Representing Spatial Information for Limb Movement: Role of Area 5 in the Monkey

“In the monkey, superior parietal lobule and especially its rostral part (area PE) contains neurons that are active in response to proprioceptive stimuli as well as during active arm movements (Kalaska et al. 1983, Lacquaniti et al. 1995, Mountcastle et al. 1975).”

“more generally, movement in space (Mountcastle et al. 1975; Lacquaniti et al. 1995).”

“Neurons of the cortex of the superior parietal lobule code the location of body parts (e.g. the arm) in a body-centred coordinate system (Duffy & Burchfield 1971; Sakata et al. 1973; Mountcastle et al. 1975; Lacquaniti et al. 1995).”

“Several studies have shown that the superior parietal lobule codes the location of body parts in a body-centered coordinate system (e.g. Duffy and Birchfiel, 1971; Sakata et al., 1973; Mountcastle et al., 1975; Lacquaniti et al., 1995).”

“Recently, Lacquaniti et al. (1995) provided evidence that many neurons in area PE encode the location of the arm in space in a body-centered coordinate system.”

“It receives its main cortical input from the primary somatosensory cortices, and in particular from those which code proprioception (see Lacquaniti et al. 1995).”

“There appears instead to be a mechanism that uses proprioceptive information in the generation of an output that reflects, in addition to the information on arm position, target location and other factors.”

“Neurons from area PE, the area forming most of the superior parietal lobule cortical convexity, are active with passive joint rotation and deep tissue pressure as well as during active arm movements (Sakata et al., 1973; Mountcastle et al., 1975; Kalaska et al., 1983; Lacquaniti et al., 1995).”

“Area 5 represents spatial information for limb movement and is involved in reaching arm movements (Lacquaniti et al., 1995; Kalaska et al., 1997).”

“…directly with the occipitoparietal cortical areas that process visuospatial information or the occipitotemporal cortical areas that process visual object information (Ungerleider and Mishkin, 1982) or the parietal areas involved in action in space (Lacquaniti et al., 1995; Gallese et al., 2002).”

“[25] showed elegantly that area 5 cell activity signalled arm postures and movements in a body-centred reference frame.”

“Further studies investigating neuronal activity in areas 5 (PE or PEc), MIP and V6A have hypothesized a role in coding arm movement direction, and in the transformation of sensory input into reference frames that can be used to guide limb action (Kalaska et al., 1983; Ferraina and Bianchi, 1994; Lacquaniti et al., 199…”

“The anterior SPC integrates mainly information from the somatosensory cortex (Pandya and Seltzer 1982) and provides the dorsal premotor cortex (PMd) with a spatial representation of the body parts (Mountcastle et al. 1975; Jones et al. 1978; Lacquaniti et al. 1995).”

“(185) fitted regression models to recordings made while monkeys performed three-dimensional reaching movements in three separate workspaces (81) to test different assumptions about possible coordinate systems.”

“Examples are Georgopoulos et al. (1982, 1986) for an extrinsic-kinematic space, Lacquaniti et al. (1995) for an intrinsic-kinematic space, Scott and Kalaska (1995, 1997), Sergio and Kalaska (1998) for an intrinsic-dynamic-mechanical space, and Keller (1973), Shidara et al. (1993), and Gomi et al.…”

“It was also extended to a large number of cerebral areas including the premotor cortex (45), the parietal cortex (147,162), and the cerebellum (93).”

“4 and 18; Murray and Coulter 1981; Pandya and Seltzer 1982; Shima et al. 1991; Lacquaniti et al. 1995; Morecraft et al. 2004).”

“This anatomical layout of the parietal network is consistent with the hypothesis that reaching in parietal cortex can be coded either in arm-centered (Lacquaniti et al., 1995) or in eyecentered (Lacquaniti et al., 1995; McIntyre et al., 1997, 1998; Batista et al., 1999) coordinates.”

“Second, available evidence (Ferraina and Bianchi, 1994; Lacquaniti et al., 1995) based on studies of arm reaching in three-dimensional space, argues against coding of motor error in areas of the superior parietal lobule comprised within the definition of Parietal Reach Region, and in the frontal areas where they proje…”

“In fact, a similar control strategy has also been proposed for arm reaching (Lacquaniti et al., 1995; Schwartz and Moran, 2000; Roitman et al., 2005).”

“1B, we use a coarse tuning (Lacquaniti et al. 1995).”

“The anterior BA5 has been described as primarily integrating information from the somatosensory cortex and providing the PMd with a spatial representation of the body parts [Jones et al., 1978; Lacquaniti et al., 1995; Mountcastle et al., 1975; Pandya and Seltzer, 1982].”

“…arise from caudodorsal prefrontal cortex (areas 8B and 9/46d) and are directed to premotor, supplementary motor, superior and medial parietal regions, namely areas involved with the control of reaching and, more generally, movement in space (e.g., Mountcastle et al., 1975; Lacquaniti et al., 1995).”

“For example, area 5 encodes arm location in a body-centered coordinate system [29, 30], and its projections to the fundus of the intraparietal sulcus are known [27, 31, 32].”

“Many neurons in dorsal area 5 are best tuned to either the azimuth, elevation, or distance of the endpoint relative to the body (Lacquaniti et al., 1995).”

“The motor commands required to perform such actions depend not only on the kinematics (Lacquaniti et al., 1995) and dynamics (Kalaska et al.”

“Electrophysiological (Andersen et al., 1987; Lacquaniti et al., 1995; MacKay and Mendonca, 1995; Sakata et al., 1985) and lesion studies (Crowne et al., 1992; Petrides and Iversen, 1979; Pu et al., 1993) in the monkey have established a role for posterior parietal cortex in coordinated visuomotor…”

“…studies of monkeys have demonstrated the existence of a functionally specialized, parietofrontal TABLE 4 ) and higher level proprioceptive (Lacquaniti et al., 1995) input from the superior parietal lobule (SPL) and is reciprocally connected with a medial region of the intraparietal sulcus…”

“, 1999) or armcentred (Lacquaniti et al., 1995) coordinates.”

“However, the parietal cortex appears to be involved in visuomotor aspects of manual manipulative movements [1,7,21,20,30,46,53,82,90].”

“…multiunit recordings have been performed in area 5 of macaque monkeys (Mountcastle et al., 1975; Pons et al., 1985; Ferraina and Bianchi, 1994; Lacquaniti et al., 1995; Snyder et al., 1997; Taoka et al., 2000; Debowy et al., 2001) (for review see Kalaska, 1996; Wise et al., 1997; Iwamura,…”

“In contrast, in the case of unseen proprioceptive targets, both the target and effector are initially coded in body-centered space in higher-order somatosensory areas (Lacquaniti et al., 1995).”

“The HOLD activity could code different spatial locations of the hand in the peripersonal space, as suggested for neurons in several cortical regions in the caudal part of the SPL (Ferraina et al., 1997, 2001; Battaglia-Mayer et al., 2000, 2001), or the arm posture, as suggested for neurons of area 5, in a more anterio…”

“1990; Lacquaniti et al., 1995).”

“The directional tuning during the delay period changed idiosyncratically between different cubes, like that seen for movement-related activity during RT tasks (Caminiti et al. 1990, 1991; Lacquaniti et al. 1995).”

“Particularly, SPL may be essential for the maintaining the body schema, as data from monkeys and humans have demonstrated that SPL integrates visual and proprioceptive input about the position of body parts to maintain spatial limb representations (Lacquaniti et al., 1995; Hagura et al., 2007; Seelke et al., 2012).”

“…5 process mainly proprioceptive information to encode arm postures and movements within a body-centered reference frame and project to the primary motor cortex and the caudal part of F2 (Johnson et al., 1996; Lacquaniti et al., 1995) as well as to other parietal areas (Pandya and Seltzer, 1982).”

“Area 5 is known to possess neurons with sensitivity to hand/arm position (Lacquaniti et al. 1995; Kalaska et al. 1997).”

“This area has been implicated in the control of reaching to remembered locations in primates (24, 25) and may play an analogous role in stepping behavior during locomotion.”

“Such a separation is supported by evidence from primates showing response differences for action-observation (Lacquaniti et al., 1995; Mountcastle, 1975) and intent-perception (di Pellegrino et al.”

“1995; Georgopoulos et al. 1982, 1988; Kalaska et al. 1983; The simple spike discharge of 231 cerebellar Purkinje cells in Lacquaniti et al. 1995; Schwartz et al. 1988).”

“…to be a region that generates an internal coordinate system for intentional reaching and grasping into immediate extra personal space (e.g., Ferraina and Bianchi 1994; Lacquaniti et al. 1995; Snyder et al. 1997; see Wise et al. 1997; Debowy et al. 2001; Krubitzer and Disbrow 2008, for review).”

“…region bordering anteriorly V6Ad (including areas PEc and PE) shows these properties (limb movement activity; Sakata et al., 1973 ; Hyvarinen, 1982 ; Lacquaniti et al., 1995 ; Ferraina et al., 2001 ; Breveglieri et al., 2006 ; Bremner and Andersen, 2012 ), so, likely, the green region in Fig.”

“Visual, auditory and tactile information converge in the posterior parietal regions of monkeys where they become systematically combined with proprioceptive and vestibular cues so as to maintain constantly updated multimodal body-centred representations of space (Andersen et al., 1997; Duhamel et al., 1992; Lacquaniti…”

“The inferior parietal lobule (IPL) is an important node in the parietal association cortex and plays a key role in integrating visual, auditory, and somatosensory information to guide movement [Battaglia-Mayer and Caminiti, 2002; Lacquaniti et al., 1995; Marconi et al., 2001].”

“Neurons in the SPL of the monkey take part in the process of visuomotor coordinate transformations by encoding reaching movements in a body-centered frame of reference (Lacquaniti et al., 1995).”

“…its left counterpart (1.68 cm 3 ), in agreement with recent reports (N. Makris et al. 2012; Wang et al. 2012), which may indicate a predominant role of the right STG(MdLF)SPL in visuospatial attention (Duffy and Burchfiel 1971; Lacquaniti et al. 1995; Mountcastle et al. 1975; Sakata et al. 1973).”

“, right middle frontal gyrus in Table 2) with the cingulate (Table 3) and cingulum (Table 5) of the superior and medial parietal cortex [56, 57].”

“…association areas, participate also in the control of visually guided movements (Pandya and Seltzer, 1982; McGuire et al., 1989) and, in particular, area PE is involved in egocentric representation of reaching in monkeys (Acuna et al., 1990; for review, see Lacquaniti et al., 1995; Kalaska, 1996).”

“…shoulder-centered , and hand-centered reference frames in premotor and parietal areas (Battaglia-Mayer et al. 2000, 2001; Buneo et al. 2002; Lacquaniti et al. 1995), whether these representation play different roles in different tasks or during the course of learning has not been resolved.”

“…other parameters about the movement, such as initial hand position and movement vector, although the extent of these effects and their representations are a matter of ongoing debate (Lacquaniti et al., 1995; Buneo et al., 2002; Chang et al., 2009; Ferraina et al., 2009; Chang and Snyder, 2010).”