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Timing and communication of parietal cortex for visuomotor control
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ScienceDirect Timing and communication of parietal cortex for visuomotor control Alexandra Battaglia-Mayer, Simone Ferrari-Toniolo and Federica Visco-Comandini In both monkeys and humans, motor cognition emerges from a parietal–frontal network containing discrete dominant domains of visual, eye and hand signals, where neurons are responsible for goal and effector selection. Within these domains, the combination of different inputs shape the tuning properties of neurons, while local and long cortico-cortical connections outline the architecture of the distributed network and determine the conduction time underlying eye–hand coordination, necessary for visually guided operations in the action space. The analysis of the communication timing between parietal and frontal nodes of the network helps understanding the sensorimotor cortical delays associated to different functions, such as online control of movement and eye–hand coordination, and opens a new perspective to the study of the parieto-frontal interactions. Address Department of Physiology and Pharmacology, SAPIENZA University of Rome, P.le Aldo Moro 5, 00185 Rome, Italy Corresponding author: Battaglia-Mayer, Alexandra ([email protected])
system (PFS) these operations depend on communication between areas. New perspectives on PFS dynamics have been opened by recent studies on the conduction time of messages from PPC to different target areas. By combining information about axon diameter, therefore speed, with axon length, parietal conduction delays to different structures were estimated [1]. The conduction delay of Superior Parietal Lobule (SPL) area PEc to dorsal premotor cortex (PMd) is of about 3.3 ms, to anterior cingulate motor area (CMAd) is 3.5 ms, to motor cortex is only 1.9 ms (Figure 1). The delay to the corpus callosum is about 3 ms [2]. Furthermore, the projection of area PEc to PMd consists of axons of different diameters, as for the other parietal projections, which implies that inter-areal communication is based on temporally dispersed conduction delays. This mechanism has the potential of modulating the oscillatory regimes [3] of the cortex, thus influencing the inter-areal synchrony, which has been proposed, among others, as a potential mechanism of cortical communication during motor planning and execution, when information transfer can take the form of traveling, high-frequency waves [4].
Current Opinion in Neurobiology 2015, 33:103–109 This review comes from a themed issue on Motor circuits and action Edited by Ole Kiehn and Mark Churchland
http://dx.doi.org/10.1016/j.conb.2015.03.005 0959-4388/# 2015 Published by Elsevier Ltd.
Introduction The functional organization and connectivity of posterior parietal cortex (PPC) in monkeys provide a background to explore the neural basis of motor cognition and stays at the core of daily functions, such as eye–hand coordination and online control of hand movement. A new perspective on these functions and on parieto-frontal dynamics is offered by the study of the conduction delays of parietal and frontal areas to their targets and by the putative mechanisms whereby these areas reciprocally interact for motor control.
Timing of cortical communication Motor behavior is framed by the processing time required whenever a change of state occurs. In the parieto-frontal www.sciencedirect.com
Communication based on temporally dispersed delays can also multiply at the target area the number of local neuronal pools on which reciprocal parieto-frontal signaling can operate, potentially allowing a simultaneous representation of sensorimotor signals within multiple reference frame by different pools of neurons. Cell belonging to each pool can be identified and selected by a common timing of arrival of action potential at synaptic level, in other words by the temporal feature of their input. In such a way, different reference frames for eye– hand action can be simultaneously represented beyond the single cell level [5]. The overall result could be an increase of the computational power of parieto-frontal processing streams. This mechanism can also favor the representation of different rule-based motor goals [6] or reaching decisions [7] within parietal and frontal areas. By fractionating the time of arrival of action potentials on the target structures through a wide spectrum of conduction delays, any given cortical area can scale the phase and strength of connections with their targets, by modulating the timing of activation of its neurons. As an example, the effective connection strength between areas can be increased, if the timing of firing of cortical projecting neurons with small axon diameter, therefore slow conduction velocity, leads the activation of neurons with large axon Current Opinion in Neurobiology 2015, 33:103–109
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transmission and decision delays, thus generating psychological refractory periods, as when two sensory signals are presented in sequence [13] in double-step tasks. Fast parieto-frontal signaling is required for on line control of action and for eye–hand coordination underlying reaching. We will briefly discuss recent studies on these issues.
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Conduction delays (ms) of projections from parietal area PEc to frontal areas and corpus callosum. Arrow thickness is inversely proportional to conduction delay (red numbers). Drawn on the basis of results from Refs. [1,2,3].
diameter and faster conduction velocity. Studies of the temporal dynamics of parieto-frontal interactions indicates that while parietal and premotor cortex oscillate in-phase in the beta band (15–30 Hz), partial spike-field coherence in parietal cortex is asynchronous with oscillations in premotor cortex during periods of attentive fixation and motor planning [8], probably down-modulating parieto-frontal communication. Using a population partial spike-field coherence approach to study temporal interactions between parietal areas 2/5 and motor cortex (MI), only a weak parietal influence was found on MI during reach planning, but a strong one during reach movement [9], with parietal cortex influencing encoding of movement direction in primary motor cortex. In the information transfer between somatosensory (SI), motor, and PPC, SI seems to be a major source of information flow in the beta band concerning feed-back signals necessary for continuous estimate of limb parameters [10,11]. The timing of communication between brain areas impacts on different functions. For instance, the nature of the transformation required during motor planning can shape the time-sequence of activation of frontal and parietal areas [12]. A bottleneck may arise when adding Current Opinion in Neurobiology 2015, 33:103–109
Encoding multiple movement parameters and combination of visual, eye and hand information by individual cells stay at the core of parietal online control of reach trajectory, such as when a target suddenly moves to a new location in space. After the pioneering study by Georgopoulos’s group (1983) in MI [14], this subject has been revitalized by recent analysis [15,16] of SPL areas PE/ PEc, as well as of PMd and M1 in monkeys. During reach correction, besides movement direction and instantaneous arm position in space, parietal activity specifies and reflects hand velocity in a way that accurately predicts (‘neural trajectories’) the hand trajectory correction. No special classes of parietal cells are recruited in this process by the change in target location, which instead is encoded through a graded utilization of the kinematics variables encoded by parietal neurons. The same applies to PMd and M1, suggesting that a common mechanism underlies trajectory formation and correction in the cerebral cortex [17]. Within this network, premotor cortex first provides the higher-order signal about the change of target location, thus calling for the specification of a new reach goal. This is in line with the consequences of its lesion in humans, which delays reach onset, but not impair reach accuracy [18], and with its role in tasks requiring switching of motor plans [19]. Thanks to the fine-grain specification of hand kinematics both before and during the hand movement toward first or second target location, SPL areas can provide both the early transformation necessary to specify the reach goal, as well as a continuous estimate of limb position, speed and movement direction. Motor cortex, thanks to the strong relations with arm movement parameters and the direct projections to the spinal cord is involved in the final composition of the reach movement. The causal role of areas PE/PEc in the online control is shown by their reversible bilateral inactivation [20], which results in the impaired online control of hand trajectory (for a review see [17]), as also observed in patients with optic ataxia (OA). The deficit in trajectory correction is in part dependent on a delayed saccade to the second target location, which is coherent with the combined influence of eye–hand signals on SPL neural activity, as well as with the eye movement disorders of OA patients [21]. No clear pattern of eye RT alteration was observed in the inactivation study of the Parietal Reach Region (PRR) [23], where however only the consequence of unilateral parietal silencing has been explored. In the same study, a deficit in saccade amplitude was instead found, when eye and hand moved www.sciencedirect.com
Parietal cortex and voluntary movement Battaglia-Mayer, Ferrari-Toniolo and Visco-Comandini 105
concurrently, contrary to the unimpaired saccades when the eye moved alone [22,23]. When studying PPC physiology the relative eye and hand position, imposed by the task demands, is a crucial parameter that deserves a particular attention. In this context, the importance of the degree of eye–hand coupling is highlighted by a case report [24] (Figure 2a) of a parietal patient showing a severe impairment in the specification of the direction of the hand force applied to an isometric manipulandum, necessary to move a cursor to visual targets. This impairment indicates that: first, OA generalizes to isometric conditions, that is to visuomotor transformations leading to action in absence of movement, regardless of the imposed physical relationship between the manipulandum and cursor; second, PPC is involved not only in the specification of kinematics [15,25], but also in that of higher-order dynamics underlying hand action. This defective control occurred both in peripheral and central vision. In the latter, eye and hand position were still decoupled, because of the task-imposed dissociation between the position of the visual target on the monitor and the manipulandum (Figure 2b). Therefore PPC seems to contain an abstract representation of the directional motor output, where the computation of the relative position of the hand and of the eye plays a crucial role, as originally implicated by the preferred directions clustering of eye and hand signals within the global tuning fields (GTF ; Figure 2c) [26] of neurons in areas V6A and PEc, and by the observation that in PPC the strongest modulation occurs when the hand moves toward the fixation point [27], thus nulling the ‘eye– hand motor error’. This brings us to the second topic, that is eye–hand coordination.
PPC and eye–hand coordination during reaching A role of PPC in eye–hand coordination is supported by older observations [28–32] that: first, in most parietal areas of the monkey brain, individual neurons combine directional eye and hand signals, although with different dominance; second, the dynamic properties of individual cells [26] and local inhibition [33] give rise to GTF, thanks to which SPL areas can encode spatially co-ordinated eye– hand actions [26]; third, an effector-independent ‘temporal clock’ signaling both target presentation and movement onset exists in both SPL and IPL areas [27]. In SPL, reaching activity is higher and leads in time that of IPL [27,34]. In the latter, population activity is stronger for coordinated eye–hand movement rather than for independent ones. In IPL areas Opt, PG (7a), the large majority of cells is of eye–hand combinatorial type, and displays greater activity when the hand moves toward the fixation point. The neural peak observed for coordinated eye–hand or independent eye or hand movement disappears during no-go tasks [27]. www.sciencedirect.com
The interest in eye–hand coordination has resurged in recent years. Neural activity in the lateral intraparietal area (LIP) and in PRR was studied [35] while monkeys made reaches or saccades to memorized targets. In both areas, local field potentials (LFP) power in the beta band correlates with saccadic RT only during coordinated reaches, implying that decreasing the power in this band could speed movement onset. This is in line with previous studies of the motor system (see [36] for a review), showing that entrainment of MI to a 20 Hz-rhythm during a visuomotor task enhances cortico-muscle beta band coherence and slows voluntary action [37]. Furthermore successful stopping in a Go/No-Go task is related to enhanced beta band activity in the inferior frontal cortex [38]. In LIP, cells with spiking coherent with beta band LFP activity predicts the reach RTs for coordinated eye and hand movements, not of saccades when the eyes move alone. This study points toward a model based on a shared LIP–PRR representation as the basis of eye– hand coordination, on the assumption of a mutual excitation between these regions [35,39], considered as independent effector-specific integrators. In SPL areas PEc and MIP, beta synchrony of LFPs dominates the early planning of coordinated eye–hand movement, and its onset is delayed when decoupling the eye from hand action [40]. Inactivation studies have generated different views on the causal role of parietal areas on eye–hand coordination. Unilateral inactivation of LIP during memory-guided saccades or coordinated reaches, resulted in delayed eye and hand RTs of coordinated reaches, unaffected temporal eye–hand coupling, increase in saccade errors, but not in reach endpoint errors, with hand RT unaffected for reaches without a concurrent saccade [41]. Also based on the evidence of different attention systems for eye and hand movement [42] the authors concluded that LIP does not play a crucial role in eye–hand coordination, but rather in saccade planning and related-attention. A more recent study from the same group showed that unilateral muscimol injections in a sector of the medial bank of the IPS, referred to as PRR [43], produced only a specific increase of RT and decrease of movement speed of the contralateral limb, leaving unaffected not only saccade RT, but also the temporal correlation between eye and hand movement. These results were congruent with PRR viewed as a motoric region, with eye–hand coordination occurring later in the eye-control and handcontrol pathways. In our previous study [20], bilateral lesion of area PE/PEc produced a significant elongation of hand RT, that was only in part explained by the concomitant increase of eye RTs, an increase of movement time duration, and no effect on the correlation between eye and hand RTs. The conclusion that PRR does not play a causal role in eye–hand coordination was however contended by a subsequent unilateral PRR inactivation study [23], reporting a decrease in temporal eye and hand RT Current Opinion in Neurobiology 2015, 33:103–109
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Visuomotor impairments after parietal lesion and the role of eye–hand coupling. (a) A parietal patient exerted force in different directions on an isometric joy-stick, as to move a visual cursor to different lighted targets on a screen. The dispersion of cursor’s endpoints (black dots), resulting from force output of ipsilesional and contralesional hand toward targets (red dots) in central or peripheral vision, are presented as 95% confidence ellipses, together with data from a control subject. The black segment within each ellipse indicates the constant error, that is the distance of the mean cursor endpoint (red cross) from the target in each direction. (b) Patient’s absolute errors observed during natural reaching and in the isometric task for both foveal and extrafoveal targets. Below each bar, a schematic representation of the final, relative position of eye, hand and target (gray circle) is shown for each task condition. The cross indicates the fixation point, when required to maintain eye fixation during the task. The eye motor error (ETg), hand motor error (HTg), and their relative difference (HETg) are shown for each task condition, together with a schematic general representation of their definition on the right of the bar graph. Modified from [24]. (c) Example of global tuning field (GTF) of a parietal neuron, where the preferred directions (PDs) during separated or coordinated eye and hand movements cluster within a restricted part of the work-space, thus allowing combination of eye and hand signals in a spatially congruent directional domain. Arrows indicate PDs in different epochs (hRT/eRT, hand/eye reaction time; hMT/eMT, hand/eye movement time; eTHT, eye target holding time) of different tasks (coordinated eye– hand reaching, blue; reaching without concomitant saccades, green; saccade only, red. Modified from [29]).
correlation during reaches, although for only one out of six targets. In spite of this, the authors assigned to PRR an essential role in establishing a tight temporal coupling between the two effectors. Current Opinion in Neurobiology 2015, 33:103–109
The discrepancies of these results can be due to differences of injection sites and in the definition of the functional areas that belongs to the so-called PRR, which differs across studies of the same authors that have www.sciencedirect.com
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actually introduced this terminology. More important, another large set of reach-related parietal areas, such as PE, PEa and PGm (7m) in SPL, and 7a in IPL [27,44,45] are influenced by both eye and hand signals. These areas are not included in PRR. This limits the comprehension of the functional role of PPC, within the more extended network for reach control. As a matter of fact, all the above mentioned inactivation studies silenced only a small region of SPL, including the study of Battaglia-Mayer et al. [20], where a consistent impairment was found only after bilateral inactivation of areas PE/PEc. A second problem is that the studies by Andersen, Snyder and Pesaran’s teams [22,35,43], while recognizing the presence of saccade-related activity in PRR, all consider it as a hand-specific module which plays no causal role in saccade generation. Although a causal role of this region in saccade planning remains to be shown, there is unequivocal evidence that all the areas that are part of it (whatever defined), such as V6A, PEc, MIP, combine eye and hand signals with different strength, depending on their position within the parieto-frontal gradient, as also occurs in areas PEa, PGm and in others IPL areas, such as Opt and PG [31,44], thus providing a necessary neural substrate for eye–hand coordination. These areas are therefore to be regarded as effector-dominant, not effector-specific, and their role will have to carefully evaluated within the PFS for a full comprehension of cortical encoding of reaching, which cannot be merely based on PPR operations. A potential way to reconcile different views is provided by the observation that in the longitudinal axis of PPC, including both SPL and IPL, parietal neurons combines eye and hand signals in a task-dependent fashion. To specify a reach goal, in the posterior (areas V6A, PGm) and intermediate (PEc, MIP) SPL areas, of which PRR is one part, a selection process will first recruit neural populations responsible for the composition of the command for reaching. Corollary and re-entrant signaling operated through reciprocal excitatory SPL–IPL connections can recruit in IPL pre-saccadic cells (mostly in LIP), as to shape an ad hoc oculomotor command and provide information about saccade onset. An early eye–hand temporal coupling could be achieved at this stage, together with relative attention allocation. The ipsilateral cortical projections of the SPL to PMd and MI, and of the IPL to the FEF, respectively, will be the final cortical stage for the composition of parallel motor commands for the eye and the hand. The presence of distinguishable visuospatial and motor peaks signaling target localization and movement onset in both FEF [46] and M1 [28] support this view. The involvement of PMd in this process is of interest also in the light of its potential role in breaking the natural eye–hand coupling, or changing reach trajectory [15,16,47], whenever required. The final temporal locking between eye and hand information could be achieved in the superior colliculus (SC), which in addition to the projections from IPL and FEF, is also target of projections from the ‘lateral www.sciencedirect.com
grasping network’ [48]. If similar projections also arise from the SPL areas, as it is reasonable to assume by the presence of reach-related neurons in the SC [49], a combined cortical input from both SPL and IPL could temporally lock eye and hand movement, thus shaping the temporal activation profile of reach neurons in the SC and underlying reticular formation [49]. At the motor output level, cortico-spinal and reticulo-spinal projections on spinal interneurons will convey hand information already temporally locked to the eye, also thanks to the projection from SC to the saccade generators of the midbrain and pons. This would strengthen the importance of these structures in the subcortical control of eye–hand coordination and reconcile, to some extent, conflicting results of the literature on neural basis of eye–hand coordination. In the PFS, the selection and recruitment of specific areas, among the many combining eye–hand signals, will depend on the task and on the transformation rules imposed by each specific remapping process.
Conclusions Different sources of information in the last years stress that the motor functions of PPC are organized along a visuomotor parietal gradient. Thanks to a broad range of cortico-cortical conduction delays, PPC can modulate the oscillatory regimes of the PFS, influencing the inter-areal synchrony that seems important for motor planning and execution. New evidence on the consequences of parietal lesion on isometric actions, that is, in absence of movement, such as when playing a video-game or moving a robot arm in an industrial setting or in a surgical theatre, confirms the causal role of PPC in motor control, particularly when gaze and hand goals are decoupled. The computation of the spatial congruency of eye–hand directional signals seems to occur in the SPL, which however does not seem to play a causal role in the temporal coupling of eye–hand coordination, although so far inactivation studies have only involved a small sector of it. This coupling probably requires the participation of other areas of the PFS and/or is achieved subcortically, in the SC and underlying reticular formation.
Conflict of interest statement Nothing declared.
Acknowledgement This study was supported by the MIUR of Italy (Grant no. 2010XPMFW4_004 to ABM).
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17. Battaglia-Mayer A, Buiatti T, Caminiti R, Ferraina S, Lacquaniti F, Shallice T: Correction and suppression of reaching movements in the cerebral cortex: physiological and neuropsychological aspects. Neurosci Biobehav Rev 2014, 42:232-251. 18. Buiatti T, Skrap M, Shallice T: Reaching a moveable visual target: dissociations in brain tumour patients. Brain Cogn 2013, 82:6-17. The larger study-group available in the literature on control of reaching after parietal and frontal lesions in humans, with special emphasis on optic ataxia. 19. Pastor-Bernier A, Tremblay E, Cisek P: Dorsal premotor cortex is involved in switching motor plans. Front Neuroeng 2012 http:// dx.doi.org/10.3389/fneng.2012.00005. 20. Battaglia-Mayer A, Ferrari-Toniolo S, Visco-Comandini F, Archambault P, Saberi-Moghadam S, Caminiti R: Impairment of online control of hand and eye movements in a monkey model of optic ataxia. Cereb Cortex 2012, 23:2644-2656. The first monkey model of the defective online correction of hand movement trajectory that characterizes OA in humans. This study shows that the delayed hand correction after parietal inactivation is in part dependent on delayed saccade toward the target location, as also implied by neuropsychological studies (see Ref. [21]) in humans. Delayed saccades were not observed in the inactivation study by Hwang et al. [23]. 21. Gaveau V, Pe´ lisson D, Blangero A, Urquizar C, Prablanc C, Vighetto A, Pisella L: Saccade control and eye–hand coordination in optic ataxia. Neuropsychologia 2008, 46:475-486. 22. Hwang E, Hauschild M, Wilke M, Andersen R: Inactivation of the parietal reach region causes optic ataxia, impairing reaches but not saccades. Neuron 2012, 76:1021-1029. This study inactivated a SPL region (PRR) which is similar to that inactivated in [20]. In this paper eye movements are studied in a ‘saccade only’ task, and not in the context of coordinated eye–hand movements. No information about timing is given. 23. Hwang JE, Hauschild M, Wilke M, Andersen R: Spatial and temporal eye–hand coordination relies on the Parietal Reach Region. J Neurosci 2014, 34:12884-12892. 24. Ferrari-Toniolo S, Papazachariadis O, Visco-Comandini F, Salvati M, D’Elia A, Di Berardino F, Caminiti R, Battaglia-Mayer A: A visuomotor disorder in the absence of movement: does optic ataxia generalize to learned isometric hand action? Neuropsychologia 2014, 63:59-71. A case report of parietal patients with lesion in the SPL and medial bank of IPS and displaying OA under isometric condition. This is the first case in the literature of a parietal patient suffering from defective control of hand force output. It indicates that the conclusions of the study by HamelPaˆquet et al. [25] need critical re-evaluation and update. 25. Hamel-Paˆquet C, Sergio L, Kalaska J: Parietal area 5 activity does not reflect the differential time-course of motor output kinetics during arm-reaching and isometric-force tasks. J Neurophysiol 2006, 95:3353-3370. 26. Battaglia-Mayer A, Ferraina S, Mitsuda T, Marconi B, Genovesio A, Onorati P, Lacquaniti F, Caminiti R: Early coding of reaching in the parieto occipital cortex. J Neurophysiol 2000, 83:2374-2391. 27. Battaglia-Mayer A, Mascaro M, Caminiti R: Temporal evolution and strength of neural activity in parietal cortex during eye and hand movements. Cereb Cortex 2007, 17:1350-1363. 28. Johnson P, Ferraina S: Cortical networks for visual reaching: intrinsic frontal lobe connectivity. Eur J Neurosci 1996, 8:1358-1362. 29. Battaglia-Mayer A, Ferraina S, Genovesio A, Marconi B, Squatrito S, Molinari M, Lacquaniti F, Caminiti R: Eye–hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex www.sciencedirect.com
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and parieto-frontal association projections. Cereb Cortex 2001, 11:528-544. 30. Marconi B, Genovesio A, Battaglia-Mayer A, Ferraina S, Squatrito S, Molinari M, Lacquaniti F, Caminiti R: Eye–hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb Cortex 2001, 11:513-527. 31. Rozzi S, Ferrari P, Bonini L, Rizzolatti G, Fogassi L: Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. Eur J Neurosci 2008, 28:1569-1588. 32. Burnod Y, Baraduc P, Battaglia-Mayer A, Guigon E, Koechlin E, Ferraina S, Lacquaniti F, Caminiti R: Parieto-frontal coding of reaching: an integrated framework. Exp Brain Res 1999, 129:325-346. 33. Mascaro M, Battaglia-Mayer A, Nasi L, Amit D, Caminiti R: The eye and the hand: neural mechanisms and network models for oculomanual coordination in parietal cortex. Cereb Cortex 2003, 13:1276-1286. 34. Hawkins K, Sayegh P, Yan X, Crawford J, Sergio L: Neural activity in superior parietal cortex during rule-based visual-motor transformations. J Cogn Neurosci 2013, 25:436-454. 35. Dean H, Hagan M, Pesaran B: Only coherent spiking in posterior parietal cortex coordinates looking and reaching. Neuron 2012, 73:829-841. 36. Engel K, Fries P: Beta oscillations — signalling the status quo? Curr Opin Neurobiol 2010, 20:156-165. 37. Pogosyan A, Gaynor L, Eusebio A, Brown P: Boosting cortical activity at beta-band frequencies slows movement in humans. Curr Biol 2009, 19:1637-1641. 38. Swann N, Tandon N, Canolty R, Ellmore TM, McEvoy LK, Dreyer S, DiSano M, Aron A: Intracranial EEG reveals a time- and frequency-specific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J Neurosci 2009, 29:12675-12685. 39. Dean H, Martı` D, Tsui E, Rinzel J, Pesaran B: Reation time correlations during eye–hand coordination: behavior and modeling. J Neurosci 2011, 31:2399-2412. An interesting model to account for the reaction-time correlation underlying eye–hand coordination. The model predicts that independent, but reciprocally connected hand and eye specific integrators with asymmetric excitation flowing from the hand to the eye integrator (and not vice versa) can predict the psychophysics of coordinated eye–hand movement. The model also implies that the hand integrator resides in SPL, and the saccade integrator in LIP. The assumption of effector specificity does not adhere to the effector-dominance in most SPL and IPL areas emerging from cell recording studies in behaving monkeys. 40. Sayegh P, Hawkins K, Neagu B, Crawford J, Hoffman K, Sergio L: Decoupling the actions of the eyes from the hand alters beta and gamma synchrony within SPL. J Neurophysiol 2014, 111:2210-2221. This study highlights the importance of the relative position of the eye and of the hand in determining neural activity in the monkey SPL, and
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suggests that LFP modulation is a better predictor of task conditions than spiking activity. 41. Yttri E, Liu Y, Snyder L: Lesions of cortical area LIP affect reach onset only when the reach is accompanied by a saccade, revealing an active eye–hand coordination circuit. Proc Natl Acad Sci U S A 2013, 110:2371-2376. 42. Jonikaitis D, Deubel H: Independent allocation of attention to eye and hand targets in coordinated eye–hand movements. Psychol Sci 2011, 22:339-347. 43. Yttri E, Wang C, Liu Y, Snyder L: The parietal reach region is limb specific and not involved in eye–hand coordination. J Neurophysiol 2014, 111:520-532. This study shows unaffected correlation of eye and hand RT during coordinated reaches after reversible inactivation of the so-called PRR and concludes that PRR is not essential for eye–hand coordination. This conclusion is opposite to that held by Hwang et al. [23], who however inactivated a cortical zone which probably correspond to MIP, therefore only one constituent of PRR. Whether PRR is limb-specific and not involved in eye–hand coordination critically depends on the areas that are included under this acronym. If PRR is formed by V6A, PEc and MIP, then it is certainly not limb-specific, but is part of the SPL areas, where neurons combine eye and hand signals with different strength, depending on their antero-posterior location with the parietal gradient. 44. Battaglia-Mayer A, Mascaro M, Brunamonti E, Caminiti R: The over-representation of contralateral space in parietal cortex: a positive image of directional motor components of neglect? Cereb Cortex 2005, 15:514-525. 45. Mountcastle V, Lynch J, Georgopoulos A, Sakata H, Acuna C: Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 1975, 38:871-908. 46. Schall J: Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: comparison with supplementary eye fields. J Neurophysiol 1991, 66:559-579. 47. Gail A, Klaes C, Westendorff S: Implementation of spatial transformation rules for goal-directed reaching via gain modulation in monkey parietal and premotor cortex. J Neurosci 2009, 29:9490-9499. 48. Borra E, Gerbella M, Rozzi S, Tonelli S, Luppino G: Projections to the superior colliculus from inferior parietal, ventral premotor, and ventrolateral prefrontal areas involved in controlling goaldirected hand actions in the macaque. Cereb Cortex 2014, 24:1054-1065. An elegant anatomical study showing that cortical areas involved in the control of hand action within the ‘lateral grasping network’ all project in a consistent fashion to the intermediate and deep layers of the ipsilateral SC and underlying reticular formation. Projections are more abundant in the SC regions related saccade, arm, and hand movement. These results are coherent with the conceptual frame for eye–hand coordination offered in the present review, which assigns to descending motor pathways a role in the final shaping of eye–hand coordination (see also Ref. [49]). 49. Reyes-Puerta V, Philipp R, Lindner W, Hoffmann K: Neuronal activity in the superior colliculus related to saccade initiation during coordinated gaze-reach movements. Eur J Neurosci 2011, 34:1966-1982.
Current Opinion in Neurobiology 2015, 33:103–109
ScienceDirect Timing and communication of parietal cortex for visuomotor control Alexandra Battaglia-Mayer, Simone Ferrari-Toniolo and Federica Visco-Comandini In both monkeys and humans, motor cognition emerges from a parietal–frontal network containing discrete dominant domains of visual, eye and hand signals, where neurons are responsible for goal and effector selection. Within these domains, the combination of different inputs shape the tuning properties of neurons, while local and long cortico-cortical connections outline the architecture of the distributed network and determine the conduction time underlying eye–hand coordination, necessary for visually guided operations in the action space. The analysis of the communication timing between parietal and frontal nodes of the network helps understanding the sensorimotor cortical delays associated to different functions, such as online control of movement and eye–hand coordination, and opens a new perspective to the study of the parieto-frontal interactions. Address Department of Physiology and Pharmacology, SAPIENZA University of Rome, P.le Aldo Moro 5, 00185 Rome, Italy Corresponding author: Battaglia-Mayer, Alexandra ([email protected])
system (PFS) these operations depend on communication between areas. New perspectives on PFS dynamics have been opened by recent studies on the conduction time of messages from PPC to different target areas. By combining information about axon diameter, therefore speed, with axon length, parietal conduction delays to different structures were estimated [1]. The conduction delay of Superior Parietal Lobule (SPL) area PEc to dorsal premotor cortex (PMd) is of about 3.3 ms, to anterior cingulate motor area (CMAd) is 3.5 ms, to motor cortex is only 1.9 ms (Figure 1). The delay to the corpus callosum is about 3 ms [2]. Furthermore, the projection of area PEc to PMd consists of axons of different diameters, as for the other parietal projections, which implies that inter-areal communication is based on temporally dispersed conduction delays. This mechanism has the potential of modulating the oscillatory regimes [3] of the cortex, thus influencing the inter-areal synchrony, which has been proposed, among others, as a potential mechanism of cortical communication during motor planning and execution, when information transfer can take the form of traveling, high-frequency waves [4].
Current Opinion in Neurobiology 2015, 33:103–109 This review comes from a themed issue on Motor circuits and action Edited by Ole Kiehn and Mark Churchland
http://dx.doi.org/10.1016/j.conb.2015.03.005 0959-4388/# 2015 Published by Elsevier Ltd.
Introduction The functional organization and connectivity of posterior parietal cortex (PPC) in monkeys provide a background to explore the neural basis of motor cognition and stays at the core of daily functions, such as eye–hand coordination and online control of hand movement. A new perspective on these functions and on parieto-frontal dynamics is offered by the study of the conduction delays of parietal and frontal areas to their targets and by the putative mechanisms whereby these areas reciprocally interact for motor control.
Timing of cortical communication Motor behavior is framed by the processing time required whenever a change of state occurs. In the parieto-frontal www.sciencedirect.com
Communication based on temporally dispersed delays can also multiply at the target area the number of local neuronal pools on which reciprocal parieto-frontal signaling can operate, potentially allowing a simultaneous representation of sensorimotor signals within multiple reference frame by different pools of neurons. Cell belonging to each pool can be identified and selected by a common timing of arrival of action potential at synaptic level, in other words by the temporal feature of their input. In such a way, different reference frames for eye– hand action can be simultaneously represented beyond the single cell level [5]. The overall result could be an increase of the computational power of parieto-frontal processing streams. This mechanism can also favor the representation of different rule-based motor goals [6] or reaching decisions [7] within parietal and frontal areas. By fractionating the time of arrival of action potentials on the target structures through a wide spectrum of conduction delays, any given cortical area can scale the phase and strength of connections with their targets, by modulating the timing of activation of its neurons. As an example, the effective connection strength between areas can be increased, if the timing of firing of cortical projecting neurons with small axon diameter, therefore slow conduction velocity, leads the activation of neurons with large axon Current Opinion in Neurobiology 2015, 33:103–109
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transmission and decision delays, thus generating psychological refractory periods, as when two sensory signals are presented in sequence [13] in double-step tasks. Fast parieto-frontal signaling is required for on line control of action and for eye–hand coordination underlying reaching. We will briefly discuss recent studies on these issues.
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Conduction delays (ms) of projections from parietal area PEc to frontal areas and corpus callosum. Arrow thickness is inversely proportional to conduction delay (red numbers). Drawn on the basis of results from Refs. [1,2,3].
diameter and faster conduction velocity. Studies of the temporal dynamics of parieto-frontal interactions indicates that while parietal and premotor cortex oscillate in-phase in the beta band (15–30 Hz), partial spike-field coherence in parietal cortex is asynchronous with oscillations in premotor cortex during periods of attentive fixation and motor planning [8], probably down-modulating parieto-frontal communication. Using a population partial spike-field coherence approach to study temporal interactions between parietal areas 2/5 and motor cortex (MI), only a weak parietal influence was found on MI during reach planning, but a strong one during reach movement [9], with parietal cortex influencing encoding of movement direction in primary motor cortex. In the information transfer between somatosensory (SI), motor, and PPC, SI seems to be a major source of information flow in the beta band concerning feed-back signals necessary for continuous estimate of limb parameters [10,11]. The timing of communication between brain areas impacts on different functions. For instance, the nature of the transformation required during motor planning can shape the time-sequence of activation of frontal and parietal areas [12]. A bottleneck may arise when adding Current Opinion in Neurobiology 2015, 33:103–109
Encoding multiple movement parameters and combination of visual, eye and hand information by individual cells stay at the core of parietal online control of reach trajectory, such as when a target suddenly moves to a new location in space. After the pioneering study by Georgopoulos’s group (1983) in MI [14], this subject has been revitalized by recent analysis [15,16] of SPL areas PE/ PEc, as well as of PMd and M1 in monkeys. During reach correction, besides movement direction and instantaneous arm position in space, parietal activity specifies and reflects hand velocity in a way that accurately predicts (‘neural trajectories’) the hand trajectory correction. No special classes of parietal cells are recruited in this process by the change in target location, which instead is encoded through a graded utilization of the kinematics variables encoded by parietal neurons. The same applies to PMd and M1, suggesting that a common mechanism underlies trajectory formation and correction in the cerebral cortex [17]. Within this network, premotor cortex first provides the higher-order signal about the change of target location, thus calling for the specification of a new reach goal. This is in line with the consequences of its lesion in humans, which delays reach onset, but not impair reach accuracy [18], and with its role in tasks requiring switching of motor plans [19]. Thanks to the fine-grain specification of hand kinematics both before and during the hand movement toward first or second target location, SPL areas can provide both the early transformation necessary to specify the reach goal, as well as a continuous estimate of limb position, speed and movement direction. Motor cortex, thanks to the strong relations with arm movement parameters and the direct projections to the spinal cord is involved in the final composition of the reach movement. The causal role of areas PE/PEc in the online control is shown by their reversible bilateral inactivation [20], which results in the impaired online control of hand trajectory (for a review see [17]), as also observed in patients with optic ataxia (OA). The deficit in trajectory correction is in part dependent on a delayed saccade to the second target location, which is coherent with the combined influence of eye–hand signals on SPL neural activity, as well as with the eye movement disorders of OA patients [21]. No clear pattern of eye RT alteration was observed in the inactivation study of the Parietal Reach Region (PRR) [23], where however only the consequence of unilateral parietal silencing has been explored. In the same study, a deficit in saccade amplitude was instead found, when eye and hand moved www.sciencedirect.com
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concurrently, contrary to the unimpaired saccades when the eye moved alone [22,23]. When studying PPC physiology the relative eye and hand position, imposed by the task demands, is a crucial parameter that deserves a particular attention. In this context, the importance of the degree of eye–hand coupling is highlighted by a case report [24] (Figure 2a) of a parietal patient showing a severe impairment in the specification of the direction of the hand force applied to an isometric manipulandum, necessary to move a cursor to visual targets. This impairment indicates that: first, OA generalizes to isometric conditions, that is to visuomotor transformations leading to action in absence of movement, regardless of the imposed physical relationship between the manipulandum and cursor; second, PPC is involved not only in the specification of kinematics [15,25], but also in that of higher-order dynamics underlying hand action. This defective control occurred both in peripheral and central vision. In the latter, eye and hand position were still decoupled, because of the task-imposed dissociation between the position of the visual target on the monitor and the manipulandum (Figure 2b). Therefore PPC seems to contain an abstract representation of the directional motor output, where the computation of the relative position of the hand and of the eye plays a crucial role, as originally implicated by the preferred directions clustering of eye and hand signals within the global tuning fields (GTF ; Figure 2c) [26] of neurons in areas V6A and PEc, and by the observation that in PPC the strongest modulation occurs when the hand moves toward the fixation point [27], thus nulling the ‘eye– hand motor error’. This brings us to the second topic, that is eye–hand coordination.
PPC and eye–hand coordination during reaching A role of PPC in eye–hand coordination is supported by older observations [28–32] that: first, in most parietal areas of the monkey brain, individual neurons combine directional eye and hand signals, although with different dominance; second, the dynamic properties of individual cells [26] and local inhibition [33] give rise to GTF, thanks to which SPL areas can encode spatially co-ordinated eye– hand actions [26]; third, an effector-independent ‘temporal clock’ signaling both target presentation and movement onset exists in both SPL and IPL areas [27]. In SPL, reaching activity is higher and leads in time that of IPL [27,34]. In the latter, population activity is stronger for coordinated eye–hand movement rather than for independent ones. In IPL areas Opt, PG (7a), the large majority of cells is of eye–hand combinatorial type, and displays greater activity when the hand moves toward the fixation point. The neural peak observed for coordinated eye–hand or independent eye or hand movement disappears during no-go tasks [27]. www.sciencedirect.com
The interest in eye–hand coordination has resurged in recent years. Neural activity in the lateral intraparietal area (LIP) and in PRR was studied [35] while monkeys made reaches or saccades to memorized targets. In both areas, local field potentials (LFP) power in the beta band correlates with saccadic RT only during coordinated reaches, implying that decreasing the power in this band could speed movement onset. This is in line with previous studies of the motor system (see [36] for a review), showing that entrainment of MI to a 20 Hz-rhythm during a visuomotor task enhances cortico-muscle beta band coherence and slows voluntary action [37]. Furthermore successful stopping in a Go/No-Go task is related to enhanced beta band activity in the inferior frontal cortex [38]. In LIP, cells with spiking coherent with beta band LFP activity predicts the reach RTs for coordinated eye and hand movements, not of saccades when the eyes move alone. This study points toward a model based on a shared LIP–PRR representation as the basis of eye– hand coordination, on the assumption of a mutual excitation between these regions [35,39], considered as independent effector-specific integrators. In SPL areas PEc and MIP, beta synchrony of LFPs dominates the early planning of coordinated eye–hand movement, and its onset is delayed when decoupling the eye from hand action [40]. Inactivation studies have generated different views on the causal role of parietal areas on eye–hand coordination. Unilateral inactivation of LIP during memory-guided saccades or coordinated reaches, resulted in delayed eye and hand RTs of coordinated reaches, unaffected temporal eye–hand coupling, increase in saccade errors, but not in reach endpoint errors, with hand RT unaffected for reaches without a concurrent saccade [41]. Also based on the evidence of different attention systems for eye and hand movement [42] the authors concluded that LIP does not play a crucial role in eye–hand coordination, but rather in saccade planning and related-attention. A more recent study from the same group showed that unilateral muscimol injections in a sector of the medial bank of the IPS, referred to as PRR [43], produced only a specific increase of RT and decrease of movement speed of the contralateral limb, leaving unaffected not only saccade RT, but also the temporal correlation between eye and hand movement. These results were congruent with PRR viewed as a motoric region, with eye–hand coordination occurring later in the eye-control and handcontrol pathways. In our previous study [20], bilateral lesion of area PE/PEc produced a significant elongation of hand RT, that was only in part explained by the concomitant increase of eye RTs, an increase of movement time duration, and no effect on the correlation between eye and hand RTs. The conclusion that PRR does not play a causal role in eye–hand coordination was however contended by a subsequent unilateral PRR inactivation study [23], reporting a decrease in temporal eye and hand RT Current Opinion in Neurobiology 2015, 33:103–109
106 Motor circuits and action
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Visuomotor impairments after parietal lesion and the role of eye–hand coupling. (a) A parietal patient exerted force in different directions on an isometric joy-stick, as to move a visual cursor to different lighted targets on a screen. The dispersion of cursor’s endpoints (black dots), resulting from force output of ipsilesional and contralesional hand toward targets (red dots) in central or peripheral vision, are presented as 95% confidence ellipses, together with data from a control subject. The black segment within each ellipse indicates the constant error, that is the distance of the mean cursor endpoint (red cross) from the target in each direction. (b) Patient’s absolute errors observed during natural reaching and in the isometric task for both foveal and extrafoveal targets. Below each bar, a schematic representation of the final, relative position of eye, hand and target (gray circle) is shown for each task condition. The cross indicates the fixation point, when required to maintain eye fixation during the task. The eye motor error (ETg), hand motor error (HTg), and their relative difference (HETg) are shown for each task condition, together with a schematic general representation of their definition on the right of the bar graph. Modified from [24]. (c) Example of global tuning field (GTF) of a parietal neuron, where the preferred directions (PDs) during separated or coordinated eye and hand movements cluster within a restricted part of the work-space, thus allowing combination of eye and hand signals in a spatially congruent directional domain. Arrows indicate PDs in different epochs (hRT/eRT, hand/eye reaction time; hMT/eMT, hand/eye movement time; eTHT, eye target holding time) of different tasks (coordinated eye– hand reaching, blue; reaching without concomitant saccades, green; saccade only, red. Modified from [29]).
correlation during reaches, although for only one out of six targets. In spite of this, the authors assigned to PRR an essential role in establishing a tight temporal coupling between the two effectors. Current Opinion in Neurobiology 2015, 33:103–109
The discrepancies of these results can be due to differences of injection sites and in the definition of the functional areas that belongs to the so-called PRR, which differs across studies of the same authors that have www.sciencedirect.com
Parietal cortex and voluntary movement Battaglia-Mayer, Ferrari-Toniolo and Visco-Comandini 107
actually introduced this terminology. More important, another large set of reach-related parietal areas, such as PE, PEa and PGm (7m) in SPL, and 7a in IPL [27,44,45] are influenced by both eye and hand signals. These areas are not included in PRR. This limits the comprehension of the functional role of PPC, within the more extended network for reach control. As a matter of fact, all the above mentioned inactivation studies silenced only a small region of SPL, including the study of Battaglia-Mayer et al. [20], where a consistent impairment was found only after bilateral inactivation of areas PE/PEc. A second problem is that the studies by Andersen, Snyder and Pesaran’s teams [22,35,43], while recognizing the presence of saccade-related activity in PRR, all consider it as a hand-specific module which plays no causal role in saccade generation. Although a causal role of this region in saccade planning remains to be shown, there is unequivocal evidence that all the areas that are part of it (whatever defined), such as V6A, PEc, MIP, combine eye and hand signals with different strength, depending on their position within the parieto-frontal gradient, as also occurs in areas PEa, PGm and in others IPL areas, such as Opt and PG [31,44], thus providing a necessary neural substrate for eye–hand coordination. These areas are therefore to be regarded as effector-dominant, not effector-specific, and their role will have to carefully evaluated within the PFS for a full comprehension of cortical encoding of reaching, which cannot be merely based on PPR operations. A potential way to reconcile different views is provided by the observation that in the longitudinal axis of PPC, including both SPL and IPL, parietal neurons combines eye and hand signals in a task-dependent fashion. To specify a reach goal, in the posterior (areas V6A, PGm) and intermediate (PEc, MIP) SPL areas, of which PRR is one part, a selection process will first recruit neural populations responsible for the composition of the command for reaching. Corollary and re-entrant signaling operated through reciprocal excitatory SPL–IPL connections can recruit in IPL pre-saccadic cells (mostly in LIP), as to shape an ad hoc oculomotor command and provide information about saccade onset. An early eye–hand temporal coupling could be achieved at this stage, together with relative attention allocation. The ipsilateral cortical projections of the SPL to PMd and MI, and of the IPL to the FEF, respectively, will be the final cortical stage for the composition of parallel motor commands for the eye and the hand. The presence of distinguishable visuospatial and motor peaks signaling target localization and movement onset in both FEF [46] and M1 [28] support this view. The involvement of PMd in this process is of interest also in the light of its potential role in breaking the natural eye–hand coupling, or changing reach trajectory [15,16,47], whenever required. The final temporal locking between eye and hand information could be achieved in the superior colliculus (SC), which in addition to the projections from IPL and FEF, is also target of projections from the ‘lateral www.sciencedirect.com
grasping network’ [48]. If similar projections also arise from the SPL areas, as it is reasonable to assume by the presence of reach-related neurons in the SC [49], a combined cortical input from both SPL and IPL could temporally lock eye and hand movement, thus shaping the temporal activation profile of reach neurons in the SC and underlying reticular formation [49]. At the motor output level, cortico-spinal and reticulo-spinal projections on spinal interneurons will convey hand information already temporally locked to the eye, also thanks to the projection from SC to the saccade generators of the midbrain and pons. This would strengthen the importance of these structures in the subcortical control of eye–hand coordination and reconcile, to some extent, conflicting results of the literature on neural basis of eye–hand coordination. In the PFS, the selection and recruitment of specific areas, among the many combining eye–hand signals, will depend on the task and on the transformation rules imposed by each specific remapping process.
Conclusions Different sources of information in the last years stress that the motor functions of PPC are organized along a visuomotor parietal gradient. Thanks to a broad range of cortico-cortical conduction delays, PPC can modulate the oscillatory regimes of the PFS, influencing the inter-areal synchrony that seems important for motor planning and execution. New evidence on the consequences of parietal lesion on isometric actions, that is, in absence of movement, such as when playing a video-game or moving a robot arm in an industrial setting or in a surgical theatre, confirms the causal role of PPC in motor control, particularly when gaze and hand goals are decoupled. The computation of the spatial congruency of eye–hand directional signals seems to occur in the SPL, which however does not seem to play a causal role in the temporal coupling of eye–hand coordination, although so far inactivation studies have only involved a small sector of it. This coupling probably requires the participation of other areas of the PFS and/or is achieved subcortically, in the SC and underlying reticular formation.
Conflict of interest statement Nothing declared.
Acknowledgement This study was supported by the MIUR of Italy (Grant no. 2010XPMFW4_004 to ABM).
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1.
Innocenti G, Vercelli A, Caminiti R: The diameter of cortical axons depends both on the area of origin and target. Cereb Cortex 2014, 24:2178-2188. Current Opinion in Neurobiology 2015, 33:103–109
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This study uses light and electron microscopy in monkeys to characterize the diameter, therefore the speed, and the length of parietal axons terminating in different frontal areas, thus allowing the estimation of parieto-frontal conduction delays.
15. Archambault P, Caminiti R, Battaglia-Mayer A: Cortical mechanisms for online control of hand movement trajectory: the role of the posterior parietal cortex. Cereb Cortex 2009, 19:2848-2864.
2.
16. Archambault P, Ferrari-Toniolo S, Battaglia-Mayer A: Online control of hand trajectory and evolution of motor intention in the parietofrontal system. J Neurosci 2011, 31:742-752.
Caminiti R, Carducci F, Piervincenzi C, Battaglia-Mayer A, Confalone G, Visco-Comandini F, Pantano P, Innocenti G: Diameter, length, speed, and conduction delay of callosal axons in macaque monkeys and humans: comparing data from histology and magnetic resonance imaging diffusion tractography. J Neurosci 2013, 33:14501-14511.
3.
Caminiti R, Ghaziri H, Galuske R, Hof P, Innocenti G: Evolution amplified processing with temporally dispersed slow neuronal connectivity in primates. Proc Natl Acad Sci U S A 2009, 106:19551-19556. A seminal study on the conduction delays of cortical efferent systems showing how evolution can modulated the range of oscillatory regimes of the cortex, shape the number of assemblies that cortical connectivity can generate, and modulate at a ms scale the firing rate of cortical neurons. 4.
Rubino D, Robbins K, Hatsopoulos N: Propagating waves mediate information transfer in the motor cortex. Nat Neurosci 2006, 9:1549-1557.
5.
McGuire L, Sabes P: Sensory transformations and the use of multiple reference frames for reach planning. Nat Neurosci 2009, 12:1056-1061.
6.
Klaes C, Westendorff S, Chakrabarti S, Gail A: Choosing goals, not rules: deciding among rule-based action plans. Neuron 2011, 70:536-548.
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Cisek P, Kalaska J: Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 2005, 45:801-814.
8.
Stetson C, Andersen R: The parietal reach region selectively anti-synchronizes with dorsal premotor cortex during planning. J Neurosci 2014, 34:11948-11958. This study shows anti-synchrony in partial spike-LFP correlation in the beta band (15–30 Hz) between parietal and dorsal premotor reach-related areas in monkeys, and hypothesizes that anti-synchrony can decrease the probability that actions potentials originated in parietal cortex activate premotor cortex during attentive fixation and reach planning. The results are interpreted within the frame of the literature suggesting that betaband activity can reduce the interaction between brain structures and can have an inhibitory role on movement initiation.
9.
Menzer D, Rao N, Bondy A, Truccolo W, Donoghue J: Population interactions between parietal and primary motor cortex during reach. J Neurophysiol 2014 http://dx.doi.org/10.1152/ jn.00851.2012. Interactions between parietal and motor cortex in monkeys were studied at the population level, using a novel partial spike-field coherence (PSFC) approach, which shows how the population analysis is more effective in revealing inter-areal interaction than cell-LFP pairing. During movement planning, PSFC revealed a significant parieto-to-frontal coherence in the low frequency power (1–10 Hz) band, and smaller coherence in the beta band (10–40 Hz). Parieto-frontal coherence in the low frequency range significantly increased during arm movement time, and depended on its direction, suggesting that the parietal input determines, at least in part, the directional tuning of motor cortical cells.
10. Zhang Y, Chen Y, Bressler SL, Ding M: Response preparation and inhibitation: the role of the cortical sensorimotor beta rhythm. Neuroscience 2008, 156:238-246. 11. Tsujimoto T, Mima T, Shimazu H, Isomura Y: Directional organization of sensorimotor oscillatory activity related to the elctromyogram in the monkey. Clin Neurophysiol 2009, 120:1168-1173. 12. Westendorff S, Klaes C, Gail A: The cortical timeline for deciding on reach motor goals. J Neurosci 2010, 30:5426-5436. 13. van de Kamp C, Gawthrop P, Gollee H, Loram I: Refractoriness in sustained visuo-manual control: is the refractory duration intrinsic or does it depend on external system properties? PLoS Comput Biol 2013, 9:e1002843. 14. Georgopoulos A, Kalaska J, Caminiti R, Massey J: Interruption of motor cortical discharge subserving aimed arm movements. Exp Brain Res 1983, 4:327-340. Current Opinion in Neurobiology 2015, 33:103–109
17. Battaglia-Mayer A, Buiatti T, Caminiti R, Ferraina S, Lacquaniti F, Shallice T: Correction and suppression of reaching movements in the cerebral cortex: physiological and neuropsychological aspects. Neurosci Biobehav Rev 2014, 42:232-251. 18. Buiatti T, Skrap M, Shallice T: Reaching a moveable visual target: dissociations in brain tumour patients. Brain Cogn 2013, 82:6-17. The larger study-group available in the literature on control of reaching after parietal and frontal lesions in humans, with special emphasis on optic ataxia. 19. Pastor-Bernier A, Tremblay E, Cisek P: Dorsal premotor cortex is involved in switching motor plans. Front Neuroeng 2012 http:// dx.doi.org/10.3389/fneng.2012.00005. 20. Battaglia-Mayer A, Ferrari-Toniolo S, Visco-Comandini F, Archambault P, Saberi-Moghadam S, Caminiti R: Impairment of online control of hand and eye movements in a monkey model of optic ataxia. Cereb Cortex 2012, 23:2644-2656. The first monkey model of the defective online correction of hand movement trajectory that characterizes OA in humans. This study shows that the delayed hand correction after parietal inactivation is in part dependent on delayed saccade toward the target location, as also implied by neuropsychological studies (see Ref. [21]) in humans. Delayed saccades were not observed in the inactivation study by Hwang et al. [23]. 21. Gaveau V, Pe´ lisson D, Blangero A, Urquizar C, Prablanc C, Vighetto A, Pisella L: Saccade control and eye–hand coordination in optic ataxia. Neuropsychologia 2008, 46:475-486. 22. Hwang E, Hauschild M, Wilke M, Andersen R: Inactivation of the parietal reach region causes optic ataxia, impairing reaches but not saccades. Neuron 2012, 76:1021-1029. This study inactivated a SPL region (PRR) which is similar to that inactivated in [20]. In this paper eye movements are studied in a ‘saccade only’ task, and not in the context of coordinated eye–hand movements. No information about timing is given. 23. Hwang JE, Hauschild M, Wilke M, Andersen R: Spatial and temporal eye–hand coordination relies on the Parietal Reach Region. J Neurosci 2014, 34:12884-12892. 24. Ferrari-Toniolo S, Papazachariadis O, Visco-Comandini F, Salvati M, D’Elia A, Di Berardino F, Caminiti R, Battaglia-Mayer A: A visuomotor disorder in the absence of movement: does optic ataxia generalize to learned isometric hand action? Neuropsychologia 2014, 63:59-71. A case report of parietal patients with lesion in the SPL and medial bank of IPS and displaying OA under isometric condition. This is the first case in the literature of a parietal patient suffering from defective control of hand force output. It indicates that the conclusions of the study by HamelPaˆquet et al. [25] need critical re-evaluation and update. 25. Hamel-Paˆquet C, Sergio L, Kalaska J: Parietal area 5 activity does not reflect the differential time-course of motor output kinetics during arm-reaching and isometric-force tasks. J Neurophysiol 2006, 95:3353-3370. 26. Battaglia-Mayer A, Ferraina S, Mitsuda T, Marconi B, Genovesio A, Onorati P, Lacquaniti F, Caminiti R: Early coding of reaching in the parieto occipital cortex. J Neurophysiol 2000, 83:2374-2391. 27. Battaglia-Mayer A, Mascaro M, Caminiti R: Temporal evolution and strength of neural activity in parietal cortex during eye and hand movements. Cereb Cortex 2007, 17:1350-1363. 28. Johnson P, Ferraina S: Cortical networks for visual reaching: intrinsic frontal lobe connectivity. Eur J Neurosci 1996, 8:1358-1362. 29. Battaglia-Mayer A, Ferraina S, Genovesio A, Marconi B, Squatrito S, Molinari M, Lacquaniti F, Caminiti R: Eye–hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex www.sciencedirect.com
Parietal cortex and voluntary movement Battaglia-Mayer, Ferrari-Toniolo and Visco-Comandini 109
and parieto-frontal association projections. Cereb Cortex 2001, 11:528-544. 30. Marconi B, Genovesio A, Battaglia-Mayer A, Ferraina S, Squatrito S, Molinari M, Lacquaniti F, Caminiti R: Eye–hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb Cortex 2001, 11:513-527. 31. Rozzi S, Ferrari P, Bonini L, Rizzolatti G, Fogassi L: Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. Eur J Neurosci 2008, 28:1569-1588. 32. Burnod Y, Baraduc P, Battaglia-Mayer A, Guigon E, Koechlin E, Ferraina S, Lacquaniti F, Caminiti R: Parieto-frontal coding of reaching: an integrated framework. Exp Brain Res 1999, 129:325-346. 33. Mascaro M, Battaglia-Mayer A, Nasi L, Amit D, Caminiti R: The eye and the hand: neural mechanisms and network models for oculomanual coordination in parietal cortex. Cereb Cortex 2003, 13:1276-1286. 34. Hawkins K, Sayegh P, Yan X, Crawford J, Sergio L: Neural activity in superior parietal cortex during rule-based visual-motor transformations. J Cogn Neurosci 2013, 25:436-454. 35. Dean H, Hagan M, Pesaran B: Only coherent spiking in posterior parietal cortex coordinates looking and reaching. Neuron 2012, 73:829-841. 36. Engel K, Fries P: Beta oscillations — signalling the status quo? Curr Opin Neurobiol 2010, 20:156-165. 37. Pogosyan A, Gaynor L, Eusebio A, Brown P: Boosting cortical activity at beta-band frequencies slows movement in humans. Curr Biol 2009, 19:1637-1641. 38. Swann N, Tandon N, Canolty R, Ellmore TM, McEvoy LK, Dreyer S, DiSano M, Aron A: Intracranial EEG reveals a time- and frequency-specific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J Neurosci 2009, 29:12675-12685. 39. Dean H, Martı` D, Tsui E, Rinzel J, Pesaran B: Reation time correlations during eye–hand coordination: behavior and modeling. J Neurosci 2011, 31:2399-2412. An interesting model to account for the reaction-time correlation underlying eye–hand coordination. The model predicts that independent, but reciprocally connected hand and eye specific integrators with asymmetric excitation flowing from the hand to the eye integrator (and not vice versa) can predict the psychophysics of coordinated eye–hand movement. The model also implies that the hand integrator resides in SPL, and the saccade integrator in LIP. The assumption of effector specificity does not adhere to the effector-dominance in most SPL and IPL areas emerging from cell recording studies in behaving monkeys. 40. Sayegh P, Hawkins K, Neagu B, Crawford J, Hoffman K, Sergio L: Decoupling the actions of the eyes from the hand alters beta and gamma synchrony within SPL. J Neurophysiol 2014, 111:2210-2221. This study highlights the importance of the relative position of the eye and of the hand in determining neural activity in the monkey SPL, and
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suggests that LFP modulation is a better predictor of task conditions than spiking activity. 41. Yttri E, Liu Y, Snyder L: Lesions of cortical area LIP affect reach onset only when the reach is accompanied by a saccade, revealing an active eye–hand coordination circuit. Proc Natl Acad Sci U S A 2013, 110:2371-2376. 42. Jonikaitis D, Deubel H: Independent allocation of attention to eye and hand targets in coordinated eye–hand movements. Psychol Sci 2011, 22:339-347. 43. Yttri E, Wang C, Liu Y, Snyder L: The parietal reach region is limb specific and not involved in eye–hand coordination. J Neurophysiol 2014, 111:520-532. This study shows unaffected correlation of eye and hand RT during coordinated reaches after reversible inactivation of the so-called PRR and concludes that PRR is not essential for eye–hand coordination. This conclusion is opposite to that held by Hwang et al. [23], who however inactivated a cortical zone which probably correspond to MIP, therefore only one constituent of PRR. Whether PRR is limb-specific and not involved in eye–hand coordination critically depends on the areas that are included under this acronym. If PRR is formed by V6A, PEc and MIP, then it is certainly not limb-specific, but is part of the SPL areas, where neurons combine eye and hand signals with different strength, depending on their antero-posterior location with the parietal gradient. 44. Battaglia-Mayer A, Mascaro M, Brunamonti E, Caminiti R: The over-representation of contralateral space in parietal cortex: a positive image of directional motor components of neglect? Cereb Cortex 2005, 15:514-525. 45. Mountcastle V, Lynch J, Georgopoulos A, Sakata H, Acuna C: Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 1975, 38:871-908. 46. Schall J: Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: comparison with supplementary eye fields. J Neurophysiol 1991, 66:559-579. 47. Gail A, Klaes C, Westendorff S: Implementation of spatial transformation rules for goal-directed reaching via gain modulation in monkey parietal and premotor cortex. J Neurosci 2009, 29:9490-9499. 48. Borra E, Gerbella M, Rozzi S, Tonelli S, Luppino G: Projections to the superior colliculus from inferior parietal, ventral premotor, and ventrolateral prefrontal areas involved in controlling goaldirected hand actions in the macaque. Cereb Cortex 2014, 24:1054-1065. An elegant anatomical study showing that cortical areas involved in the control of hand action within the ‘lateral grasping network’ all project in a consistent fashion to the intermediate and deep layers of the ipsilateral SC and underlying reticular formation. Projections are more abundant in the SC regions related saccade, arm, and hand movement. These results are coherent with the conceptual frame for eye–hand coordination offered in the present review, which assigns to descending motor pathways a role in the final shaping of eye–hand coordination (see also Ref. [49]). 49. Reyes-Puerta V, Philipp R, Lindner W, Hoffmann K: Neuronal activity in the superior colliculus related to saccade initiation during coordinated gaze-reach movements. Eur J Neurosci 2011, 34:1966-1982.
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