The Pulvinar Thalamic Nucleus of Non-Human Primates: Architectonic and Functional Subdivisions

70 Pages·2018·2.592 MB·English

by  Ricardo Gattass, Juliana G.M. Soares, Bruss Lima

Advances in Anatomy, Embryology and Cell Biology
Ricardo Gattass
Juliana G.M. Soares
Bruss Lima
The Pulvinar Thalamic
Nucleus of Non-Human
Primates: Architectonic
and Functional
Subdivisions
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Ricardo Gattass (cid:129)
Juliana G.M. Soares (cid:129)
Bruss Lima
The Pulvinar
Thalamic Nucleus
of Non-Human
Primates:
Architectonic and
Functional
Subdivisions
RicardoGattass JulianaG.M.Soares
LaboratoryofCognitivePhysiology LaboratoryofCognitivePhysiology
InstituteofBiophysicsCarlosChagas InstituteofBiophysicsCarlosChagas
Filho Filho
FederalUniversityofRiodeJaneiro FederalUniversityofRiodeJaneiro
RiodeJaneiro,Brazil RiodeJaneiro,Brazil
BrussLima
LaboratoryofCognitivePhysiology
InstituteofBiophysicsCarlosChagas
Filho
FederalUniversityofRiodeJaneiro
RiodeJaneiro,Brazil
ISSN0301-5556 ISSN2192-7065 (electronic)
AdvancesinAnatomy,EmbryologyandCellBiology
ISBN978-3-319-70045-8 ISBN978-3-319-70046-5 (eBook)
https://doi.org/10.1007/978-3-319-70046-5
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Abstract
Traditionally, the thalamus is considered a simple relay station controlling the
transmission of sensory information from the periphery to the cortex. This may
be partly true for the so called “first-order” nuclei, such as the lateral geniculate
nucleus(LGN),whichreceivesignalsfromretinalganglioncellsandtransmitthem
totheprimaryvisualcortex.However,recentstudieshavechallengedthissimplis-
tic view of thalamic function, particularly concerning its “higher-order” nuclei,
suchasthepulvinar,whichreceivestrongdriverinputfromthecortex.Inaddition
to receiving cortical afferents, the pulvinar also projects back to several cortical
areas,suggestingthatitmayservearoleinindirectcortical-corticalcommunication
via the thalamus (in parallel to the more direct cortical-cortical pathways).
Visuotopic organization is an important feature of several of the cortical visual
areas that are reciprocally interconnected with the pulvinar. Accordingly, the
pulvinar also exhibits visuotopic organization, probably reflecting its pattern of
connectivity with the cortex and the superior colliculus (SC). However, while
individual cortical areas usually have a single map of the visual world, multiple
visuotopic maps can be present in the pulvinar. How do these maps relate to the
pattern of pulvinar-corticalconnectivityand tothe anatomicalsubdivisions of the
pulvinar?Withinthisframework,itisparamountthatweunderstandthefunctional,
anatomical, and connectional organization of the pulvinar in order to evaluate its
role in cortical information processing. To this aim, we use an evolutionary
approach where we compare how pulvinar organization evolved among New
WorldandOldWorldmonkeys.Wearguethatthechemoarchitecturalorganization
of the pulvinar is highly conserved along primate evolution. On the other hand,
pulvinar functional organization, as evidenced by the number and arrangement of
topographicallyorganizedvisualmaps,ismarkedlyvariableacrossspecies.Weare
thereby challenged by the fact that diverse functional maps, which probably
evolved because of distinct selective and behavioral pressures, are able to coexist
within a common chemoarchitectural scaffold. We also discuss the comparative
cyto- and myeloarchitecture of the pulvinar across different primate species and
argue that both descriptions reside somewhat in between the rigid
v
vi Abstract
chemoarchitectural scaffold on the one hand and the flexible functional layout of
thepulvinarontheother.Assuch,thecyto-andmyeloarchitecturesofthepulvinar
only partially match the pattern of pulvinar-cortical connectivity, while electro-
physiologicalandconnectivitydataarehighlyconsonantwithoneother.Tosupport
our claims, we review electrophysiological, anatomical, and chemo-, cyto-, and
myeloarchitectural data of the pulvinar in different primate species, with special
focus on the New World capuchin monkey and the Old World macaque monkey.
Wefinishbydiscussingthepotentialroleofthepulvinarasafunctionalhubcapable
of organizing brain activity across different brain systems and across distant
regions. The roles of the pulvinar include the control of eye movements, the
selection of salient stimuli, and the modulation of attention, suggesting that the
pulvinar may act to gate incoming information to the neocortex. Indeed, early
studies appointed the pulvinar as a link between the retinotectal system and the
retino-geniculate-cortical system. Later studies have highlighted the role of the
pulvinar as an integration center. The emerging view is that the pulvinar may be
critical to several integrative aspects of cognition, such as modulating cortical
arousalandtheeffectiveallocationofattention.
Contents
1 Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
2 CytoarchitectureandMyeloarchitectureofthePulvinar. . . . . . . . . 5
3 ChemoarchitectureofthePulvinar. . . . . . . . . . . . . . . . . . . . . . . . . . 9
3.1 ChemoarchitectureintheMacaqueMonkey. . . . . . . . . . . . . . . . . 9
3.2 ChemoarchitectureinNewWorldMonkeys. . . . . . . . . . . . . . . . . 11
4 VisualMapRepresentationsinthePrimatePulvinar. . . . . . . . . . . . 15
5 ConnectivityofthePulvinar. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
5.1 PulvinarConnectivitywiththeRetinaandPretectalNuclei. . . . . . 21
5.2 PulvinarConnectivitywiththeSuperiorColliculus. . . . . . . . . . . . 22
5.3 Cortical-PulvinarConnectivity. . . . . . . . . . . . . . . . . . . . . . . . . . 23
6 ReestablishingtheChemoarchitecturalBordersBasedon
ElectrophysiologicalandConnectivityData. . . . . . . . . . . . . . . . . . . 31
7 VisualTopographyofthePulvinarProjectionZones. . . . . . . . . . . . 35
8 ComparativePulvinarOrganizationAcrossDifferent
PrimateSpecies. . . . . . .. . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . 37
9 ResponsePropertiesofPulvinarNeuronsStudiedwithSingle-Unit
ElectrophysiologicalRecordings. . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
9.1 NeuronsClassifiedas“Static”. . . . . . . . . . . . . . . . . . . . . . . . . . . 40
9.2 NeuronsClassifiedas“Dynamic”. . . . . . . . . . . . . . . . . . . . . . . . 43
10 ModulationofPulvinarNeuronalActivitybyArousal. . . . . . . . . . . 49
11 GABAInactivationofthePulvinar. . . . . . . . . . . . . . . . . . . . . . . . . . 53
12 TheRoleofthePulvinarinSpatialVisualAttention. . . . . . . . . . . . 57
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
vii
Chapter 1
Introduction
The optic tracts terminate in a structure denominated as the thalami nervorum
opticorum, or the “optic nerve chamber.” This large gray mass of nervous tissue
locatedatthebaseofthebrainisnowcommonlydesignatedasthethalamus.The
thalamicnucleiareassignedintotheanterior,medial,lateral,ventral,andposterior
nucleargroups,inadditiontothemidlinenuclei.Thepulvinarcomprisesthelargest
portion of the posterior group, which extends from the habenular complex to the
caudal end of the thalamus (Walker 1938). In primates, the pulvinar is also the
largest thalamic nucleus. During evolution, parts of the pulvinar seem to have
evolved from a telencephalic anlage. The development and differentiation of the
pulvinar paralleled a major neocortical enlargement encompassing the temporal,
parietal,andoccipitalregions.Accordingly,thepulvinarisheavilyinterconnected
withseveralcorticalareas(Siqueira1971;Hartingetal.1972;Rakic1974).
The pulvinar can be subdivided into well-delimitated regions based on
chemoarchitectural, cytoarchitectural, myeloarchitectural, connectivity, and elec-
trophysiological criteria (see Table 1.1). However, the subdivisions that emerge
fromthesevarioustechniquesdonotalwaysmatchoneanother.Theclassicalwork
by Walker (1938) used cytoarchitectural criteria to subdivide the pulvinar of the
macaquemonkeyintomedial,lateral,andinferiorportions.However,thisclassical
delimitationdoesnotcorrespondtothoseproposedlaterbyotherresearchersbased
on connectivity (e.g., Lin and Kaas 1979; Ungerleider et al. 1984; Soares et al.
2001),electrophysiologicaltopographicmapping(Allmanetal.1972;Gattassetal.
1978a;Bender1981),orchemoarchitecture(Cusicketal.1993;SteeleandWeller
1993;Gutierrezetal.1995;StepniewskaandKaas1997;Adamsetal.2000).
Subdivisions of the pulvinar based on its chemoarchitectural features are the
most consistently preserved across species of New and Old World monkeys (i.e.,
compare the subdivisions revealed using immunocytochemistry across macaque,
capuchin,squirrel,andowlmonkeysinTable1.1).Immunocytochemicalstaining
forcalbindin,forexample,isoneofthemethodsgenerallyemployedtorevealthe
chemoarchitecture of the primate brain. In the neocortex, calbindin is observed
©SpringerInternationalPublishingAG2018 1
R.Gattassetal.,ThePulvinarThalamicNucleusofNon-HumanPrimates:
ArchitectonicandFunctionalSubdivisions,AdvancesinAnatomy,Embryologyand
CellBiology225,https://doi.org/10.1007/978-3-319-70046-5_1
2 1 Introduction
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Table1.1Pulvinarpartitioningbasedondifferentm SpeciesMethod RhesusmonkeyCytoarchitecture Electrophysiology Connectivity Imunocytochemistry CapuchinmonkeyElectrophysiology Connectivity Imunocytochemistry SquirrelmonkeyCytochemistry Immunocytochemistry OwlmonkeyElectrophysiology Cytoarchitectureandconnecti Immunocytochemistry (1)Walker(1938);(2)Bender(1981);(3)UngerleiderandKaas(1997);(8)Adametal.(2000);(9)Gattassetetal.(1999);(14)Allmanetal.(1972);(15)Linand