Top

Published in:

01-05-2018 | Original Article

Sensory properties of the caudal aspect of the macaque’s superior parietal lobule

Authors: Michela Gamberini, Giulia Dal Bò, Rossella Breveglieri, Sofia Briganti, Lauretta Passarelli, Patrizia Fattori, Claudio Galletti

Published in: Brain Structure and Function | Issue 4/2018

Abstract

In the superior parietal lobule (SPL), the anterior part (area PE) is known to process somatosensory information, while the caudalmost part (areas V6Av and V6) processes visual information. Here we studied the visual and somatosensory properties of the areas PEc and V6Ad located in between the somatosensory and visual domains of SPL. About 1500 neurons were extracellularly recorded in 19 hemispheres of 12 monkeys (Macaca fascicularis). Visual and somatosensory properties of single neurons were generally studied separately, while in a subpopulation of neurons, both the sensory properties were tested. Visual neurons were more represented in V6Ad and somatosensory neurons in PEc. The visual neurons of these two areas showed similar properties and represented a large part of the contralateral visual field, mostly the lower part. In contrast, somatosensory neurons showed remarkable differences. The arms were overrepresented in both the areas, but V6Ad represented only the upper limbs, whereas PEc both the upper and lower limbs. Interestingly, we found that in both the areas, bimodal visual–somatosensory cells represented the proximal part of the arms. We suggest that PEc is involved in locomotion and in the control of hand/foot interaction with the objects of the environment, while V6Ad is in the control of the object prehension specifically performed with the upper limbs. Neuroimaging and lesion studies from literature support a strict homology with humans.

Abdollahi RO, Jastorff J, Orban GA (2013) Common and segregated processing of observed actions in human SPL. Cereb cortex 23:2734–2753. https://doi.org/10.1093/cercor/bhs264 CrossRefPubMed

Bakola S, Gamberini M, Passarelli L et al (2010) Cortical connections of parietal field PEc in the macaque: linking vision and somatic sensation for the control of limb action. Cereb Cortex 20:2592–2604. https://doi.org/10.1093/cercor/bhq007 CrossRefPubMed

Battaglia-Mayer A, Ferraina S, Genovesio A et al (2001) Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections. Cereb Cortex 11:528–544CrossRefPubMed

Battaglini PP, Muzur A, Galletti C et al (2002) Effects of lesions to area V6A in monkeys. Exp Brain Res 144:419–422. https://doi.org/10.1007/s00221-002-1099-4 CrossRefPubMed

Bosco A, Breveglieri R, Hadjidimitrakis K et al (2016) Reference frames for reaching when decoupling eye and target position in depth and direction. Sci Rep 6:21646. https://doi.org/10.1038/srep21646 CrossRefPubMedPubMedCentral

Bremner LR, Andersen RA (2012) Coding of the reach vector in parietal area 5d. Neuron 75:342–351. https://doi.org/10.1016/j.neuron.2012.03.041 CrossRefPubMedPubMedCentral

Breveglieri R, Kutz D, Fattori P et al (2002) Somatosensory cells in the parieto-occipital area V6A of the macaque. Neuroreport 13:2113–2116. https://doi.org/10.1097/00001756-200211150-00024 CrossRefPubMed

Breveglieri R, Galletti C, Gamberini M et al (2006) Somatosensory cells in area PEc of macaque posterior parietal cortex. J Neurosci 26:3679–3684. https://doi.org/10.1523/JNEUROSCI.4637-05.2006 CrossRefPubMed

Breveglieri R, Galletti C, Monaco S, Fattori P (2008) Visual, somatosensory, and bimodal activities in the macaque parietal area PEc. Cereb Cortex 18:806–816. https://doi.org/10.1093/cercor/bhm127 CrossRefPubMed

Breveglieri R, Hadjidimitrakis K, Bosco A et al (2012) Eye position encoding in three-dimensional space: integration of version and vergence signals in the medial posterior parietal cortex. J Neurosci 32:159–169. https://doi.org/10.1523/JNEUROSCI.4028-11.2012 CrossRefPubMed

Breveglieri R, Galletti C, Bosco A et al (2015) Object affordance modulates visual responses in the macaque medial posterior parietal cortex. J Cogn Neurosci 27:1447–1455CrossRefPubMed

Breveglieri R, Bosco A, Galletti C et al (2016) Neural activity in the medial parietal area V6A while grasping with or without visual feedback. Sci Rep 6:28893. https://doi.org/10.1038/srep28893 CrossRefPubMedPubMedCentral

Breveglieri R, De Vitis M, Bosco A et al (2017) Interplay between grip and vision in the monkey medial parietal lobe. Cereb Cortex 1–15. https://doi.org/10.1093/cercor/bhx109

Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues

Caminiti R, Borra E, Visco-Comandini F et al (2017) Computational architecture of the parieto-frontal network underlying cognitive-motor control in monkeys. eNeuro 4:ENEURO.0306–16. https://doi.org/10.1523/ENEURO.0306-16.2017 CrossRef

Cavina-Pratesi C, Monaco S, Fattori P et al (2010) Functional magnetic resonance imaging reveals the neural substrates of arm transport and grip formation in reach-to-grasp actions in humans. J Neurosci 30:10306–10323. https://doi.org/10.1523/JNEUROSCI.2023-10.2010 CrossRefPubMed

Chang SWC, Papadimitriou C, Snyder LH (2009) Using a compound gain field to compute a reach plan. Neuron 64:744–755. https://doi.org/10.1016/j.neuron.2009.11.005 CrossRefPubMedPubMedCentral

Colby CL, Duhamel JR (1996) Spatial representations for action in parietal cortex. Cogn Brain Res 5:105–115. https://doi.org/10.1016/S0926-6410(96)00046-8 CrossRef

Colby CL, Duhamel JR, Goldberg ME (1993) Ventral intraparietal area of the macaque: anatomic location and visual response properties. J Neurophysiol 69:902–914CrossRefPubMed

Fattori P, Gamberini M, Kutz DF, Galletti C (2001) ‘Arm-reaching’ neurons in the parietal area V6A of the macaque monkey. Eur J Neurosci 13:2309–2313. https://doi.org/10.1046/j.0953-816X.2001.01618.x CrossRefPubMed

Fattori P, Breveglieri R, Amoroso K, Galletti C (2004) Evidence for both reaching and grasping activity in the medial parieto-occipital cortex of the macaque. Eur J Neurosci 20:2457–2466. https://doi.org/10.1111/j.1460-9568.2004.03697.x CrossRefPubMed

Fattori P, Kutz DF, Breveglieri R et al (2005) Spatial tuning of reaching activity in the medial parieto-occipital cortex (area V6A) of macaque monkey. Eur J Neurosci 22:956–972. https://doi.org/10.1111/j.1460-9568.2005.04288.x CrossRefPubMed

Fattori P, Breveglieri R, Marzocchi N et al (2009) Hand orientation during reach-to-grasp movements modulates neuronal activity in the medial posterior parietal area V6A. J Neurosci 29:1928–1936. https://doi.org/10.1523/JNEUROSCI.4998-08.2009 CrossRefPubMed

Fattori P, Raos V, Breveglieri RRR et al (2010) The dorsomedial pathway is not just for reaching: grasping neurons in the medial parieto-occipital cortex of the macaque monkey. J Neurosci 30:342–349. https://doi.org/10.1523/JNEUROSCI.3800-09.2010 CrossRefPubMed

Fattori P, Breveglieri R, Raos V et al (2012) Vision for action in the macaque medial posterior parietal cortex. J Neurosci 32:3221–3234. https://doi.org/10.1523/JNEUROSCI.5358-11.2012 CrossRefPubMed

Fattori P, Breveglieri R, Bosco A et al (2017) Vision for prehension in the medial parietal cortex. Cereb Cortex 27:1149–1163. https://doi.org/10.1093/cercor/bhv302 PubMed

Ferraina S, Garasto MR, Battaglia-Mayer A et al (1997) Visual control of hand-reaching movement: activity in parietal area 7 m. Eur J Neurosci 9:1090–1095. https://doi.org/10.1111/j.1460-9568.1997.tb01460.x CrossRefPubMed

Ferraina S, Battaglia-Mayer A, Genovesio A et al (2001) Early coding of visuomanual coordination during reaching in parietal area PEc. J Neurophysiol 85:462–467CrossRefPubMed

Filippini M, Breveglieri R, Akhras MA et al (2017) Decoding information for grasping from the macaque dorsomedial visual stream. J Neurosci 37:4311–4322. https://doi.org/10.1523/JNEUROSCI.3077-16.2017 CrossRefPubMed

Gail A, Klaes C, Westendorff S (2009) Implementation of spatial transformation rules for goal-directed reaching via gain modulation in monkey parietal and premotor cortex. J Neurosci 29:9490–9499. https://doi.org/10.1523/JNEUROSCI.1095-09.2009 CrossRefPubMed

Galati G, Committeri G, Pitzalis S et al (2011) Intentional signals during saccadic and reaching delays in the human posterior parietal cortex. Eur J Neurosci 34:1871–1885. https://doi.org/10.1111/j.1460-9568.2011.07885.x CrossRefPubMed

Galletti C, Fattori P (2017) The dorsal visual stream revisited: stable circuits or dynamic pathways? Cortex. https://doi.org/10.1016/j.cortex.2017.01.009 PubMed

Galletti C, Battaglini PP, Fattori P (1993) Parietal neurons encoding spatial locations in craniotopic coordinates. Exp Brain Res 96:221–229. https://doi.org/10.1007/BF00227102 CrossRefPubMed

Galletti C, Battaglini P, Fattori P (1995) Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur J Neurosci 7:2486–2501CrossRefPubMed

Galletti C, Fattori P, Shipp S, Zeki S (1996) Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur J Neurosci 8:30–52CrossRefPubMed

Galletti C, Fattori P, Gamberini M, Kutz DF (1999a) The cortical visual area V6: brain location and visual topography. Eur J Neurosci 11:3922–3936CrossRefPubMed

Galletti C, Fattori P, Kutz DF, Gamberini M (1999b) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neurosci 11:575–582. https://doi.org/10.1046/j.1460-9568.1999.00817.x CrossRefPubMed

Galletti C, Kutz DF, Gamberini M et al (2003) Role of the medial parieto-occipital cortex in the control of reaching and grasping movements. Exp Brain Res 153:158–170. https://doi.org/10.1007/s00221-003-1589-z CrossRefPubMed

Gamberini M, Passarelli L, Fattori P et al (2009) Cortical connections of the visuomotor parietooccipital area V6Ad of the macaque monkey. J Comp Neurol 513:622–642. https://doi.org/10.1002/cne.21980 CrossRefPubMed

Gamberini M, Galletti C, Bosco A et al (2011) Is the medial posterior parietal area V6A a single functional area? J Neurosci 31:5145–5157. https://doi.org/10.1523/JNEUROSCI.5489-10.2011 CrossRefPubMed

Gamberini M, Fattori P, Galletti C (2015) The medial parietal occipital areas in the macaque monkey. Vis Neurosci 32:E013. https://doi.org/10.1017/S0952523815000103 CrossRefPubMed

Gardner EP (2017) Neural pathways for cognitive command and control of hand movements. Proc Natl Acad Sci USA 114:4048–4050. https://doi.org/10.1073/pnas.1702746114 CrossRefPubMedPubMedCentral

Hadjidimitrakis K, Breveglieri R, Placenti G et al (2011) Fix your eyes in the space you could reach: neurons in the macaque medial parietal cortex prefer gaze positions in peripersonal space. PLoS One 6:e23335. https://doi.org/10.1371/journal.pone.0023335 CrossRefPubMedPubMedCentral

Hadjidimitrakis K, Bertozzi F, Breveglieri R et al (2014) Common neural substrate for processing depth and direction signals for reaching in the monkey medial posterior parietal cortex. Cereb Cortex 24:1645–1657. https://doi.org/10.1093/cercor/bht021 CrossRefPubMed

Hadjidimitrakis K, Dal Bo’ G, Breveglieri R et al (2015) Overlapping representations for reach depth and direction in caudal superior parietal lobule of macaques. J Neurophysiol 114:2340–2352. https://doi.org/10.1152/jn.00486.2015 CrossRefPubMedPubMedCentral

Huang R-S, Chen C-F, Tran AT et al (2012) Mapping multisensory parietal face and body areas in humans. PNAS 109:18114–18119. https://doi.org/10.1073/pnas.1207946109 CrossRefPubMedPubMedCentral

Hwang EJ, Hauschild M, Wilke M, Andersen RA (2014) Spatial and temporal eye-hand coordination relies on the parietal reach region. J Neurosci 34:12884–12892. https://doi.org/10.1523/JNEUROSCI.3719-13.2014 CrossRefPubMedPubMedCentral

Jakobson LS, Archibald YM, Carey DP, Goodale MA (1991) A kinematic analysis of reaching and grasping movements in a patient recovering from optic ataxia. Neuropsychologia 29:803–809. https://doi.org/10.1016/0028-3932(91)90073-H CrossRefPubMed

Jeannerod M (1986) Mechanisms of visuomotor coordination: a study in normal and brain-damaged subjects. Neuropsychologia 24:41–78. https://doi.org/10.1016/0028-3932(86)90042-4 CrossRefPubMed

Kaas JH (1983) What, if anything, is SI? Organization of first somatosensory area of cortex. Physiol Rev 63:206–231CrossRefPubMed

Kalaska JF, Scott SH, Cisek P, Sergio LE (1997) Cortical control of reaching movements. Curr Opin Neurobiol 7:849–859. https://doi.org/10.1016/S0959-4388(97)80146-8 CrossRefPubMed

Kase CS, Troncoso JF, Court JE et al (1977) Global spatial disorientation. Clinico-pathologic correlations. J Neurol Sci 34:267–278CrossRefPubMed

Kutz DF, Fattori P, Gamberini M et al (2003) Early- and late-responding cells to saccadic eye movements in the cortical area V6A of macaque monkey. Exp Brain Res Exp 149:83–95. https://doi.org/10.1007/s00221-002-1337-9 CrossRef

Lacquaniti F, Guigon E, Bianchi L et al (1995) Representing spatial information for limb movement: role of area 5 in the monkey. Cereb Cortex 5:391–409CrossRefPubMed

Luppino G, Ben Hamed S, Gamberini M et al (2005) Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur J Neurosci 21:3056–3076. https://doi.org/10.1111/j.1460-9568.2005.04149.x CrossRefPubMed

Marconi B, Genovesio A, Battaglia-Mayer A et al (2001) Eye–hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb Cortex 11:513–527. https://doi.org/10.1093/cercor/11.6.513 CrossRefPubMed

Marigold DS (2008) Role of peripheral visual cues in online visual guidance of locomotion. Exerc Sport Sci Rev 36:145–151. https://doi.org/10.1097/JES.0b013e31817bff72 CrossRefPubMed

Marigold DS, Patla AE (2008) Visual information from the lower visual field is important for walking across multi-surface terrain. Exp Brain Res 188:23–31. https://doi.org/10.1007/s00221-008-1335-7 CrossRefPubMed

McGuire LMM, Sabes PN (2011) Heterogeneous representations in the superior parietal lobule are common across reaches to visual and proprioceptive targets. J Neurosci 31:6661–6673. https://doi.org/10.1523/JNEUROSCI.2921-10.2011 CrossRefPubMedPubMedCentral

Mountcastle VB, Lynch JC, Georgopoulos A et al (1975) Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 38:871–908CrossRefPubMed

Nelson RJ (1980) Representation of the body surface in postcentral cortex (SI) of Macaca fascicularis representations of the body surface in postcentral. J Comp Neurol 194:611–643. https://doi.org/10.1002/cne.901920402 CrossRef

Padberg J, Franca JG, Cooke DF et al (2007) Parallel evolution of cortical areas involved in skilled hand use. J Neurosci 27:10106–10115. https://doi.org/10.1523/JNEUROSCI.2632-07.2007 CrossRefPubMed

Pandya D, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol 204:196–210. https://doi.org/10.1002/cne.902040208 CrossRefPubMed

Passarelli L, Rosa MGP, Gamberini M et al (2011) Cortical connections of area V6Av in the macaque: a visual-input node to the eye/hand coordination system. J Neurosci 31:1790–1801. https://doi.org/10.1523/JNEUROSCI.4784-10.2011 CrossRefPubMed

Perenin M-T, Vighetto A (1988) Optic ataxia: a specific disruption in visuomotor mechanisms. Brain 111:643–674CrossRefPubMed

Piserchia V, Breveglieri R, Hadjidimitrakis K et al (2017) Mixed body/hand reference frame for reaching in 3D space in macaque parietal area PEc. Cereb Cortex 27:1976–1990. https://doi.org/10.1093/cercor/bhw039 PubMed

Pitzalis S, Sereno MI, Committeri G et al (2013) The human homologue of macaque area V6A. Neuroimage 82:517–530. https://doi.org/10.1016/j.neuroimage.2013.06.026 CrossRefPubMed

Raffi M, Ballabeni A, Maioli MG, Squatrito S (2008) Neuronal responses in macaque area PEc to saccades and eye position. Neuroscience 156:413–424. https://doi.org/10.1016/j.neuroscience.2008.08.018 CrossRefPubMed

Raffi M, Maioli MG, Squatrito S (2011) Optic flow direction coding in area PEc of the behaving monkey. Neuroscience 194:136–149. https://doi.org/10.1016/j.neuroscience.2011.07.036 CrossRefPubMed

Raffi M, Persiani M, Piras A, Squatrito S (2014) Optic flow neurons in area PEc integrate eye and head position signals. Neurosci Lett 568:23–28. https://doi.org/10.1016/j.neulet.2014.03.042 CrossRefPubMed

Scherberger H, Andersen RA (2007) Target selection signals for arm reaching in the posterior parietal cortex. J Neurosci 27:2001–2012. https://doi.org/10.1523/JNEUROSCI.4274-06.2007 CrossRefPubMed

Seelke AMH, Padberg JJ, Disbrow E et al (2012) Topographic maps within Brodmann’s area 5 of macaque monkeys. Cereb Cortex 22:1834–1850. https://doi.org/10.1093/cercor/bhr257 CrossRefPubMed

Snyder LH, Batista AP, Andersen RA (1997) Coding of intention in the posterior parietal cortex. Nature 386:167–170. https://doi.org/10.1038/386167a0 CrossRefPubMed

Squatrito S, Raffi M, Maioli MG, Battaglia-Mayer A (2001) Visual motion responses of neurons in the caudal area pe of macaque monkeys. J Neurosci 21:RC130PubMed

Suzuki H, Azuma M (1976) A glass-insulated ‘elgiloy’ microelectrode for recording unit activity in chronic monkey experiments. Electroencephalogr Clin Neurophysiol 41:93–95. https://doi.org/10.1016/0013-4694(76)90218-2 CrossRefPubMed

Taoka M, Toda T, Iwamura Y (1998) Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex. Exp Brain Res 123:315–322. https://doi.org/10.1007/s002210050574 CrossRefPubMed

Taoka M, Toda T, Iriki A et al (2000) Bilateral receptive field neurons in the hindlimb region of the postcentral somatosensory cortex in awake macaque monkeys. Exp Brain Res 134:139–146. https://doi.org/10.1007/s002210000464 CrossRefPubMed

Tosoni A, Pitzalis S, Committeri G et al (2015) Resting-state connectivity and functional specialization in human medial parieto-occipital cortex. Brain Struct Funct 220:3307–3321. https://doi.org/10.1007/s00429-014-0858-x CrossRefPubMed

Van Essen DC, Lewis JW, Drury H et al (2001) Mapping visual cortex in monkeys and humans using surface-based atlases. Vision Res 41:1359–1378CrossRefPubMed

Title: Sensory properties of the caudal aspect of the macaque’s superior parietal lobule
Authors: Michela Gamberini
Giulia Dal Bò
Rossella Breveglieri
Sofia Briganti
Lauretta Passarelli
Patrizia Fattori
Claudio Galletti
Publication date: 01-05-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-017-1593-x

At a glance: The STEP trials

Springer Medicine

Sensory properties of the caudal aspect of the macaque’s superior parietal lobule

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2018

Investigation of brain structure in the 1-month infant

Individual variability in the structural properties of neurons in the human inferior olive

Receptor-driven, multimodal mapping of the human amygdala

Neurophysiological variability masks differences in functional neuroanatomical networks and their effectiveness to modulate response inhibition between children and adults

Neural circuits underlying jaw movements for the prey-catching behavior in frog: distribution of vestibular afferent terminals on motoneurons supplying the jaw

Organization of auditory areas in the superior temporal gyrus of marmoset monkeys revealed by real-time optical imaging