Mapping the parietal cortex of human and non-human primates

https://doi.org/10.1016/j.neuropsychologia.2005.11.001Get rights and content

Abstract

The present essay reviews a series of functional magnetic resonance imaging (fMRI) studies conducted in parallel in humans and awake monkeys, concentrating on the intraparietal sulcus (IPS). MR responses to a range of visual stimuli indicate that the human IPS contains more functional regions along its anterior–posterior extent than are known in the monkey. Human IPS includes four motion sensitive regions, ventral IPS (VIPS), parieto-occipital IPS (POIPS), dorsal IPS medial (DIPSM) and dorsal IPS anterior (DIPSA), which are also sensitive to three-dimensional structure from motion (3D SFM). On the other hand, the monkey IPS contains only one motion sensitive area (VIP), which is not particularly sensitive to 3D SFM. The human IPS includes four regions sensitive to two-dimensional shape and three representations of central vision, while monkey IPS appears to contain only two shape sensitive regions and one central representation. These data support the hypothesis that monkey LIP corresponds to the region of human IPS between DIPSM and POIPS and that a portion of the anterior part of human IPS is evolutionarily new. This additional cortical tissue may provide the capacity for an enhanced visual analysis of moving images necessary for sophisticated control of manipulation and tool handling.

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)

  • M.A. Goodale et al.

    Separate visual pathways for perception and action

    Trends in Neuroscience

    (1992)
  • J. Gottlieb

    Parietal mechanisms of target representation

    Current Opinion in Neurobiology

    (2002)
  • C. Grefkes et al.

    Crossmodal processing of object features in human anterior intraparietal cortex: An fMRI study implies equivalencies between humans and monkeys

    Neuron

    (2002)
  • M. Koyama et al.

    Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: Comparison of cortical eye fields with humans

    Neuron

    (2004)
  • L. Krubitzer et al.

    Nature versus nurture revisited: An old idea with a new twist

    Progress in Neurobiology

    (2003)
  • F. Lacquaniti et al.

    Visuomotor transformations for reaching to memorized targets: A PET study

    NeuroImage

    (1997)
  • F.P. Leite et al.

    Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla

    Neuroimage

    (2002)
  • G.A. Orban et al.

    Similarities and differences in motion processing between the human and macaque brain: Evidence from fMRI

    Neuropsychologia

    (2003)
  • G.A. Orban et al.

    Human cortical regions involved in extracting depth from motion

    Neuron

    (1999)
  • G.A. Orban et al.

    Comparative mapping of higher visual areas in monkeys and humans

    Trends in Cognitive Science

    (2004)
  • G. Rizzolatti et al.

    The cortical motor system

    Neuron

    (2001)
  • G. Rizzolatti et al.

    Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention

    Neuropsychologia

    (1987)
  • M.I. Sereno et al.

    From monkeys to humans: What do we now know about brain homologies?

    Current Opinion in Neurobiology

    (2005)
  • R.A. Andersen et al.

    Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque

    Journal of Neuroscience

    (1990)
  • R.A. Andersen et al.

    Intentional maps in posterior parietal cortex

    Annual Review of Neuroscience

    (2002)
  • S.V. Astafiev et al.

    Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing

    Journal of Neuroscience

    (2003)
  • Baker, J. T., Patel, G. H., Corbetta, M., & Snyder L. H. (2005). Distribution of activity across the monkey cerebral...
  • A.P. Batista et al.

    The parietal reach region codes the next planned movement in a sequential reach task

    Journal of Neurophysiology

    (2001)
  • S. Ben Hamed et al.

    Representation of the visual field in the lateral intraparietal area of macaque monkeys: A quantitative receptive field analysis

    Experimental Brain Research

    (2001)
  • F. Binkofski et al.

    A fronto-parietal circuit for object manipulation in man: Evidence from an fMRI study

    European Journal of Neuroscience

    (1999)
  • J.W. Bisley et al.

    Neuronal activity in the lateral intraparietal area and spatial attention

    Science

    (2003)
  • D.C. Bradley et al.

    Encoding of three-dimensional structure-from-motion by primate area MT neurons

    Nature

    (1998)
  • F. Bremmer et al.

    Heading encoding in the macaque ventral intraparietal area (VIP)

    European Journal of Neuroscience

    (2002)
  • F. Bremmer et al.

    Visual-vestibular interactive responses in the macaque ventral intraparietal area (VIP)

    European Journal of Neuroscience

    (2002)
  • C. Chef d’Hotel et al.

    Flows of diffeomorphism for multimodal image registration

    Proceedings of the IEEE International Symposium on Biomedical Imaging

    (2002)
  • Choi, H.-J., Zilles, K., Mohlberg, H., Schleicher, A., Fink, G.R., & Amunts, K., et al. (in press). Cytoarchitectonic...
  • A.K. Churchland et al.

    Discharge properties of MST neurons that project to the frontal pursuit area in macaque monkeys

    Journal of Neurophysiology

    (2005)
  • K.G. Claeys et al.

    Color discrimination involves ventral and dorsal stream visual areas

    Cerebral Cortex

    (2004)
  • G. Committeri et al.

    Reference frames for spatial cognition: Different brain areas are involved in viewer-, object-, and landmark-centered judgments about object location

    Journal of Cognitive Neuroscience

    (2004)
  • J.D. Connolly et al.

    fMRI evidence for a “parietal reach region” in the human brain

    Experimental Brain Research

    (2003)
  • C. Constantinidis et al.

    Neuronal responses in area 7a to multiple stimulus displays. II. Responses are suppressed at the cued location

    Cerebral Cortex

    (2001)
  • M. Corbetta et al.

    Voluntary orienting is dissociated from target detection in human posterior parietal cortex

    Nature Neuroscience

    (2000)
  • M. Corbetta et al.

    Neural systems for visual orienting and their relationships to spatial working memory

    Journal of Cognitive Neuroscience

    (2002)
  • L. Cornette et al.

    The neural substrate of orientation working memory

    Journal of Cognitive Neuroscience

    (2001)
  • J. Culham

    Human brain imaging reveals a parietal area specialized for grasping

  • J.C. Culham et al.

    Cortical fMRI activation produced by attentive tracking of moving targets

    Journal of Neurophysiology

    (1998)
  • J.C. Culham et al.

    Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas

    Experimental Brain Research

    (2003)
  • P. Dechent et al.

    Characterization of the human visual V6 complex by functional magnetic resonance imaging

    European Journal of Neuroscience

    (2003)
  • K. Denys et al.

    The processing of visual shape in the cerebral cortex of human and nonhuman primates: A functional magnetic resonance imaging study

    Journal of Neuroscience

    (2004)
  • K. Denys et al.

    Visual activation in prefrontal cortex is stronger in monkeys than in humans

    Journal of Cognitive Neuroscience

    (2004)
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