Elsevier

NeuroImage

Volume 37, Issue 4, 1 October 2007, Pages 1315-1328
NeuroImage

Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery

https://doi.org/10.1016/j.neuroimage.2007.06.008Get rights and content

Abstract

We used functional magnetic resonance imaging (fMRI) to map the cortical representations of executed reaching, observed reaching, and imagined reaching in humans. Whereas previous studies have mostly examined hand actions related to grasping, hand–object interactions, or local finger movements, here we were interested in reaching only (i.e. the transport phase of the hand to a particular location in space), without grasping. We hypothesized that mirror neuron areas specific to reaching-related representations would be active in all three conditions. An overlap between executed, observed, and imagined reaching activations was found in dorsal premotor cortex as well as in the superior parietal lobe and the intraparietal sulcus, in accord with our hypothesis. Activations for observed reaching were more dorsal than activations typically reported in the literature for observation of hand–object interactions (grasping). Our results suggest that the mirror neuron system is specific to the type of hand action performed, and that these fronto-parietal activations are a putative human homologue of the neural circuits underlying reaching in macaques. The parietal activations reported here for executed, imagined, and observed reaching are also consistent with previous functional imaging studies on planned reaching and delayed pointing movements, and extend the proposed localization of human reach-related brain areas to observation as well as imagery of reaching.

Introduction

Despite the long tradition of studying space perception from a purely visual perspective, recent research has revealed that motor actions are a key part of space perception. Interactions with the world, such as through eye and hand movements, contribute to a representation of space that is not just visual, but also motor. Mirror neurons for hand actions are one example of such visuomotor representations.

Electrophysiological studies in macaques have identified several frontal areas involved in hand action representations (Preuss et al., 1996, Muakkassa and Strick, 1979, Matelli and Luppino, 2001, Rizzolatti et al., 1988). For instance, both dorsal premotor cortex (PMd, or F2 and F7) and ventral premotor cortex (PMv, or F4 and F5) contain arm/hand representations that are specific to certain motor actions, such as grasping or reaching (Matelli and Luppino, 2001). More specifically, neurons that respond to both hand action execution (e.g. grasping) and hand action observation (e.g. observed grasping) have been found in macaque ventral premotor area F5 (for a review, see Rizzolatti and Craighero, 2004, Rizzolatti et al., 1996a, Buccino et al., 2004a). These “mirror neurons” suggest an observation–execution matching system that allows monkeys to recognize actions performed by other individuals by mapping them onto their own motor representations.

Mirror neurons have also been studied in macaque parietal cortex, in particular in the inferior parietal lobule (Fogassi et al., 1998). Their presence in the parietal lobe is in accord with the many hand/arm motor representations found in monkey parietal cortex, such as the anterior intraparietal area (AIP), which deals with grasping and object manipulation, the medial intraparietal area (MIP), which controls arm movements during reaching, and other arm-related parietal areas, such as areas V6A, 5, and 7 (Johnson et al., 1996, Stepniewska et al., 2005, Fattori et al., 2001, Galletti et al., 1997, Andersen and Buneo, 2002, Buneo et al., 2002, Ferraina et al., 2001, Kalaska, 1996, Battaglia-Mayer et al., 2000, Culham and Kanwisher, 2001). These parietal areas have specific premotor targets: distinct parieto-frontal neural circuits have been found in the macaque brain for grasping (AIP–F5), and reaching (MIP/V6A–F2vr), for instance (Matelli and Luppino, 2001).

Over the last few years, functional imaging studies in humans have begun to explore mirror neuron activations for hand actions in humans (for a review, see Grèzes and Decety, 2001, Decety and Grèzes, 1999, Buccino et al., 2004a). Investigation of the mirror-neuron system in humans has mainly focused on the involvement of ventral premotor cortex and the inferior frontal gyrus (Broca's area), an area thought to be the human homologue of macaque F5 (Rizzolatti et al., 1996a).

Several human neuroimaging studies have investigated observation of grasping or of object manipulation (Grafton et al., 1996a, Binkofski et al., 1999, Buccino et al., 2001, Johnson-Frey et al., 2003, Molnar-Szakacs et al., 2006, Tai et al., 2004, Grèzes et al., 2003). Other studies have compared grasping observation with grasping execution or imitation (Rizzolatti et al., 1996b, Grèzes et al., 2003, Hamzei et al., 2003; see also a neuromagnetic study by Nishitani and Hari, 2000), observation versus imitation of simple finger movements (Iacoboni et al., 1999), or observation versus execution of more complex finger movements, such as playing guitar strings (Buccino et al., 2004b). In addition to execution and observation of hand actions, mental simulation (imagery) of hand actions, such as imagined grasping, has also been investigated (Grafton et al., 1996a, Grèzes and Decety, 2001). Finally, there is also a literature on observation of pantomimes and planning of tool use (Decety et al., 1997, Johnson-Frey et al., 2005) as well as execution of pantomimes (e.g. pantomimed grasping compared to actual grasping, and pantomimed reaching to touch an object compared to actual reaching to touch an object; Króliczak et al., 2007).

The majority of these studies involve hand–object interactions, whether through prehension, touching of an object, or preshaping of the hand during a pantomimed interaction with a missing object. In other cases precise, local, finger movement that is limited to the hand was studied, such as finger lifting (Iacoboni et al., 1999). A majority of these studies have found activations in ventral premotor/inferior frontal cortex as well as in the inferior parietal lobe. The frontal activations included Broca's area, the putative human homologue of macaque F5, in most cases. In some cases, the superior parietal lobe, precuneus, and the intraparietal sulcus were also involved, with greater activations in the hemisphere contralateral to the moving hand. Typically studies that involve less of a transport phase in both observation and execution conditions (e.g. Rizzolatti et al., 1996b, where only the final phase of the hand grasping an object was viewed) find activations in the inferior frontal gyrus and the inferior parietal lobule, but not the superior parietal lobule. Tasks that involve a greater transport phase (e.g. Hamzei et al., 2003, where a cup was grasped and moved from the lap to the mouth; Grafton et al., 1996b, Culham et al., 2003) do activate the superior parietal lobule. It is unclear, however, why some studies report superior parietal activations and others do not.

Whereas a number of these studies have focused on hand actions that involve hand preshaping (e.g. during grasping or pantomimed grasping) or precise local hand movements (whether an object is present or not), less is known about which brain areas are involved in the execution, observation, and imagery of hand actions that do not involve object-directed movement, local finger configurations, or touching of an object. For instance, it is unknown if just the transport phase of the hand through space, such as during reaching, activates its own set of mirror neurons during execution, observation, and imagery of reaching. In other words, few studies have investigated whether mirror neuron activations change with hand actions in accordance to the fronto-parietal neural circuits identified in macaques, with AIP–F5 representing grasping-related actions, and MIP–F2vr representing reaching-related actions. Are there mirror neuron activations for reaching (without grasping or touching) in humans, and how do they compare to mirror neuron activations for grasping, hand–object interactions, or smaller finger movements such as finger lifting? Reaching movements are different from the aforementioned hand actions in that only a transport phase of the hand is required, where preshaping of the hand for appropriate hand–object interactions or even touching is not necessary. For reaching, extraction of the visual properties of the object is not necessary; instead, the hand and arm need guided toward the appropriate point in space, regardless of what is located at that point in space. Buccino et al. (2001) found a somatotopic organization for observation of movements performed with different effectors (hand, mouth, or foot) in both premotor and parietal cortex. This suggests multiple mirror neuron systems in the human brain, dependent on the particular effector with which an action is performed. It remains unclear whether there is a similar systematic differentiation between mirror neuron activations for different types of hand movements, e.g. between reaching movements, and hand–object interactions (including touching) or grasping movements. Observation of static images depicting object prehension versus observation of images depicting object touching results in an increase in activation in bilateral inferior frontal gyrus, suggesting that the less hand–object interaction (touching instead of grasping), the less involvement of the inferior frontal gyrus (Johnson-Frey et al., 2003). It remains unknown whether observation of reaching without touching of an object is similar to this static image observation task, in terms of not activating the inferior frontal gyrus. Likewise, it remains unknown which other brain areas, outside Broca's area or premotor cortex, are differentially active for reaching observation relative to grasping observation.

Reaching (defined as involving some arm transport as opposed to just hand/finger movements) has been difficult to investigate with fMRI, due to problems with head motion caused by the moving hand (see Culham et al., 2006). Typically, fMRI studies have investigated a proxy for reaching, such as delayed pointing (Medendorp et al., 2005, Hagler et al., 2007, Connolly et al., 2003, Astafiev et al., 2003, DeSouza et al., 2000) or using a joystick cursor to a visual target (e.g. Grefkes et al., 2004, Lacquaniti et al., 1997). Despite the difficulties, some fMRI studies have investigated reaching-to-point movements (Kawashima et al., 1996, Frey et al., 2005, Desmurget et al., 2001), reaching-to-touch (e.g. with the knuckles) (Culham et al., 2003), or reaching-to-grasp (Chapman et al., 2002, Frey et al., 2005). Prado et al. (2005) investigated actual reaching. The activations reported for these tasks typically include the medial IPS as well as the precuneus, i.e. more medial areas of the superior parietal lobe. Other activations include the parieto-occipital cortex, supplementary motor cortex, and the cingulate sulcus. In addition, an area located at the junction between the anterior IPS and the inferior postcentral sulcus, hypothesized to be the human homologue of AIP (see Frey et al., 2005, Binkofski et al., 1999), is activated during both grasping and reach-to-point tasks as well as during some pointing tasks (Culham et al., 2006). This suggests some overlap between reaching and grasping. Both grasping and reaching activate the hemisphere contralateral to the moving hand substantially more than the ipsilateral hemisphere. In general, activations for reaching tasks tend to be more dorsal and medial in the parietal lobe (medial to the IPS) compared to object manipulation. Studies that involve a transport phase of the hand prior to an executed grasp (e.g. Culham et al., 2003, Grafton et al., 1996b) tend to find superior parietal activations, whereas studies in which the transport phase is not present, involving just local grasping (e.g. Rizzolatti et al., 1996b) tend to find more inferior parietal activations.

According to Culham et al. (2006), reaching-to-point tasks may actually involve preshaping the hand as well as calculating object properties such as the centroid of the shape, and thus may be different from reaching alone. Similarly, pointing may be expected to be different from actual reaching. Areas activated by delayed pointing activations in humans may thus not be exactly equivalent to macaque reach-related areas. It is also important to note that reaching-to-touch an object still represents a hand–object interaction, even if no grasping occurs, and that this task may thus be different from reaching without touching. Likewise, a grasping pantomime, or a pantomime in which an object is implied but not present, also represents an object-directed action: the object is implicit, and the pantomiming hand is preshaped accordingly. Since no preshaping of the hand needs to happen in reaching-only, pantomimed hand–object interactions are still likely to differ from reaching by activating grasping-related neural circuits.

While several studies have investigated the execution aspect of grasping or reaching-like hand actions, we are aware of no studies that have investigated parieto-frontal mirror neurons for reaching per se. It is thus unknown which brain areas are involved in both execution of reaching and in observation as well as mental simulation of reaching.

In addition, the majority of previous mirror neuron studies have compared only two types of conditions at a time, i.e. either execution with observation of hand actions, or observation with imagery, or execution/imitation with imagery of hand actions (see Grèzes and Decety, 2001). Since different studies used different hand actions (e.g. object manipulation or finger tapping) as well as different objects, it is difficult to draw general conclusions about which brain areas are involved in all three conditions (action execution, observation, and imagery) for a particular hand action. It is also unclear whether there are differences in activation levels between observation, imagery, and execution within mirror neuron areas—for instance, whether observing a hand action is more potent at driving mirror neurons than imagining the same hand action.

Here, we compare execution of visually-guided reaching (i.e. reaching directly towards visually presented targets without the use of a mirror) with observed as well as imagined reaching in the same experiment. Since our task involves no explicit touching or grasping of objects, and therefore no preshaping of the hand to match a viewed object shape, mirror neuron activations for observation as well as imagery of reaching should involve more of the reach-related substrates than hand manipulation-related substrates.

Section snippets

Participants

Sixteen subjects (ten males) participated in this experiment (age range 19–48). One subject was discarded due to excessive head motion. All subjects were right-handed and had normal or corrected-to-normal vision. Human subjects' approval was obtained from the UCSD Institutional Review Board. All subjects gave informed consent.

Stimuli

The stimuli used were photographs of abstract wooden shapes on a black background (see Figs. 1a and c), with five different views taken per shape. The abstract shapes

Results

All three conditions (executed, observed, and imagined reaching) activated a fronto-parietal network when compared to baseline (Fig. 2, Table 1, Table 2, Table 3). Fig. 2 shows average group activations displayed on an inflated cortical surface. The activations for all three conditions overlapped in dorsal premotor cortex, as well as in superior parietal cortex and in the intraparietal sulcus (see Figs. 4a and b). Fig. 3 shows activations from 5 individual subjects who are representative of the

Discussion

We used fMRI to compare human cortical activations for executed, observed, and imagined reaching with the goal of identifying a mirror neuron system that represents reaching and reaching-related behaviors. Our results suggest that such a mirror neuron system exists, and that it bears both differences and similarities to the mirror neuron system underlying grasping movements and object manipulation. Specifically, mirror neurons for execution, imagery, and observation of reaching are found in

Acknowledgments

This work was funded by NSF BCS 0224321 to M.I.S. and by NIH 5T32MH020002, which funded J.D.N. The authors are grateful to Emanuel Todorov and Ruey-Song Huang for helpful input, and to Alan E. Robinson and two anonymous reviewers for comments on an earlier draft. We would also like to thank the UCSD Center for Functional Magnetic Resonance Imaging, and in particular Giedrius T. Buracas and Larry May, for support and technical assistance.

References (65)

  • J. Grèzes et al.

    Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study

    NeuroImage

    (2003)
  • D.J. Hagler et al.

    Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data

    NeuroImage

    (2006)
  • D.J. Hagler et al.

    Parietal and superior frontal visuospatial maps activated by pointing and saccades

    NeuroImage

    (2007)
  • F. Hamzei et al.

    The human action recognition system and its relationship to Broca's area: an fMRI study

    NeuroImage

    (2003)
  • S.H. Johnson-Frey et al.

    Actions or hand–object interactions? Human inferior frontal cortex and action observation

    Neuron

    (2003)
  • 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)
  • F. Lacquaniti et al.

    Visuomotor transformations to memorized targets: a PET study

    NeuroImage

    (1997)
  • M. Matelli et al.

    Parietofrontal circuits for action and space perception in the macaque monkey

    NeuroImage

    (2001)
  • I. Molnar-Szakacs et al.

    Observing complex action sequences: the role of the fronto-parietal mirror neuron system

    NeuroImage

    (2006)
  • K.F. Muakkassa et al.

    Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas

    Brain Res.

    (1979)
  • J. Prado et al.

    Two cortical systems for reaching in central and peripheral vision

    Neuron

    (2005)
  • G. Rizzolatti et al.

    Premotor cortex and the recognition of motor actions

    Cogn. Brain Res.

    (1996)
  • Y.F. Tai et al.

    The human premotor cortex is “mirror” only for biological actions

    Curr. Biol.

    (2004)
  • R.A. Andersen et al.

    Intentional maps in posterior parietal cortex

    Annu. Rev. Neurosci.

    (2002)
  • S.V. Astafiev et al.

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

    J. Neurosci.

    (2003)
  • S.V. Astafiev et al.

    Extrastriate body area in human occipital cortex responds to the performance of motor actions

    Nat. Neurosci.

    (2004)
  • A. Battaglia-Mayer et al.

    Early coding of reaching in parietooccipital cortex

    J. Neurophysiol.

    (2000)
  • F. Binkofski et al.

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

    Eur. J. Neurosci.

    (1999)
  • O. Blanke et al.

    Location of the human frontal eye field as defined by electrical cortical stimulation: anatomical, functional and electrophysiological characteristics

    NeuroReport

    (2000)
  • G. Buccino et al.

    Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study

    Eur. J. Neurosci.

    (2001)
  • G. Buccino et al.

    The mirror neuron system and action recognition

    Brain Lang.

    (2004)
  • C.A. Buneo et al.

    Direct visuomotor transformations for reaching

    Nature

    (2002)
  • Cited by (0)

    View full text