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Published in: Brain Structure and Function 9/2021

Open Access 01-12-2021 | Review

Vision for action: thalamic and cortical inputs to the macaque superior parietal lobule

Authors: Michela Gamberini, Lauretta Passarelli, Matteo Filippini, Patrizia Fattori, Claudio Galletti

Published in: Brain Structure and Function | Issue 9/2021

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Abstract

The dorsal visual stream, the cortical circuit that in the primate brain is mainly dedicated to the visual control of actions, is split into two routes, a lateral and a medial one, both involved in coding different aspects of sensorimotor control of actions. The lateral route, named “lateral grasping network”, is mainly involved in the control of the distal part of prehension, namely grasping and manipulation. The medial route, named “reach-to-grasp network”, is involved in the control of the full deployment of prehension act, from the direction of arm movement to the shaping of the hand according to the object to be grasped. In macaque monkeys, the reach-to-grasp network (the target of this review) includes areas of the superior parietal lobule (SPL) that hosts visual and somatosensory neurons well suited to control goal-directed limb movements toward stationary as well as moving objects. After a brief summary of the neuronal functional properties of these areas, we will analyze their cortical and thalamic inputs thanks to retrograde neuronal tracers separately injected into the SPL areas V6, V6A, PEc, and PE. These areas receive visual and somatosensory information distributed in a caudorostral, visuosomatic trend, and some of them are directly connected with the dorsal premotor cortex. This review is particularly focused on the origin and type of visual information reaching the SPL, and on the functional role this information can play in guiding limb interaction with objects in structured and dynamic environments.
Literature
go back to reference Arcaro MJ, Pinsk MA, Li X, Kastner S (2011) Visuotopic organization of macaque posterior parietal cortex: a functional magnetic resonance imaging study. J Neurosci 31:2064–2078PubMedPubMedCentralCrossRef Arcaro MJ, Pinsk MA, Li X, Kastner S (2011) Visuotopic organization of macaque posterior parietal cortex: a functional magnetic resonance imaging study. J Neurosci 31:2064–2078PubMedPubMedCentralCrossRef
go back to reference Baizer JS, Ungerleider LG, Desimone R (1991) Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. J Neurosci 11:168–190PubMedPubMedCentralCrossRef Baizer JS, Ungerleider LG, Desimone R (1991) Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. J Neurosci 11:168–190PubMedPubMedCentralCrossRef
go back to reference Battaglia-Mayer A, Mascaro M, Caminiti R (2007) Temporal evolution and strength of neural activity in parietal cortex during eye and hand movements. Cereb Cortex 17:1350–1363PubMedCrossRef Battaglia-Mayer A, Mascaro M, Caminiti R (2007) Temporal evolution and strength of neural activity in parietal cortex during eye and hand movements. Cereb Cortex 17:1350–1363PubMedCrossRef
go back to reference Ben HS, Duhamel J-R, Bremmer F, Graf W (2001) Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis. Exp Brain Res 140:127–144CrossRef Ben HS, Duhamel J-R, Bremmer F, Graf W (2001) Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis. Exp Brain Res 140:127–144CrossRef
go back to reference Blatt GJ, Andersen RA, Stoner GR (1990) Visual receptive field organization and cortico-cortical connections of the lateral intraparietal area (area LIP) in the macaque. J Comp Neurol 299:421–445PubMedCrossRef Blatt GJ, Andersen RA, Stoner GR (1990) Visual receptive field organization and cortico-cortical connections of the lateral intraparietal area (area LIP) in the macaque. J Comp Neurol 299:421–445PubMedCrossRef
go back to reference Brodmann K (1909) Vergleichende Lokalisationslehre der Groβhirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Brodmann K (1909) Vergleichende Lokalisationslehre der Groβhirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues.
go back to reference Cardin V, Smith AT (2010) Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation. Cereb Cortex 20:1964–1973PubMedCrossRef Cardin V, Smith AT (2010) Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation. Cereb Cortex 20:1964–1973PubMedCrossRef
go back to reference Cardin V, Smith AT (2011) Sensitivity of human visual cortical area V6 to stereoscopic depth gradients associated with self-motion. J Neurophysiol 106:1240–1249PubMedPubMedCentralCrossRef Cardin V, Smith AT (2011) Sensitivity of human visual cortical area V6 to stereoscopic depth gradients associated with self-motion. J Neurophysiol 106:1240–1249PubMedPubMedCentralCrossRef
go back to reference Caspari N, Arsenault JT, Vandenberghe R, Vanduffel W (2018) Functional similarity of medial superior parietal areas for shift-selective attention signals in humans and monkeys. Cereb Cortex 28:2085–2099PubMed Caspari N, Arsenault JT, Vandenberghe R, Vanduffel W (2018) Functional similarity of medial superior parietal areas for shift-selective attention signals in humans and monkeys. Cereb Cortex 28:2085–2099PubMed
go back to reference Colby CL, Gattass R, Olson CR, Gross CG (1988) Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. J Comp Neurol 269:392–413PubMedCrossRef Colby CL, Gattass R, Olson CR, Gross CG (1988) Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. J Comp Neurol 269:392–413PubMedCrossRef
go back to reference Colby CL, Duhamel JR, Goldberg ME (1993) Ventral intraparietal area of the macaque: anatomic location and visual response properties. J Neurophysiol 69:902–914PubMedCrossRef Colby CL, Duhamel JR, Goldberg ME (1993) Ventral intraparietal area of the macaque: anatomic location and visual response properties. J Neurophysiol 69:902–914PubMedCrossRef
go back to reference Cottereau BR, Smith AT, Rima S et al (2017) Processing of egomotion-consistent optic flow in the rhesus macaque cortex. Cereb Cortex 27:330–343PubMedPubMedCentral Cottereau BR, Smith AT, Rima S et al (2017) Processing of egomotion-consistent optic flow in the rhesus macaque cortex. Cereb Cortex 27:330–343PubMedPubMedCentral
go back to reference Di Marco S, Fattori P, Galati G et al (2021) Preference for locomotion-compatible curved paths and forward direction of self-motion in somatomotor and visual areas. Cortex 137:74–92PubMedCrossRef Di Marco S, Fattori P, Galati G et al (2021) Preference for locomotion-compatible curved paths and forward direction of self-motion in somatomotor and visual areas. Cortex 137:74–92PubMedCrossRef
go back to reference Dow BM (1974) Functional classes of cells and their laminar distribution in monkey visual cortex. J Neurophysiol 37:927–946PubMedCrossRef Dow BM (1974) Functional classes of cells and their laminar distribution in monkey visual cortex. J Neurophysiol 37:927–946PubMedCrossRef
go back to reference Fischer E, Bülthoff HH, Logothetis NK, Bartels A (2012a) Human areas V3A and V6 compensate for self-induced planar visual motion. Neuron 73:1228–1240PubMedCrossRef Fischer E, Bülthoff HH, Logothetis NK, Bartels A (2012a) Human areas V3A and V6 compensate for self-induced planar visual motion. Neuron 73:1228–1240PubMedCrossRef
go back to reference Fischer E, Bülthoff HH, Logothetis NK, Bartels A (2012b) Visual motion responses in the posterior cingulate sulcus: a comparison to V5/MT and MST. Cereb Cortex 22:865–876PubMedCrossRef Fischer E, Bülthoff HH, Logothetis NK, Bartels A (2012b) Visual motion responses in the posterior cingulate sulcus: a comparison to V5/MT and MST. Cereb Cortex 22:865–876PubMedCrossRef
go back to reference Fusi S, Miller EK, Rigotti M (2016) Why neurons mix: high dimensionality for higher cognition. Curr Opin Neurobiol 37:66–74PubMedCrossRef Fusi S, Miller EK, Rigotti M (2016) Why neurons mix: high dimensionality for higher cognition. Curr Opin Neurobiol 37:66–74PubMedCrossRef
go back to reference Galletti C, Fattori P (2003) Neuronal mechanisms for detection of motion in the field of view. Neuropsychologia 41:1717–1727PubMedCrossRef Galletti C, Fattori P (2003) Neuronal mechanisms for detection of motion in the field of view. Neuropsychologia 41:1717–1727PubMedCrossRef
go back to reference Galletti C, Battaglini PP, Fattori P (1993) Parietal neurons encoding spatial locations in craniotopic coordinates. Exp Brain Res 96:221–229PubMedCrossRef Galletti C, Battaglini PP, Fattori P (1993) Parietal neurons encoding spatial locations in craniotopic coordinates. Exp Brain Res 96:221–229PubMedCrossRef
go back to reference Graziano MSA, Cooke DF, Taylor CSR (2000) Coding the location of the arm by sight. Science 290:1782–1786PubMedCrossRef Graziano MSA, Cooke DF, Taylor CSR (2000) Coding the location of the arm by sight. Science 290:1782–1786PubMedCrossRef
go back to reference Hsu DT, Price JL (2007) Midline and intralaminar thalamic connections with the orbital and medial prefrontal networks in macaque monkeys. J Comp Neurol 504:89–111PubMedCrossRef Hsu DT, Price JL (2007) Midline and intralaminar thalamic connections with the orbital and medial prefrontal networks in macaque monkeys. J Comp Neurol 504:89–111PubMedCrossRef
go back to reference Hsu DT, Kirouac GJ, Zubieta J-K, Bhatnagar S (2014) Contributions of the paraventricular thalamic nucleus in the regulation of stress, motivation, and mood. Front Behav Neurosci 8:73PubMedPubMedCentralCrossRef Hsu DT, Kirouac GJ, Zubieta J-K, Bhatnagar S (2014) Contributions of the paraventricular thalamic nucleus in the regulation of stress, motivation, and mood. Front Behav Neurosci 8:73PubMedPubMedCentralCrossRef
go back to reference Kaas JH, Qi H-X, Stepniewska I (2018) The evolution of parietal cortex in primates. Handb Clin Neurol 151:31–52PubMedCrossRef Kaas JH, Qi H-X, Stepniewska I (2018) The evolution of parietal cortex in primates. Handb Clin Neurol 151:31–52PubMedCrossRef
go back to reference Land MF (2014) Do we have an internal model of the outside world? Philos Trans R Soc B Biol Sci 369:20130045CrossRef Land MF (2014) Do we have an internal model of the outside world? Philos Trans R Soc B Biol Sci 369:20130045CrossRef
go back to reference Lund JS, Lund RD, Hendrickson AE et al (1975) The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol 164:287–303PubMedCrossRef Lund JS, Lund RD, Hendrickson AE et al (1975) The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol 164:287–303PubMedCrossRef
go back to reference Mai JK, Forutan F (2012) Chapter 19—Thalamus. In: Mai JK, Paxinos GBT (eds) The human. Academic Press, San Diego, pp 618–677 Mai JK, Forutan F (2012) Chapter 19—Thalamus. In: Mai JK, Paxinos GBT (eds) The human. Academic Press, San Diego, pp 618–677
go back to reference Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31:236–250PubMedCrossRef Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31:236–250PubMedCrossRef
go back to reference Milner AD, Goodale MA (1995) Oxford psychology series, No. 27. The visual brain in action Milner AD, Goodale MA (1995) Oxford psychology series, No. 27. The visual brain in action
go back to reference Mushiake H, Strick PL (1995) Pallidal neuron activity during sequential arm movements. J Neurophysiol 74:2754–2758PubMedCrossRef Mushiake H, Strick PL (1995) Pallidal neuron activity during sequential arm movements. J Neurophysiol 74:2754–2758PubMedCrossRef
go back to reference Nau M, Schröder TN, Bellmund JLS, Doeller CF (2018) Hexadirectional coding of visual space in human entorhinal cortex. Nat Neurosci 21:188–190PubMedCrossRef Nau M, Schröder TN, Bellmund JLS, Doeller CF (2018) Hexadirectional coding of visual space in human entorhinal cortex. Nat Neurosci 21:188–190PubMedCrossRef
go back to reference Pitzalis S, Sereno MI, Committeri G et al (2010) Human V6: the medial motion area. Cereb Cortex 20:411–424PubMedCrossRef Pitzalis S, Sereno MI, Committeri G et al (2010) Human V6: the medial motion area. Cereb Cortex 20:411–424PubMedCrossRef
go back to reference Pitzalis S, Hadj-Bouziane F, Dal Bò G et al (2021) Optic flow selectivity in the macaque parieto-occipital sulcus. Brain Struct Funct 1–20 Pitzalis S, Hadj-Bouziane F, Dal Bò G et al (2021) Optic flow selectivity in the macaque parieto-occipital sulcus. Brain Struct Funct 1–20
go back to reference Rausell E, Bickford L, Manger PR et al (1998) Extensive divergence and convergence in the thalamocortical projection to monkey somatosensory cortex. J Neurosci 18:4216–4232PubMedPubMedCentralCrossRef Rausell E, Bickford L, Manger PR et al (1998) Extensive divergence and convergence in the thalamocortical projection to monkey somatosensory cortex. J Neurosci 18:4216–4232PubMedPubMedCentralCrossRef
go back to reference Rizzolatti G, Gerbella M, Rozzi S (2020) 420—the posterior parietal cortex. Fritzsch BBT-TSACR, 2nd edn. Elsevier, Oxford, pp 333–348 Rizzolatti G, Gerbella M, Rozzi S (2020) 420—the posterior parietal cortex. Fritzsch BBT-TSACR, 2nd edn. Elsevier, Oxford, pp 333–348
go back to reference Sulpizio S, Del Maschio N, Del Mauro G et al (2020) Bilingualism as a gradient measure modulates functional connectivity of language and control networks. Neuroimage 205:116306PubMedCrossRef Sulpizio S, Del Maschio N, Del Mauro G et al (2020) Bilingualism as a gradient measure modulates functional connectivity of language and control networks. Neuroimage 205:116306PubMedCrossRef
go back to reference Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Anal Vis Behav Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Anal Vis Behav
go back to reference Vallar G, Coslett HB (2018) The parietal lobe. Academic Press Vallar G, Coslett HB (2018) The parietal lobe. Academic Press
go back to reference Yeterian EH, Pandya DN (1997) Corticothalamic connections of extrastriate visual areas in rhesus monkeys. J Comp Neurol 378:562–585PubMedCrossRef Yeterian EH, Pandya DN (1997) Corticothalamic connections of extrastriate visual areas in rhesus monkeys. J Comp Neurol 378:562–585PubMedCrossRef
go back to reference Zeki SM (1978) Functional specialisation in the visual cortex of the rhesus monkey. Nature 274:423–428PubMedCrossRef Zeki SM (1978) Functional specialisation in the visual cortex of the rhesus monkey. Nature 274:423–428PubMedCrossRef
Metadata
Title
Vision for action: thalamic and cortical inputs to the macaque superior parietal lobule
Authors
Michela Gamberini
Lauretta Passarelli
Matteo Filippini
Patrizia Fattori
Claudio Galletti
Publication date
01-12-2021
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 9/2021
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-021-02377-7

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