. resting-state fMRI, we will emphasize a distinctive contribution of monkey fMRI: the possibility to combine refined perturbations of cortical areas with imaging, allowing us to make causal instead of correlational-based inferences about the participation of specific brain regions in cognitive or perceptual processing. Finally, we will review comparative monkey-human fMRI studies providing unique insights into cortical primate evolution, and we will conclude with studies directly linking electrophysiology, monkey imaging, and human fMRI. Primates rely heavily on vision for interacting with the environment and with their (non)conspecifics. This is reflected in the extent of cortical surface specialized for processing visual information. Using myeloarchitectonics, connectivity, and receptive field mapping data, involving large cohorts of animals in dozens of laboratories, more than 30 visual areas have been identified in nonhuman primates, spanning half of the cerebral cortex (Felleman and Van Essen, 1991Felleman D.J. Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex.Cereb. Cortex. 1991; 1: 1-47Crossref PubMed Google Scholar). Considerable information regarding the topography and function of visual areas has been gleaned from such electrophysiological and tractography-based mapping studies. However, even at relatively early stages of the visual system, the number and exact definition of visual areas remain heavily debated because of the sequential nature of the recordings, their finite sampling size, problems inherent to reconstructing electrode tracts in 3D space, and interpolation issues across subjects and experiments. After more than half a century of such efforts, functional imaging in nonhuman primates has finally allowed investigators to obtain detailed topographic information in a noninvasive manner across the entire brain of individual living subjects, obviating most of the issues raised above. Initially, fMRI-based retinotopic mapping in monkeys, using either anesthetized high-field BOLD (Brewer et al., 2002Brewer A.A. Press W.A. Logothetis N.K. Wandell B.A. Visual areas in macaque cortex measured using functional magnetic resonance imaging.J. Neurosci. 2002; 22: 10416-10426PubMed Google Scholar) or awake low-field cerebral blood volume paradigms (Fize et al., 2003Fize D. Vanduffel W. Nelissen K. Denys K. Chef d'Hotel C. Faugeras O. Orban G.A. The retinotopic organization of primate dorsal V4 and surrounding areas: A functional magnetic resonance imaging study in awake monkeys.J. Neurosci. 2003; 23: 7395-7406PubMed Google Scholar, Vanduffel et al., 2002Vanduffel W. Fize D. Peuskens H. Denys K. Sunaert S. Todd J.T. Orban G.A. Extracting 3D from motion: differences in human and monkey intraparietal cortex.Science. 2002; 298: 413-415Crossref PubMed Scopus (170) Google Scholar), confirmed the alternating representations of vertical (VM) and horizontal meridians (HMs) between V1-V2, V2-V3, and V3-V4, respectively, with a horizontal meridian as the anterior border of V4 (Figure 1). Each area contains a representation of the entire contralateral hemifield, with segregated upper and lower quadrants (split-field representation). Evidence for additional visual field maps anterior to ventral V4 was scant in these original studies, except that a foveal and lower field representation in ventral cortex was attributed to TEO. Area V3A is located on the anectant gyrus at the junction between the parieto-occipital and lunate sulci. Within the visual hierarchy, this is the first region located exclusively in dorsal visual cortex containing a representation of both the upper and lower quadrants, split by a horizontal meridian (complete hemifield). The foveal representation of area V3A is separated from the central foveal confluence of areas V1 through V4 and a vertical meridian representation borders V3A posteriorly and anteriorly. However, unlike V1–V4, area V3A could not be identified consistently in all subjects, and the definitions of V3A differ slightly in the Brewer et al., 2002Brewer A.A. Press W.A. Logothetis N.K. Wandell B.A. Visual areas in macaque cortex measured using functional magnetic resonance imaging.J. Neurosci. 2002; 22: 10416-10426PubMed Google Scholar and Fize et al., 2003Fize D. Vanduffel W. Nelissen K. Denys K. Chef d'Hotel C. Faugeras O. Orban G.A. The retinotopic organization of primate dorsal V4 and surrounding areas: A functional magnetic resonance imaging study in awake monkeys.J. Neurosci. 2003; 23: 7395-7406PubMed Google Scholar studies. This may reflect the complex folding pattern within parts of the lunate sulcus or variability in retinotopic organization of V3A across subjects. An organization similar to that of V3A was initially ascribed to area MT (middle temporal area) in those initial monkey fMRI studies: a horizontal meridian split a ventral upper-quadrant representation from a dorsally located lower field. Moreover, a vertical meridian separated this area from its neighbors, including the fundus superior temporal area (FST), although these were not described in detail. A more recent study investigated MT and its surrounding areas in more detail using high-resolution (7 Tesla, 0.75 mm isotropic voxels) phase-encoded retinotopic mapping (Kolster et al., 2009Kolster H. Mandeville J.B. Arsenault J.T. Ekstrom L.B. Wald L.L. Vanduffel W. Visual field map clusters in macaque extrastriate visual cortex.J. Neurosci. 2009; 29: 7031-7039Crossref PubMed Scopus (39) Google Scholar). Results showed that MT and its immediate neighbors are organized as a visual-field map cluster (Wandell et al., 2005Wandell B.A. Brewer A.A. Dougherty R.F. Visual field map clusters in human cortex.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005; 360: 693-707Crossref PubMed Scopus (124) Google Scholar) with a shared foveal representation surrounded by a semicircular representation of isoeccentric contours (Figure 1). This foveal representation, distinct from the central foveal confluence of V1–V4, is located in the posterior bank of the superior temporal sulcus (STS). When phase reversals along isoeccentricity lines were plotted, clear evidence emerged for a lower vertical meridian at the V4t-MT border, and an upper vertical meridian between MT and MSTv (ventral middle superior temporal area). There is again a lower vertical meridian between the latter areas and FST, and an upper vertical meridian at the anterior border of FST. Thus, MT, MSTv, and FST each contain a complete contralateral visual field, while in V4t only the upper quadrant is represented, although the lower visual field representation may have remained undetected in V4t (Figure 1). In addition, Kolster et al., 2009Kolster H. Mandeville J.B. Arsenault J.T. Ekstrom L.B. Wald L.L. Vanduffel W. Visual field map clusters in macaque extrastriate visual cortex.J. Neurosci. 2009; 29: 7031-7039Crossref PubMed Scopus (39) Google Scholar described another full hemifield ventral to the MT cluster with a foveal representation distinct from that of the MT cluster, which they assigned to dorsal posterior inferior temporal area (PITd) in accordance with Felleman and Van Essen, 1991Felleman D.J. Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex.Cereb. Cortex. 1991; 1: 1-47Crossref PubMed Google Scholar. Subsequent studies by Kolster et al., 2014Kolster H. Janssens T. Orban G.A. Vanduffel W. The retinotopic organization of macaque occipitotemporal cortex anterior to V4 and caudo-ventral to the MT cluster.J. Neurosci. 2014; (Published online July 30, 2014)https://doi.org/10.1523/JNEUROSCI.3288-13.2014Crossref PubMed Scopus (2) Google Scholar and Janssens et al., 2014Janssens T. Zhu Q. Popivanov I.D. Vanduffel W. Probalistic and single-subject retinotopic maps reveal the topographic organization of face patches in the macaque cortex.J. Neurosci. 2014; (Published online July 30, 2014)https://doi.org/10.1523/JNEUROSCI.2914-13.2013Crossref Google Scholar described the retinotopic organization of cortex rostroventral to V4 in greater detail, using checkerboard and dynamic biologically relevant phase-encoded stimuli, respectively. Both studies showed clear evidence for a split hemifield anterior to the horizontal meridian of V4, with a contralateral lower and upper visual field rostral to dorsal and ventral V4, respectively, fitting exactly the description of V4A in earlier studies (Zeki, 1971Zeki S.M. Cortical projections from two prestriate areas in the monkey.Brain Res. 1971; 34: 19-35Crossref PubMed Google Scholar). Rostral to V4A and distinct from the MT cluster, three additional hemifields were found. The first, termed dorsal occipitotemporal area (OTd), was interposed between V4A and V4t of the MT cluster sharing a lower vertical meridian with V4A and an upper vertical meridian with PITd. The latter area extended more rostrally to a lower vertical meridian that bordered, at least partially, a more caudoventral field map, ventral PIT (PITv). PITv shared an upper vertical meridian with ventral V4A, more caudally. The Janssens et al., 2014Janssens T. Zhu Q. Popivanov I.D. Vanduffel W. Probalistic and single-subject retinotopic maps reveal the topographic organization of face patches in the macaque cortex.J. Neurosci. 2014; (Published online July 30, 2014)https://doi.org/10.1523/JNEUROSCI.2914-13.2013Crossref Google Scholar study showed that V4A, PITd, PITv, and OTd shared a common foveal representation, clearly distinct from the central foveal confluence (of V1–V4) or the MT cluster (V4t, MT, MSTv, FST) (Figure 1). Hence in monkey occipitotemporal cortex, at least three separate visual field map clusters can be identified, indicating an evolutionarily preserved and fundamental organizational principle of primate visual cortex (Kolster et al., 2009Kolster H. Mandeville J.B. Arsenault J.T. Ekstrom L.B. Wald L.L. Vanduffel W. Visual field map clusters in macaque extrastriate visual cortex.J. Neurosci. 2009; 29: 7031-7039Crossref PubMed Scopus (39) Google Scholar). As Wandell et al., 2005Wandell B.A. Brewer A.A. Dougherty R.F. Visual field map clusters in human cortex.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005; 360: 693-707Crossref PubMed Scopus (124) Google Scholar proposed, such clustering may be the most efficient manner for minimizing neural distance between processing modules requiring strong functional interactions. The Janssens et al., 2014Janssens T. Zhu Q. Popivanov I.D. Vanduffel W. Probalistic and single-subject retinotopic maps reveal the topographic organization of face patches in the macaque cortex.J. Neurosci. 2014; (Published online July 30, 2014)https://doi.org/10.1523/JNEUROSCI.2914-13.2013Crossref Google Scholar study also hinted at other regions anterior to the MT and PIT clusters showing foveal biases. These regions, located in the anterior bank of the STS, corresponding to the superior temporal polysensory area (STP), and cortex in the middle temporal gyrus, do not necessarily overlap with regions showing face selectivity, as postulated for human visual cortex (Hasson et al., 2002Hasson U. Levy I. Behrmann M. Hendler T. Malach R. Eccentricity bias as an organizing principle for human high-order object areas.Neuron. 2002; 34: 479-490Abstract Full Text Full Text PDF PubMed Scopus (185) Google Scholar). Fize et al., 2003Fize D. Vanduffel W. Nelissen K. Denys K. Chef d'Hotel C. Faugeras O. Orban G.A. The retinotopic organization of primate dorsal V4 and surrounding areas: A functional magnetic resonance imaging study in awake monkeys.J. Neurosci. 2003; 23: 7395-7406PubMed Google Scholar reported a central visual field representation within the lateral bank of the intraparietal sulcus (IPS) in the majority of the animals tested but without clear polar angle organization, consistent with published electrophysiology (Ben Hamed et al., 2001Ben Hamed S. Duhamel J.R. Bremmer F. Graf W. Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis.Exp. Brain Res. 2001; 140: 127-144Crossref PubMed Google Scholar). Recent retinotopic mapping in the monkey focusing on the IPS (Arcaro et al., 2011Arcaro M.J. Pinsk M.A. Li X. Kastner S. Visuotopic organization of macaque posterior parietal cortex: a functional magnetic resonance imaging study.J. Neurosci. 2011; 31: 2064-2078Crossref PubMed Scopus (25) Google Scholar) reported three parietal regions showing a foveal bias and crude polar angle organization. Two were located in the posterior end of the lateral bank and were named caudal intraparietal area 1 and 2 (CIP1 and CIP2). The authors showed convincing evidence for two upper vertical meridian representations designated as the borders between V3A and CIP1, and CIP2 and lateral intraparietal area (LIP), respectively, but their evidence for a lower visual field representation in CIP1/2 is rather marginal. Higher-resolution and/or more complex stimuli better suited for driving IPS neurons (instead of colored checkerboard stimuli) may eventually clarify the organization of these two higher-order areas (e.g., T. Janssens et al., 2013, Soc. Neurosci., abstract). LIP was defined in the Arcaro et al., 2011Arcaro M.J. Pinsk M.A. Li X. Kastner S. Visuotopic organization of macaque posterior parietal cortex: a functional magnetic resonance imaging study.J. Neurosci. 2011; 31: 2064-2078Crossref PubMed Scopus (25) Google Scholar study as a complete contralateral hemifield, with an upper vertical meridian at its caudal boundary with CIP2, and a lower vertical meridian as its rostral border. This region fits well with LIPv and LIPd as described in earlier electrophysiological and imaging studies (Baker et al., 2006Baker J.T. Patel G.H. Corbetta M. Snyder L.H. Distribution of activity across the monkey cerebral cortical surface, thalamus and midbrain during rapid, visually guided saccades.Cereb. Cortex. 2006; 16: 447-459Crossref PubMed Scopus (41) Google Scholar, Ben Hamed et al., 2001Ben Hamed S. Duhamel J.R. Bremmer F. Graf W. Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis.Exp. Brain Res. 2001; 140: 127-144Crossref PubMed Google Scholar). In frontal cortex, several studies have indicated a crude topographic organization in the anterior bank of the arcuate sulcus (Bruce and Goldberg, 1985Bruce C.J. Goldberg M.E. Primate frontal eye fields. I. Single neurons discharging before saccades.J. Neurophysiol. 1985; 53: 603-635PubMed Google Scholar). The small and large saccade zones of the frontal eye field (FEF), located caudolaterally and rostromedially, respectively, receive visual afferents from foveal versus more peripheral visual field representations in extrastriate cortex, respectively (Schall et al., 1995Schall J.D. Morel A. King D.J. Bullier J. Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams.J. Neurosci. 1995; 15: 4464-4487PubMed Google Scholar). The receptive fields of the visual neurons are in register with the movement fields of the (visuo)motor neurons in the FEF. Consistent with these neuronal properties, Wardak et al., 2010Wardak C. Vanduffel W. Orban G.A. Searching for a salient target involves frontal regions.Cereb. Cortex. 2010; 20: 2464-2477Crossref PubMed Scopus (18) Google Scholar observed eccentricity biases in FEF, with larger eccentricities represented most medially. Higher-resolution imaging (Janssens et al., 2014Janssens T. Zhu Q. Popivanov I.D. Vanduffel W. Probalistic and single-subject retinotopic maps reveal the topographic organization of face patches in the macaque cortex.J. Neurosci. 2014; (Published online July 30, 2014)https://doi.org/10.1523/JNEUROSCI.2914-13.2013Crossref Google Scholar) confirmed this finding: a foveal visual field in FEF is surrounded by more peripheral visual field representations stretching anteromedially, as expected, but also ventrolaterally. In conclusion, a clear-cut retinotopic organization as found in occipitotemporal cortex is largely lacking within major parts of parietal and frontal cortex. While smoothly progressing eccentricity representations along the cortex are preserved to some extent, polar angle representations are much more variable. This overview demonstrates that retinotopy has proven useful to parcel visual cortex and to define visual areas. Initially, it was proposed that functional properties could also be used to define cortical areas, with V4 and MT being labeled the color- and motion-specific areas (Zeki et al., 1991Zeki S. Watson J.D. Lueck C.J. Friston K.J. Kennard C. Frackowiak R.S. A direct demonstration of functional specialization in human visual cortex.J. Neurosci. 1991; 11: 641-649PubMed Google Scholar). The latter strategy has received little support as many cortical areas forming functional networks proved to be motion or color selective as discussed below. Over a decade ago, monkey fMRI confirmed and extended earlier electrophysiological studies demonstrating visual motion sensitivity for translating dot fields in areas V2, V3, MT, MSTv, FST, regions within the IPS (then labeled VIP), and the arcuate sulcus (FEF). When moving lines were presented, motion sensitivity was also found in V4, TE, LIP, and CIP (Vanduffel et al., 2001Vanduffel W. Fize D. Mandeville J.B. Nelissen K. Van Hecke P. Rosen B.R. Tootell R.B. Orban G.A. Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys.Neuron. 2001; 32: 565-577Abstract Full Text Full Text PDF PubMed Scopus (214) Google Scholar). The somewhat surprising motion sensitivity in area V4 was also confirmed by Tolias et al., 2001Tolias A.S. Smirnakis S.M. Augath M.A. Trinath T. Logothetis N.K. Motion processing in the macaque: revisited with functional magnetic resonance imaging.J. Neurosci. 2001; 21: 8594-8601PubMed Google Scholar. In contrast to human V3A (Tootell et al., 1997Tootell R.B. Mendola J.D. Hadjikhani N.K. Ledden P.J. Liu A.K. Reppas J.B. Sereno M.I. Dale A.M. Functional analysis of V3A and related areas in human visual cortex.J. Neurosci. 1997; 17: 7060-7078PubMed Google Scholar), but again consistent with monkey electrophysiology, Vanduffel et al., 2001Vanduffel W. Fize D. Mandeville J.B. Nelissen K. Van Hecke P. Rosen B.R. Tootell R.B. Orban G.A. Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys.Neuron. 2001; 32: 565-577Abstract Full Text Full Text PDF PubMed Scopus (214) Google Scholar showed a lack of motion sensitivity in monkey V3A. A year later, the same group showed sensitivity for three-dimensional-structure-from-motion using paperclip stimuli in areas V2, V3, V4, and area MT along with its neighbors. Unlike observations in humans, very little three-dimensional-structure-from-motion sensitivity was observed in parietal cortex (see below) (Vanduffel et al., 2002Vanduffel W. Fize D. Peuskens H. Denys K. Sunaert S. Todd J.T. Orban G.A. Extracting 3D from motion: differences in human and monkey intraparietal cortex.Science. 2002; 298: 413-415Crossref PubMed Scopus (170) Google Scholar). A more exhaustive mapping of motion sensitivity within the STS using a wide variety of motion stimuli was performed by Nelissen et al., 2006Nelissen K. Vanduffel W. Orban G.A. Charting the lower superior temporal region, a new motion-sensitive region in monkey superior temporal sulcus.J. Neurosci. 2006; 26: 5929-5947Crossref PubMed Scopus (81) Google Scholar. This study confirmed fMRI-defined motion sensitivity in MT, MSTv, MSTd, FST, and STPm (middle STP) (Figure 1C). However, profound motion sensitivity was also observed in an area immediately rostroventral to FST deemed lower super temporal area (LST). This region responded to a broad range of speeds, moving images of objects, patterns defined by opponent motion, and actions. The recently described field maps anterior to V4 and caudoventral to the MT cluster (i.e., V4A, PITd, PITv, and OTd) displayed little motion sensitivity unlike components of the MT cluster itself (Kolster et al., 2014Kolster H. Janssens T. Orban G.A. Vanduffel W. The retinotopic organization of macaque occipitotemporal cortex anterior to V4 and caudo-ventral to the MT cluster.J. Neurosci. 2014; (Published online July 30, 2014)https://doi.org/10.1523/JNEUROSCI.3288-13.2014Crossref PubMed Scopus (2) Google Scholar), supporting the notion that field map clusters comprise functionally similar areas. Color processing is another instance where fMRI revised the original view of "centers," such as V4, once considered the "color area" (Zeki, 1973Zeki S.M. Colour coding in rhesus monkey prestriate cortex.Brain Res. 1973; 53: 422-427Crossref PubMed Google Scholar). Confirming earlier maps obtained with 2-deoxyglucose (Tootell et al., 2004Tootell R.B. Nelissen K. Vanduffel W. Orban G.A. Search for color 'center(s)' in macaque visual cortex.Cereb. Cortex. 2004; 14: 353-363Crossref PubMed Scopus (56) Google Scholar) and PET (Takechi et al., 1997Takechi H. Onoe H. Shizuno H. Yoshikawa E. Sadato N. Tsukada H. Watanabe Y. Mapping of cortical areas involved in color vision in non-human primates.Neurosci. Lett. 1997; 230: 17-20Crossref PubMed Scopus (29) Google Scholar), several color-selective fMRI-defined patches have been discovered in monkey ventral stream beyond V4 (Conway et al., 2007Conway B.R. Moeller S. Tsao D.Y. Specialized color modules in macaque extrastriate cortex.Neuron. 2007; 56: 560-573Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, Harada et al., 2009Harada T. Goda N. Ogawa T. Ito M. Toyoda H. Sadato N. Komatsu H. Distribution of colour-selective activity in the monkey inferior temporal cortex revealed by functional magnetic resonance imaging.Eur. J. Neurosci. 2009; 30: 1960-1970Crossref PubMed Scopus (18) Google Scholar). More recently, Lafer-Sousa and Conway, 2013Lafer-Sousa R. Conway B.R. Parallel, multi-stage p
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