Elsevier

NeuroImage

Volume 54, Issue 3, 1 February 2011, Pages 2401-2411
NeuroImage

Working memory maintenance of grasp-target information in the human posterior parietal cortex

https://doi.org/10.1016/j.neuroimage.2010.09.080Get rights and content

Abstract

Event-related functional magnetic resonance imaging was applied to identify cortical areas involved in maintaining target information in working memory used for an upcoming grasping action. Participants had to grasp with their thumb and index finger of the dominant right hand three-dimensional objects of different size and orientation. Reaching-to-grasp movements were performed without visual feedback either immediately after object presentation or after a variable delay of 2–12 s. The right inferior parietal cortex demonstrated sustained neural activity throughout the delay, which overlapped with activity observed during encoding of the grasp target. Immediate and delayed grasping activated similar motor-related brain areas and showed no differential activity. The results suggest that the right inferior parietal cortex plays an important functional role in working memory maintenance of grasp-related information. Moreover, our findings confirm the assumption that brain areas engaged in maintaining information are also involved in encoding the same information, and thus extend previous findings on working memory function of the posterior parietal cortex in saccadic behavior to reach-to-grasp movements.

Research Highlights

►Right inferior parietal cortex maintains grasp-target information in working memory. ►Activity in right inferior parietal cortex persists across variable memory delays. ►Grasp-target encoding and maintenance share neural substrates.

Introduction

Short-term storage of visual targets provides a great flexibility in planning and executing actions, as the movement does not have to depend on current available sensory information. Persistent neural activity is believed to be the mechanism that temporally bridges the gap between past sensory stimuli and contingent memory-guided actions. Such sustained delay-period activity has been reported for both human and monkey prefrontal and posterior parietal cortices (Funahashi et al., 1989, Andersen and Buneo, 2002, Curtis and D'Esposito, 2003). Accordingly, lesion or inactivation of these areas can cause severe impairments in working memory (Curtis and D'Esposito, 2004, Dias and Segraves, 1999, Li et al., 1999, Muri et al., 1996).

So far, movement-related working memory functions have been extensively investigated in the oculomotor system using delayed saccade tasks. In this task, visual information about the target location must be stored over several seconds and later used to guide a memory-based saccade. Human neuroimaging studies have provided converging evidence for a widely distributed fronto-parietal network functionally related to the maintenance of spatial information in working memory. Activity in oculomotor centers, such as the frontal eye fields (FEF) or supplementary eye fields (SEF), and the posterior parietal cortex (PPC) have consistently been shown to prevail throughout a memory delay until a saccadic response is generated (Brown et al., 2004, Connolly et al., 2002, Curtis and D'Esposito, 2006, Curtis et al., 2004, Schluppeck et al., 2006, Postle et al., 2000a, Postle et al., 2000b). Oculomotor areas seem to maintain a prospective motor code, whereas higher-order areas in the frontal and parietal cortex preferentially represent a retrospective sensory (visuospatial) code (Curtis et al., 2004; for divergent results, see Srimal and Curtis, 2008).

The question arises whether persistent activity in higher-order frontal or parietal areas is specifically tied to saccadic working memory or whether a similar fronto-parietal network underlies working memory for manual actions as well. Electrophysiological studies in monkeys provide preliminary evidence that the PPC, in particular the grasp-specific anterior intraparietal area (AIP), is involved in maintaining visuospatial information of a grasp target. For example, Murata et al. (1996) briefly presented a monkey one of six different grasp targets which required different hand movements. After a 2 s delay period in the dark, the monkey was asked to grasp the target without visual feedback. Sustained activity in AIP neurons was observed across the delay period, although the grasp target was not visible. Most of the neurons also responded to the sight of the target and showed the same selectivity for object features during object fixation and delay period.

In line with the results in monkeys, a recent neuroimaging study found overlapping activity in the PPC for both immediate and delayed hand actions (Himmelbach et al., 2009). Given patient data, however, real-time and memory-based hand movements are supposed to be processes by different cortical systems: immediate actions by the parieto-occipital areas of the dorsal visual stream and delayed actions by the inferotemporal–occipital areas of the ventral visual stream (Goodale et al., 1994, Milner et al., 1999b, Milner et al., 1999a).

Here, we applied functional magnetic resonance imaging (fMRI) to identify the human cortical areas involved in working memory maintenance of visuospatial target information for grasping. To identify cortical areas whose activity persists throughout the delay period, we used six different time delays ranging from 2 to 12 s in 2 s increments. Since longer delays are more informative for mnemonic processes than shorter ones, we included more trials with longer delay lengths (cf., Schluppeck et al., 2006). The jittered delays improved the temporal de-correlation of the blood oxygenation level dependent (BOLD) signal coupled with the target presentation and the motor response and thus allowed us to disambiguate the variance attributed to the delay period. Due to the randomized presentation of trials of different delay length and trials without any delay, participants could not predict when they were going to respond and thus remained in a state of readiness during each delay period. In addition, we varied the length and orientation of the grasp target so that the participant could not prepare for one and the same grasp response in all trials. Rather, the participants had to store and actively maintain specific grasp-related visuospatial information in each trial. For cortical regions involved in working memory maintenance of grasp-relevant visuospatial information, we expect sustained activity above-baseline level throughout the duration of each of the six different delay periods.

Section snippets

Participants

Twenty-three healthy adults participated in the study. Data of 2 participants were discarded due to severe motion artefacts resulting in a final sample of 21 adults (six males; mean age ± SD: 23.6 ± 3.0 years). They were all right-handed as measured by the Edinburgh Handedness Inventory (Oldfield, 1971). All participants provided informed consent according to the Declaration of Helsinki before the experiment and they received monetary compensation.

Grasping stimuli and experimental setup

Grasping stimuli were white rectangular bars of two

Behavioral data

Movement initiation time, i.e., the time from the go-signal until movement start, and movement time, i.e., the time between release of the home button and return, were analyzed. Mean movement initiation times for immediate and delayed grasping trials did not differ significantly and amounted to 470 ms (SD = 96 ms) and 494 ms (93) (t20 = 1.89, p = 0.07), respectively. In contrast, mean movement times were significantly longer for delayed than immediate grasps (immediate: 1522 ± 343 ms, delayed 1572 ± 350 ms; t

Discussion

We used event-related fMRI to investigate cortical areas involved in maintaining grasp-target information in working memory. To test for sustained delay-period activity, a crucial feature of working memory maintenance, we examined the hemodynamic response for variable delay lengths. We found an area in the right inferior parietal cortex that showed persistent delay-period activity above-baseline level throughout each of the delay periods. Moreover, posterior parietal activity significantly

Conclusion

We have assessed the cortical processes underlying working memory maintenance of visuospatial information used for grasping. We found persistent neural activity in the right inferior parietal cortex bridging the time between the perception of the grasp target and the grasping movement. Our results further extend previous findings on working memory maintenance and saccadic behavior and suggest that the inferior parietal cortex plays an important role in working memory maintenance of target

Acknowledgments

We thank Isabell Sauerbier and Owino Eloka for their help in data collection and Denise Y. Henriques and Iseult A. M. Beets for proof-reading the present manuscript. We also thank Jan Gläscher for his assistance with the rfxplot toolbox. This research was supported by grant FI 1567 to Katja Fiehler and Frank Rösler, grant FR 2100/1-3 to Volker Franz and the research unit DFG/FOR 560 ‘Perception and Action’, all from the German Research Foundation (DFG).

References (93)

  • M.A. Goodale et al.

    Differences in the visual control of pantomimed and natural grasping movements

    Neuropsychologia

    (1994)
  • J. Grèzes et al.

    Does visual perception of objects afford action? Evidence from a neuroimaging study

    Neuropsychologia

    (2002)
  • C. Hesse et al.

    Memory mechanisms in grasping

    Neuropsychologia

    (2009)
  • M. Himmelbach et al.

    Brain activation during immediate and delayed reaching in optic ataxia

    Neuropsychologia

    (2009)
  • M. Jeannerod

    Mental imagery in the motor context

    Neuropsychologia

    (1995)
  • K.S. LaBar et al.

    Neuroanatomic overlap of working memory and spatial attention networks: a functional MRI comparison within subjects

    Neuroimage

    (1999)
  • M. Lotze et al.

    Motor imagery

    J. Physiol. Paris

    (2006)
  • A.D. Milner et al.

    Delayed reaching and grasping in patients with optic ataxia

    Prog. Brain Res.

    (2003)
  • T.R. Oakes et al.

    Comparison of fMRI motion correction software tools

    Neuroimage

    (2005)
  • R.C. Oldfield

    The assessment and analysis of handedness: the Edinburgh inventory

    Neuropsychologia

    (1971)
  • B.R. Postle

    Distraction-spanning sustained activity during delayed recognition of locations

    Neuroimage

    (2006)
  • B.R. Postle

    Working memory as an emergent property of the mind and brain

    Neuroscience

    (2006)
  • B.R. Postle et al.

    Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks

    Brain Res. Protoc.

    (2000)
  • S. Rossit et al.

    Immediate and delayed reaching in hemispatial neglect

    Neuropsychologia

    (2009)
  • A.T. Sack et al.

    Tracking the mind's image in the brain II: transcranial magnetic stimulation reveals parietal asymmetry in visuospatial imagery

    Neuron

    (2002)
  • V. Singh-Curry et al.

    The functional role of the inferior parietal lobe in the dorsal and ventral stream dichotomy

    Neuropsychologia

    (2009)
  • R. Srimal et al.

    Persistent neural activity during the maintenance of spatial position in working memory

    Neuroimage

    (2008)
  • M.C. Stoeckel et al.

    A fronto-parietal circuit for tactile object discrimination: an event-related fMRI study

    Neuroimage

    (2003)
  • E. Tunik et al.

    Beyond grasping: representation of action in human anterior intraparietal sulcus

    Neuroimage

    (2007)
  • G. Vallar et al.

    The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man

    Neuropsychologia

    (1986)
  • K.J. Worsley et al.

    Analysis of fMRI time-series revisited—again

    Neuroimage

    (1995)
  • R.A. Andersen et al.

    Intentional maps in posterior parietal cortex

    Annu. Rev. Neurosci.

    (2002)
  • Y. Benjamini et al.

    Controlling the false discovery rate—a practical and powerful approach to multiple testing

    J. R. Stat. Soc. B

    (1995)
  • N.E. Berthier et al.

    Visual information and object size in the control of reaching

    J. Mot Behav.

    (1996)
  • F. Binkofski et al.

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

    Eur. J. Neurosci.

    (1999)
  • M.R. Brown et al.

    Comparison of memory- and visually guided saccades using event-related fMRI

    J. Neurophysiol.

    (2004)
  • C.A. Buneo et al.

    Properties of spike train spectra in two parietal reach areas

    Exp. Brain Res.

    (2003)
  • S.H. Butler et al.

    Impairments of oculomotor control in a patient with a right temporo-parietal lesion

    Cog. Neuropsychol.

    (2006)
  • C. Cavina-Pratesi et al.

    FMRI reveals a dissociation between grasping and perceiving the size of real 3D objects

    PLoS ONE

    (2007)
  • H.J. Choi et al.

    Cytoarchitectonic identification and probabilistic mapping of two distinct areas within the anterior ventral bank of the human intraparietal sulcus

    J. Comp. Neurol.

    (2006)
  • J.D. Connolly et al.

    Human fMRI evidence for the neural correlates of preparatory set

    Nat. Neurosci.

    (2002)
  • J.D. Connolly et al.

    FMRI evidence for a ‘parietal reach region’ in the human brain

    Exp. Brain Res.

    (2003)
  • J.C. Culham

    Human Brain Imaging Reveals a Parietal Area Specialized in Grasping

  • J.C. Culham et al.

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

    Exp. Brain Res.

    (2003)
  • C.E. Curtis et al.

    The effects of prefrontal lesions on working memory performance and theory

    Cogn. Affect. Behav. Neurosci.

    (2004)
  • C.E. Curtis et al.

    Selection and maintenance of saccade goals in the human frontal eye fields

    J. Neurophysiol.

    (2006)
  • Cited by (44)

    • The neural underpinnings of haptically guided functional grasping of tools: An fMRI study

      2019, NeuroImage
      Citation Excerpt :

      Notably, the substantial overlap of (and little between-task differences for) the temporo-occipital and inferior parietal cortices, i.e., their similar engagement above baseline in planning both kinds of grasps, goes against an interpretation of tool-specific control of skilled hand postures and kinematics exerted by these regions in the absence of overt movements (cf. Buxbaum et al., 2014; Osiurak and Badets, 2017). Consistent with a plethora of earlier studies on delayed manual actions, including grasping (e.g., Fiehler et al., 2011; Singhal et al., 2013), and partly corroborating our results obtained in the haptic exploration phase, the execution of haptically guided functional grasps of tools was associated with greater bilateral engagement of the medial and superior lateral (dorso-dorsal) parieto-frontal regions typically considered as the seat of essential motor control (Jeannerod, 1988; Milner and Goodale, 1993; see also Kroliczak et al., 2008; Monaco et al., 2015). Even though no visual feedback was present, there was also substantial bilateral involvement of early visual cortices (suggesting a role of visual imagery, Singhal et al., 2013) and aIC, which has been previously linked to grasping tasks as well (Fink et al., 1997; Kroliczak et al., 2007; Mutschler et al., 2009; see also Kurth et al., 2010).

    • Directional tuning during reach planning in the supramarginal gyrus using local field potentials

      2019, Journal of Clinical Neuroscience
      Citation Excerpt :

      Different regions covered by the MP grid also showed increased high frequency activation with decreased low frequency activation, but during the Delay phase only. This data agrees with fMRI studies showing increased activity in the right inferior parietal lobule during the delay phase of a grasping task [27,28]. Studies involving electrical stimulation of the human inferior parietal lobule elicited a “desire to move” [29,30].

    • Time-resolved decoding of planned delayed and immediate prehension movements

      2018, Cortex
      Citation Excerpt :

      Rather, we argue that they constitute a common thread for planned movements that do not depend on the presence of a delay. Early neuropsychology and behavioral evidence suggested distinct cortical pathways for memory-driven and immediate actions (Hu et al., 1999; Milner, Dijkerman, McIntosh, Rossetti, & Pisella, 2003, 2001; Goodale et al., 2004; Rossit, Szymanek, Butler, & Harvey, 2010; but see Himmelbach & Karnath, 2005; Franz, Hesse, & Kollath, 2009; Hesse & Franz, 2009; Himmelbach et al., 2009; Fiehler et al., 2011). In highlighting a convergence between delayed and non-delayed movement plans (at the level of neural representations), our data are in line with results by Fiehler et al. (2011), which demonstrated that overlapping clusters of voxels in human primary motor cortex and dorsal premotor cortex are recruited during the planning phase and immediate execution of grasping movements.

    View all citing articles on Scopus
    View full text