Real and Imagined Grasping Movements Differently Activate the Human Dorsomedial Parietal Cortex

Highlights

• The human dorsomedial parietal cortex responds to pantomimed grasping movements.

• Areas hV6A and hPEc are differently activated by real and imagined grasping movements.

• Areas hV6Ad and hPEc are respectively involved in cognitive and pragmatic aspects of the control of grasping.

Abstract

Object prehension typically includes a transport phase (reaching) and a grip phase (grasping). Within the posterior parietal cortex (PPC), grasping movements have been traditionally associated to a lateral activation, although recent monkey evidence suggests also a medial involvement. Here, we wanted to determine whether grasping-related activities are present in the human dorsomedial parietal cortex, by focusing on two cortical regions specialized in the monkey in controlling limb movements, i.e., V6A (composed by its ventral and dorsal sectors, V6Av and V6Ad, respectively) and PEc, both recently defined also in humans. We acquired functional magnetic resonance images while participants performed both real (pantomimed) and imagined grasping of visually-presented objects. We found that the human areas V6Ad (hV6Ad) and PEc (hPEc) were both activated by real grasping, whereas hV6Ad only was activated by the imagery of grasping movements. hV6Av was not involved in either types of grasping. These results speak against the traditional notion of a medial-to-lateral segregation of reaching versus grasping information within the PPC and strengthen the idea that the human dorsomedial parietal cortex implements the whole complex pattern of visuomotor transformations required for object-oriented actions. Our findings suggest that hV6Ad is particularly involved in implementing all the visuomotor transformations needed to create an abstract representation of the object-directed action, while hPEc is involved in implementing the sensorimotor transformations needed to actually perform that action.

Introduction

Prehension of an object requires both transporting the hand toward the object (reaching component) and shaping the hand according to it (grip component). The classic dominant view, derived from monkey studies (Jeannerod et al., 1995) and that remains deeply influential even to date (Rizzolatti and Kalaska, 2013), posits that these components are largely anatomically segregated within the posterior parietal cortex (PPC): the dorsomedial PPC, which primarily includes area V6A, PEc and the medial intraparietal area (MIP), would be involved in reaching movements (Colby and Duhamel, 1991, Ferraina et al., 2001, Battaglia-Mayer et al., 2000, Fattori et al., 2001, Fattori et al., 2005), while the dorsolateral PPC, especially the anterior intraparietal area (AIP), would be involved in grasping movements (Sakata et al., 1995, Murata et al., 2000, Baumann et al., 2009). However, several lines of evidence are not entirely consistent with the notion of independent neural coding for grasp and reach movements, particularly with respect to the macaque area V6A (Galletti et al., 2003, Fattori et al., 2004, Fattori et al., 2017, Galletti and Fattori, 2018 for recent review). Monkey area V6A shows grasping-related responses, besides reaching-related ones, reflecting sensitivity to wrist orientation and grip formation (Fattori et al., 2009, Fattori et al., 2010, Gamberini et al., 2011, Breveglieri et al., 2016, Breveglieri et al., 2018). In addition, it has been demonstrated that different grasping-relevant information, such as grip types and hand configurations, can be decoded from V6A activity pattern (Filippini et al., 2017, Nelissen et al., 2018). Mainly based on this evidence, it has been recently proposed that V6A is involved in the fast control of visually-guided prehension, including object grasping (Fattori et al., 2017, Galletti and Fattori, 2018).

As shown in Fig. 1, macaque area V6A is located in the anterior bank of the parieto-occipital sulcus (POs). The area has been divided in a ventral (V6Av) and a dorsal (V6Ad) sector based on cytoarchitectonic criteria (Luppino et al., 2005). Both sectors host visual and somatosensory cells, with area V6Av showing a majority of visual cells and area V6Ad a majority of cells sensitive to somatic stimulation (Gamberini et al., 2011). Both subdivisions of area V6A respond to reach-to-grasp actions (Gamberini et al., 2011, Breveglieri et al., 2016, Breveglieri et al., 2018), and V6Ad is particularly involved in controlling the hand-to-object interaction, with cells selectively modulated by the type of grip used (Fattori et al., 2010). Moving anteriorly from V6Ad, the dorsomedial PPC hosts a distinct cytoarchitectonic area, called PEc (Pandya and Seltzer, 1982). Area PEc is specialized in the integration of hand- and eye-related information (Ferraina et al., 2001), is well equipped to control arm-reaching actions (Hadjidimitrakis et al., 2015, Piserchia et al., 2017), and shares many somatosensory and visual properties with V6A (Gamberini et al., 2018). At present, however, PEc cells have not yet been specifically tested for grasping. Overall, macaque evidence supports the notion that at least one area (V6A) of the dorsomedial circuit is recruited by grasping movements (Fattori et al., 2017).

In humans, grasping-related activity has been mainly associated to the dorsolateral PPC, with many studies reporting activations in a region in the anterior IPS sulcus (aIPs), a likely human homologue of monkey AIP, during reaching-to-grasp (Culham et al., 2003, Hinkley et al., 2009, Frey et al., 2005, Grafton et al., 1996), haptic object manipulation (Hinkley et al., 2009, Binkofski et al., 1999), arm transport and grip formation (Cavina-Pratesi et al., 2010), and pantomimed grasping (Shikata et al., 2003, Simon et al., 2002, Johnson-Frey et al., 2005, Króliczak et al., 2007, Bozzacchi et al., 2012, Makuuchi et al., 2012). Recently, a growing number of studies have started to report grasping-related activity also on the most medial part of human PPC, as in macaque. These studies reported grasping-related foci of activation in the cortical territory extending from the dorsalmost part of the POs to the cingulate sulcus (Monaco et al., 2011, Gallivan et al., 2011, Gutteling et al., 2015, Vesia et al., 2017, Styrkowiec et al., 2019; see also Fattori et al., 2017 for a recent review). In particular, by using decoding techniques from activation patterns and adaptation, it has been observed that the cortical region likely corresponding to the human homolog of macaque area V6A (hV6A; Pitzalis et al., 2013, Tosoni et al., 2015) plays a role in processing wrist orientation and grip formation (Gallivan et al., 2011, Monaco et al., 2011), well in line with clinical observations that lesions to the same cortical region do not only lead to reaching errors, but also to difficulties in achieving an appropriate wrist posture (Jeannerod, 1986, Perenin and Vighetto, 1988, Jakobson et al., 1991). Although macaque area PEc has never been explicitly tested with grasping tasks, recent fMRI data on humans reveal the recruitment of the anterior precuneus, where PEc is located in the macaque (see Fig. 1), during action tasks like reaching and grasping (Monaco et al., 2011), in haptically guided grasping of tools (Styrkowiec et al., 2019), and when a multivoxel pattern classifier was applied to discriminate between grasping and pointing movements (Gutteling et al., 2015). Notably, however, all these studies, described such dorsomedial activations in terms of whole-brain neural circuits, not ascribed to specific dorsomedial parietal areas.

The cortical territory extending in humans from the POs to the cingulate sulcus has been recently described by our group as hosting the human homologues of monkey V6 (Pitzalis et al., 2006, Pitzalis et al., 2015), V6Av (Pitzalis et al., 2013, Pitzalis et al., 2015), V6Ad (Tosoni et al., 2015, Pitzalis et al., 2019), and PEc (Pitzalis et al., 2019). These regions show a trend in the functional specialization following a posterior-to-anterior axis, with the most posterior hV6 and hV6Av involved in the visual analysis of motion (Pitzalis et al., 2010) and the anterior hV6Ad and hPEc specialized in the visuomotor control of arm (Tosoni et al., 2015) and arm/leg (Pitzalis et al., 2019) movements, respectively. However, the role of these regions during grasping is still largely unexplored.

Here, we wanted to determine whether grasping-related activity is present in the dorsomedial PPC areas hV6A, as it is the case in monkey (Fattori et al., 2017), and hPEc, as suggested by the above recalled recent reports in humans (Monaco et al., 2011, Styrkowiec et al., 2019, Gutteling et al., 2015). To this aim, we acquired functional magnetic resonance images while participants performed: (1) a pantomimed grasping action requiring to execute the complex pattern of hand movements (extension/flexion of fingers and wrist rotation) necessary to grasp a visually-presented object (real grasping), and (2) an imagined grasping action requiring to mental simulate the grasping of that particular object, and thus in the absence of real hand/fingers movements (imagined grasping). Since we were interested in grasping only (i.e., the shaping of the hand in relation to the shape and size of the object), without reaching, we explicitly asked participants to imagine the object very close to their hand so as to abolish the transport phase of the hand toward the object.

Following the above recalled fMRI evidence suggesting the involvement of dorsomedial regions (including areas hV6A and hPEc) in coding aspects of executed grasping movements (Monaco et al., 2011, Gallivan et al., 2011, Gutteling et al., 2015, Vesia et al., 2017, Styrkowiec et al., 2019), we hypothesized that both of these areas should respond to real grasping. Additionally, based on previous reports showing the anterior precuneus (including area hPEc) as predominantly proprioceptive-motor and the anterior POs (including area hV6Ad) as predominantly visuomotor (Filimon et al., 2009, Pitzalis et al., 2019), we expected to find a different sensitivity with respect to the ‘pure visual’ condition (imagined grasping). Finally, based on previous macaque reports demonstrating a higher visual sensitivity of V6Av and somatic sensitivity of V6Ad (Gamberini et al., 2011), we hypothesized a different functional profile between the ventral and dorsal partitions of human area V6A. All these hypotheses have been verified in the present work, strongly supporting the view that, besides reaching, the dorsomedial parietal cortex is involved in selecting appropriate hand motor programs for grasping.

Overall, our results suggest a functional specialization within the dorsomedial PPC, with the dorsal (but not the ventral) sector of hV6A involved in creating a more abstract representation of the grasping action, being activated by both real and imagined grasping, and hPEc involved in more pragmatic aspects of that action, being activated by the real grasping only. The specific involvement of hV6Ad and hPEc in the control of hand action remains however largely unexplored being investigated here for the first time.