Mapping the parietal cortex of human and non-human primates
Introduction
The parietal cortex is a typical higher order multimodal cortex, receiving visual, somatosensory and auditory signals. It is generally believed that its main function is the transformation of sensory signals into motor signals. Parietal cortex is much expanded in humans compared to macaques: while the overall cerebral cortex surface of humans amounts to 10 times that of the macaque, this ratio is at least twice as large for the lower part of the parietal cortex, the inferior parietal lobule (IPL) (Orban, Van Essen, & Vanduffel, 2004; Van Essen, 2004). The present review is restricted to the part of parietal cortex devoted to vision, which is generally referred to as posterior parietal cortex (PPC). With the advent of functional imaging the human parietal cortex has received considerable attention. Motor tasks have been tested, in the earlier PET studies (Faillenot, Toni, Decety, Gregoire, & Jeannerod, 1997; Grafton, Fagg, Woods, & Arbib, 1996; Lacquaniti et al., 1997, Petit et al., 1993; Pierrot-Deseilligny, Rivaud, Gaymard, & Agid, 1991; Rizzolatti et al., 1996) but also in the more recent fMRI studies (e.g. Astafiev et al., 2003, Binkofski et al., 1999; Connolly, Andersen, & Goodale, 2003; Muri, Iba-Zizen, Derosier, Cabanis, & Pierrot-Deseilligny, 1996; Petit & Haxby, 1999). Most fMRI studies of PPC, however, have focused on cognitive tasks, or on passive sensory stimulation and simple discriminations (Claeys et al., 2004, Shikata et al., 2001, Shulman et al., 1999). This profusion of studies has revealed that parietal cortex is involved in a surprisingly large series of cognitive functions including motor planning, spatial and other types of attention, visual and non-visual working memory, spatial representation and coordinate transformation, mental rotation, task relevant processing, calculation and even aspects of long term memory and language (Shannon & Buckner, 2004; Simon, Mangin, Cohen, Le Bihan, & Dehaene, 2002; for review Behrmann, Geng, & Shomstein, 2004; Culham & Kanwisher, 2001).
Even if one considers the function that has been most explored in the IPS, attention, progress has nonetheless been rather slow. Moreover, most results are simply reported in extremely coarse anatomical terms, e.g. anterior versus posterior intraparietal sulcus (IPS), SPL versus IPL. Recently, it has become clear that different parietal regions may be involved in the automatic attraction of attention and its voluntary control (Behrmann et al., 2004; Corbetta et al., 2000, Corbetta et al., 2002), or in shifting and maintaining spatial attention (Vandenberghe, Gitelman, Parrish, & Mesulam, 2001; Yantis et al., 2002). Finally a series of studies (Corbetta et al., 1998; Beauchamp, Petit, Ellmore, Ingeholm, & Haxby, 2001; Corbetta et al., 1998, Perry and Zeki, 2000; Vandenberghe et al., 2001) have underscored the similarity of the regions involved in covert and overt shift in attention, in agreement with the influential premotor theory of attention (Rizzolatti, Riggio, Dascola, & Umilta, 1987).
In contrast to human parietal cortex, which is still poorly understood, that of the macaque is known to contain a restricted number of cortical areas. In particular, the lateral intraparietal (LIP) region (Andersen, Bracewell, Barash, Gnadt, & Fogassi, 1990) and the posterior reach region (PRR), including V6A and the medial intraparietal (MIP) region, have been a focus of single cell investigations (Andersen & Buneo, 2002; Batista & Andersen, 2001; Fattori, Gamberini, Kutz, & Galletti, 2001; Ferraina, Pare, & Wurtz, 2002). Although the exact parcellation of monkey PPC and the precise limits of most areas are still in debate (Van Essen, 2004), a coherent picture of the sensori-motor and related cognitive functions implemented by the PPC, is beginning to emerge (for reviews Andersen & Buneo, 2002; Glimcher, 2003, Gold and Shadlen, 2003; Gottlieb, 2002, Rizzolatti and Luppino, 2001). A brief, speculative, but thought-provoking description goes as follows. In general, the parietal cortex uses sensory inputs to plan one or a series of actions, when the goal and the task have already been decided (by other regions). To that end the PPC needs to deploy a series of capabilities. We speculate that during the course of evolution these capabilities have adapted to operate across a range of behavioral conditions other than strict sensory-motor control, thereby becoming more autonomous and giving rise to the many cognitive functions in which the human PPC appears to be involved.
First, neuronal populations within the PPC must receive the appropriate external signals to operate upon and keep track of the behavioral goal and task (decided by other regions), hence the PPC's role in the control of selection or attention and the task related processing (Assad, 2003, Gottlieb, 2002). Second, the PPC has to process the appropriate features of the sensory signals. For simple motor acts, like reaching or making saccades, position may be sufficient. However, it will be important to represent space in the appropriate coordinate system (eye-centered, head-centered, etc.), hence the functions of spatial representation and coordinate transformations (Andersen & Buneo, 2002). For other actions, e.g. pursuit and catching, the derivative of position over time, i.e. motion, will be critical (Churchland & Lisberger, 2005; Claeys, Lindsey, De Schutter, & Orban, 2003; Indovina et al., 2005). For still other actions, such as grasping, manipulation, tool use, more complex sensory features such as orientation in space, size, 2D and 3D shape will be important (Goodale & Milner, 1992; Iriki, Tanaka, & Iwamura, 1996; Murata, Gallese, Luppino, Kaseda, & Sakata, 2000; Sakata, Taira, Murata, & Mine, 1995; Sereno & Maunsell, 1998; Vanduffel et al., 2002). Third, to decide among choices, prior probabilities and their value or utility will have to be integrated (Platt & Glimcher, 1999; Shadlen & Newsome, 2001; Sugrue, Corrado, & Newsome, 2005), hence the decision processing in the PPC. This integration usually develops over time, hence the delay activity, that may underlie working memory and temporal processing in the PPC (Cornette, Dupont, Salmon, & Orban, 2001; Janssen & Shadlen, 2005; Smith & Jonides, 1999). Fourth, a number of actions will require coordinating the movements of different body parts, e.g. eyes and head, eyes and hand or both hands, hence the eye-hand and other coordination functions (Andersen & Buneo, 2002; Committeri et al., 2004; Puttemans, Wenderoth, & Swinnen, 2005; Vidal, Amorim, & Berthoz, 2004). Finally, in many instances a series of actions will be required, calling for integration of the successive actions (Fogassi et al., 2005) and the evaluation of the result from the previous action by integration of visual and haptic signals, hence the action planning and multimodal integration (Grefkes, Weiss, Zilles, & Fink, 2002; Johansson, Westling, Bäckström, & Flanagan, 2001). Thus the sensory control of action has required the development of a number of computational competences that may have been applied in other behavioral contexts, evolving to yield the complexity of cognitive functions in which the human PPC participates.
The success of single cell studies have prompted many researchers to call for integration of human functional imaging (Culham & Kanwisher, 2001; Glimcher, 2003, Treue, 2003) with the single cell studies in the monkey. This however requires that two issues be resolved: the relationship between fMRI and neuronal signals (Logothetis, Pauls, Augath, Trinath, & Oeltermann, 2001) and the homologies between cortical areas in the two species (Kaas, 2002; Krubitzer & Kahn, 2003; Orban et al., 2004, Sereno and Tootell, 2005) need to be established. Both problems can be significantly advanced (Orban, 2002) by the use of fMRI in the awake monkey (Vanduffel et al., 2001). To address neuronal operations in higher order cortex such as PPC, it is essential that the monkey subjects are awake. Indeed anesthesia severely depresses neuronal activity in higher order cortex. Therefore, one aim is to review a series of awake monkey fMRI studies which relate to parietal cortex (Denys et al., 2004a, Denys et al., 2004b, Koyama et al., 2004; Sawamura, Georgieva, Vogels, Vanduffel, & Orban, 2005; Tsao et al., 2003, Vanduffel et al., 2001, Vanduffel et al., 2002). It is, however, highly unlikely that all human areas will turn out to have a monkey counterpart. Indeed it would imply that individual cortical areas, like the overall cortical surface, are 10 times larger in humans than in monkeys. This is not an attractive proposal, given the limitations of connection lengths and hence optimal area size. One thus faces the limitations of the monkey model (Behrmann et al., 2004). But even within these restrictions, the parallel study of human and monkey cortex should be extremely beneficial. Charting the homologous areas will provide the beginnings of a map (a protomap) of human PPC allowing imaging results to be reported in a much more detailed and meaningful way. Furthermore, these homologous areas can act as seeds for understanding neighboring, newly emerged cortex in humans. Indeed for homologous areas, the knowledge derived from single cell studies provides a mechanistic description of the neuronal function localized with the fMRI. This knowledge of neuronal operations can then be extrapolated to evolutionary new cortex, which, presumably enhances and transforms the processing performed in the more basic, homologous regions, with the fMRI indicating the nature of this transformation. Thus a second aim of the review is to further investigate those human functional regions that appeared quite different from their monkey counterparts in our first direct inter-species comparisons in the realm of motion and 3D structure from motion processing (Orban et al., 2003, Vanduffel et al., 2002). In the discussion we will attempt a first outline of a human PPC map, distinguishing evolutionarily old from new areas.
Section snippets
Methods
The detailed description of the methods is given in the original papers (Denys et al., 2004a, Fize et al., 2003; Orban, Sunaert, Todd, Van Hecke, & Marchal, 1999; Peuskens et al., 2004, Sawamura et al., 2005; Sunaert, Van Hecke, Marchal, & Orban, 1999; Vanduffel et al., 2001, Vanduffel et al., 2002). Here we only provide a brief summary.
Four motion sensitive regions in human PPC: functional properties
We established that human IPS contains four motion sensitive regions (Orban et al., 2003, Sunaert et al., 1999). Their locations are shown on the flatmap of a single human subject in Fig. 1A. The most posterior of these, the ventral IPS (VIPS) region, is located in the occipital part of the intraparietal sulcus (IPS), just dorsal to hV3A. The second is located at the confluence of the occipital and parietal parts of the IPS with the parieto-occipital sulcus (POS) and hence is referred to as
Pittfalls of human–monkey fMRI comparisons
Studies in which BOLD and MION measurements are compared in the same subjects have shown that the use of the contrast agent improved the contrast-noise ratio (by approximately five-fold) compared to blood oxygenation level-dependent (BOLD) measurements (Leite et al., 2002, Vanduffel et al., 2001). Because the MR signals obtained with MION and BOLD show a different relationship with vessel diameter, MION MR signals, unlike BOLD are more confined to the parenchym than to the superficial draining
Conclusion
The PPC links vision to action and hence parietal areas may differ with regard to the visual features analyzed or the types of body movements controlled. An increased number of cortical parietal regions in humans may be devoted either to control a wider range of body movements or to provide a more detailed analysis of the visual input. The present results support at least the later interpretation and indicate the significance of moving images in the visual input to human PPC. This reflects the
Acknowledgements
The technical help of Y. Celis, A. Coeman, M. De Paep, W. Depuydt, C. Fransen, P. Kayenbergh, G. Meulemans, is kindly acknowledged. Supported by grants GOA 2005/18, IUAP P5/04, GSKE, FWO G 0151.04, EU project Neuro-IT-Net (IST-2001-35498). CW is supported by the Fyssen foundation. The authors are indebted to G. Rizzolatti, G. Luppino and S. Raiguel for helpful comments on an earlier version of the manuscript. The Laboratoire Guerbet (Roissy, France) provided the contrast agent (Sinerem®).
References (129)
Neural coding of behavioral relevance in parietal cortex
Current Opinion in Neurobiology
(2003)- et al.
A parametric fMRI study of overt and covert shifts of visuospatial attention
NeuroImage
(2001) - et al.
Parietal cortex and attention
Current Opinion in Neurobiology
(2004) - et al.
Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain
Current Biology
(2000) - et al.
Polymodal motion processing in posterior parietal and premotor cortex: A human fMRI study strongly implies equivalencies between humans and monkeys
Neuron
(2001) - et al.
A higher order motion region in human inferior parietal lobule: Evidence from fMRI
Neuron
(2003) - et al.
A common network of functional areas for attention and eye movements
Neuron
(1998) - et al.
Attention response functions: Characterizing brain areas using fMRI activation during parametric variations of attentional load
Neuron
(2001) - et al.
Neuroimaging of cognitive functions in human parietal cortex
Current Opinion in Neurobiology
(2001) - et al.
Cortical topography of human anterior intraparietal cortex active during visually guided grasping
Cognitive Brain Research
(2005)
Separate visual pathways for perception and action
Trends in Neuroscience
Parietal mechanisms of target representation
Current Opinion in Neurobiology
Crossmodal processing of object features in human anterior intraparietal cortex: An fMRI study implies equivalencies between humans and monkeys
Neuron
Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: Comparison of cortical eye fields with humans
Neuron
Nature versus nurture revisited: An old idea with a new twist
Progress in Neurobiology
Visuomotor transformations for reaching to memorized targets: A PET study
NeuroImage
Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla
Neuroimage
Similarities and differences in motion processing between the human and macaque brain: Evidence from fMRI
Neuropsychologia
Human cortical regions involved in extracting depth from motion
Neuron
Comparative mapping of higher visual areas in monkeys and humans
Trends in Cognitive Science
The cortical motor system
Neuron
Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention
Neuropsychologia
From monkeys to humans: What do we now know about brain homologies?
Current Opinion in Neurobiology
Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque
Journal of Neuroscience
Intentional maps in posterior parietal cortex
Annual Review of Neuroscience
Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing
Journal of Neuroscience
The parietal reach region codes the next planned movement in a sequential reach task
Journal of Neurophysiology
Representation of the visual field in the lateral intraparietal area of macaque monkeys: A quantitative receptive field analysis
Experimental Brain Research
A fronto-parietal circuit for object manipulation in man: Evidence from an fMRI study
European Journal of Neuroscience
Neuronal activity in the lateral intraparietal area and spatial attention
Science
Encoding of three-dimensional structure-from-motion by primate area MT neurons
Nature
Heading encoding in the macaque ventral intraparietal area (VIP)
European Journal of Neuroscience
Visual-vestibular interactive responses in the macaque ventral intraparietal area (VIP)
European Journal of Neuroscience
Flows of diffeomorphism for multimodal image registration
Proceedings of the IEEE International Symposium on Biomedical Imaging
Discharge properties of MST neurons that project to the frontal pursuit area in macaque monkeys
Journal of Neurophysiology
Color discrimination involves ventral and dorsal stream visual areas
Cerebral Cortex
Reference frames for spatial cognition: Different brain areas are involved in viewer-, object-, and landmark-centered judgments about object location
Journal of Cognitive Neuroscience
fMRI evidence for a “parietal reach region” in the human brain
Experimental Brain Research
Neuronal responses in area 7a to multiple stimulus displays. II. Responses are suppressed at the cued location
Cerebral Cortex
Voluntary orienting is dissociated from target detection in human posterior parietal cortex
Nature Neuroscience
Neural systems for visual orienting and their relationships to spatial working memory
Journal of Cognitive Neuroscience
The neural substrate of orientation working memory
Journal of Cognitive Neuroscience
Human brain imaging reveals a parietal area specialized for grasping
Cortical fMRI activation produced by attentive tracking of moving targets
Journal of Neurophysiology
Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas
Experimental Brain Research
Characterization of the human visual V6 complex by functional magnetic resonance imaging
European Journal of Neuroscience
The processing of visual shape in the cerebral cortex of human and nonhuman primates: A functional magnetic resonance imaging study
Journal of Neuroscience
Visual activation in prefrontal cortex is stronger in monkeys than in humans
Journal of Cognitive Neuroscience
Cited by (230)
Parieto-premotor functional connectivity changes during parietal lobe seizures are associated with motor semiology
2021, Clinical NeurophysiologyCitation Excerpt :Furthermore the incidence of PLE is probably underestimated due to misleading clinical and electrical features that can make differential diagnosis difficult from epileptic seizures arising from other lobes or even psychogenic nonepileptic seizures (Francione et al., 2015; Pilipović-Dragović et al., 2018; Salanova et al., 1995a; Sveinbjornsdottir and Duncan, 1993). Functionally, the parietal lobe is a multimodal cortex that receives and integrates somato-sensory, visual and auditory inputs and that participates in motor planning, attention, spatial representation, working and long-term memory, calculation and language processes (Orban et al., 2006). Posterior parietal cortex is strongly interconnected with sub-cortical and others cortical areas (Caspers and Zilles, 2018).
The role of transcranial magnetic stimulation in understanding attention-related networks in single subjects
2021, Current Research in NeurobiologyThe Fossil Evidence of Human Brain Evolution
2020, Evolutionary Neuroscience