ORIGINAL ARTICLE

Thalamic projections to visual and visuomotor areas (V6and V6A) in the Rostral Bank of the parieto-occipital sulcusof the Macaque

Michela Gamberini • Sophia Bakola • Lauretta Passarelli •

Kathleen J. Burman • Marcello G. P. Rosa • Patrizia Fattori •

Claudio Galletti

Received: 15 September 2014 / Accepted: 9 January 2015

� Springer-Verlag Berlin Heidelberg 2015

Abstract The medial posterior parietal cortex of the

primate brain includes different functional areas, which

have been defined based on the functional properties, cyto-

and myeloarchitectural criteria, and cortico-cortical con-

nections. Here, we describe the thalamic projections to two

of these areas (V6 and V6A), based on 14 retrograde

neuronal tracer injections in 11 hemispheres of 9 Macaca

fascicularis. The injections were placed either by direct

visualisation or using electrophysiological guidance, and

the location of injection sites was determined post mortem

based on cyto- and myeloarchitectural criteria. We found

that the majority of the thalamic afferents to the visual area

V6 originate in subdivisions of the lateral and inferior

pulvinar nuclei, with weaker inputs originating from the

central densocellular, paracentral, lateral posterior, lateral

geniculate, ventral anterior and mediodorsal nuclei. In

contrast, injections in both the dorsal and ventral parts of

the visuomotor area V6A revealed strong inputs from the

lateral posterior and medial pulvinar nuclei, as well as

smaller inputs from the ventrolateral complex and from the

central densocellular, paracentral, and mediodorsal nuclei.

These projection patterns are in line with the functional

properties of injected areas: ‘‘dorsal stream’’ extrastriate

area V6 receives information from visuotopically organ-

ised subdivisions of the thalamus; whereas visuomotor area

V6A, which is involved in the sensory guidance of arm

movement, receives its primary afferents from thalamic

nuclei that provide high-order somatic and visual input.

Keywords Posterior parietal cortex � Connectivity �Primate � Thalamus � Superior parietal lobule �Sensorimotor input

Abbreviations

Thalamic nuclei

AD Anterior dorsal

AM Anterior medial

AV Anterior ventral

Bsc Brachium of superior colliculus

Can Capsule of the anterior nuclei

Cdc Central densocellular

CL Central lateral

CM Centromedian

Csl Centralis superior lateralis

GLvo Lateral geniculate, pars oralis

GLd Lateral geniculate, dorsalis

GMpc Medial geniculate, pars parvocellularis

LGN Lateral geniculate

Li Limitans

LP Lateral posterior

MD Mediodorsal

MDdc Mediodorsal, pars densocellularis

MDmc Mediodorsal, pars magnocellularis

MDpc Mediodorsal, pars parvocellularis

MG Medial geniculate

MGpc Medial geniculate, pars parvocellularis

M. Gamberini � S. Bakola � L. Passarelli � P. Fattori �C. Galletti (&)

Department of Pharmacy and Biotechnology, University of

Bologna, Piazza di Porta S. Donato, 2, 40126 Bologna, Italy

e-mail: claudio.galletti@unibo.it

S. Bakola � K. J. Burman � M. G. P. Rosa

Department of Physiology, Monash University, Clayton,

VIC 3800, Australia

S. Bakola � M. G. P. Rosa

Australian Research Council, Centre of Excellence for

Integrative Brain Function, Monash University Node, Clayton,

VIC 3800, Australia

123

Brain Struct Funct

DOI 10.1007/s00429-015-0990-2

PC/Pcn Paracentral

Pul Pulvinar

PuI Pulvinar, inferior subdivision

PuL Pulvinar, lateral subdivision

PuM Pulvinar, medial subdivision

SG Suprageniculatus

STN Subthalamic

R Reticular

VAmc Ventral anterior, pars magnocellularis

VAdc Ventral anterior, pars densocellularis

VL Ventral lateral

VLc Ventral lateral, pars caudalis

VLm Ventral lateral, pars medialis

VLo Ventral lateral, pars oralis

VLps Ventral lateral, pars postrema

VPI Ventral posterior inferior

VPL Ventral posterior lateral

VPLo Ventral posterior lateral, pars oralis

VPLc Ventral posterior lateral, pars caudalis

VPM Ventral posterior medial

X Area X

Neuronal tracers and histological solutions

CTB-green Cholera toxin B subunit conjugated with

Alexa fluor 488

CTB-red Cholera toxin B subunit conjugated with

Alexa fluor 594

CTB-gold Cholera toxin B subunit conjugated with

colloidal gold

DY Diamidino-yellow

FB Fast blue

WGA-HRP Wheat germ agglutinin conjugated to

horseradish peroxidase

PBS Phosphate buffered saline

Cortical areas

SPL Superior parietal lobule

V6 Area V6

V6Ad Area V6A, dorsal portion

V6Av Area V6A, ventral portion

Introduction

The cortical areas located on the rostral bank of the pa-

rieto-occipital sulcus and adjacent portions of the superior

parietal lobule have been extensively studied in the

macaque monkey, particularly over the last two decades

(Galletti et al. 1996, 1999a, b, 2004; Breveglieri et al.

2002; Fattori et al. 2005; Luppino et al. 2005; for a

review see Gamberini et al. 2011). These studies have

reported the existence of two areas that are distinct in

terms of physiological properties, connections, and cyto-

architecture. From caudal to rostral (Fig. 1), they have

been designated as areas V6 and V6A, with V6A subdi-

vided into ventral (V6Av) and dorsal (V6Ad) regions.

Area V6 is a visual extrastriate area, in which neurons

form a systematic representation of the entire contralateral

visual field, albeit with a much reduced emphasis on

central vision in comparison with the striate cortex

(Daniel and Whitteridge 1961; Galletti et al. 1999a). In

contrast, V6Av and V6Ad are better described as two

functionally related subdivisions of the same visuomotor

area, V6A, which have relatively complementary func-

tions related to the integration of visual and somatic

signals for the control of arm and hand movements

towards targets in peripersonal space (Gamberini et al.

2011). Although the cortical connections of these regions

have been described in detail (Galletti et al. 2001; Gam-

berini et al. 2009; Passarelli et al. 2011), their thalamic

afferents have not yet been compared.

Previous studies in macaques (Yeterian and Pandya

1985; Schmahmann and Pandya 1990; Yeterian and

Pandya 1997) and New World owl and squirrel monkeys

(Gharbawie et al. 2010) have shown that posterior parietal

areas are preferentially connected with the lateral posterior

(LP), ventral lateral (VL), and medial pulvinar (PuM)

thalamic nuclei (see, Grieve et al. 2000). In addition, pre-

liminary results obtained after injections in the V6/V6A

region indicated weak but consistent connections with the

medial and lateral subdivisions of the pulvinar complex

(Shipp et al. 1998). Finally, the dorsomedial visual area

(DM), an extrastriate region that has been considered the

New World monkey homologue of area V6 (Rosa et al.

2009; Paxinos et al. 2012), receives projections from the

lateral (PuL) and inferior (PuI) subdivisions of the pulvi-

nar, as well as sparser connections from the lateral genic-

ulate nucleus (LGN) and nucleus limitans (Li) (see, Beck

and Kaas 1998).

Since the precise cytoarchitectural and myeloarchitec-

tural correlates of V6, V6Av, and V6Ad have been estab-

lished in the macaque (Luppino et al. 2005), it has become

possible to achieve a more detailed understanding of their

afferent projections from specific thalamic nuclei. In the

present paper, we aimed to compare the relative numerical

weight of the projections from different thalamic nuclei to

areas V6 and V6A, to obtain further insights on the net-

work activity that defines their neuronal function (e.g.

Burman et al. 2011).

Materials and methods

Experimental protocols were approved by the Bioethics

Committee of the University of Bologna and by the

Brain Struct Funct

123

Monash University Animal Experimentation Ethics

Committee, in accordance with the guidelines of the

European Directive 86/609/EEC, the revised Directive

2010/63/EU, and the Australian Code of Practice for the

Care and Use of Animals for Scientific Purposes. Fourteen

retrograde tracer injections were placed in 11 hemispheres

of 9 male adult monkeys (Macaca fascicularis, 3–7 kg).

Selection of injection sites was performed either by direct

visualisation of areas V6 and V6A (dorsal and ventral

subdivisions), based on sulcal morphology, or under

electrophysiological guidance, following previously

defined criteria (Galletti et al. 2001; Gamberini et al.

2009; Passarelli et al. 2011). The extent of each injection

site was reconstructed post mortem from cyto- and my-

eloarchitectural material. Figure 2a illustrates a schematic

of the extent of the injection sites relative to the bound-

aries of the different areas, projected onto a flat map

reconstruction of a reference macaque brain prepared with

the software CARET (http://www.nitrc.org/projects/caret/,

Van Essen et al. 2001). Table 1 presents details of indi-

vidual injections.

Injections by direct visualisation of the cortex

Full details of the experimental procedures have been

described previously (Galletti et al. 1995, 1999b, 2001,

2005; Gamberini et al. 2009; Passarelli et al. 2011). In six

animals (cases A1R, A3R/A3L, A4R, MF1, MF2, and

11L), the target region was visualised during surgery under

aseptic conditions. Four of these animals were pre-treated

with atropine (0.05 mg/kg, i.m.) and anaesthetized with

ketamine hydrochloride (12 mg/kg, i.m.) followed, after

30 min, with sodium thiopental (8 mg/kg, i.v., with sup-

plemental doses as required). To avoid oedema, mannitol

was administered intravenously (1 g/kg). A different pro-

tocol was used for animals MF1 and MF2, which were

premedicated with intramuscular injections of diazepam

(3.0 mg/kg) and atropine (0.2 mg/kg), with anaesthesia

being induced, 30 min later, with alfaxalone (10 mg/kg,

i.m.; supplemental doses of 5 mg/kg were administered

intravenously during surgery, as required). In all cases,

animals were secured to a stereotaxic frame and, after

craniotomy, the superior parietal lobule was exposed, the

pos

ls

sts

lf

ipscs cin

CC

pos

ars

cal

BA

iosots

ps

pos

a

v

lsstslf

ips

cs

pcd

MIP

PEcPEMS

V6

V6Ad

V6AvPG

PFG

PF

V6AdV6AvV6

pom

cin

CC

pos

a

v

PEcPE

PGm

M S

V6

area31 V6Av

V6Ad

pom

Fig. 1 Anatomical localization of the areas of the rostral bank of

parieto-occipital sulcus. a Lateral view of macaque brain. The

enlargement in the bottom part of the figure highlights in colour the

location of areas V6A (subdivided into V6Ad and V6Av) and V6,

which are hidden on the depth of the parieto-occipital sulcus. The

intraparietal and parieto-occipital sulci are opened to show the areas

hidden within (grey surface). Dashed lines delimit other areas

reported in the literature (see below). b Mesial view of macaque

brain. The enlargement in the bottom part of the figure shows the

cortical areas located in the mesial wall of the hemisphere, with the

areas of interest shown in colour. ars arcuate sulcus, cal calcarine

sulcus, cin cingulate sulcus, cs central sulcus, ips intraparietal sulcus,

ios inferior occipital sulcus, lf lateral fissure, ls lunate sulcus, ots

occipito-temporal sulcus, pcd post central dimple, pos parieto-

occipital sulcus, pom medial parieto-occipital sulcus, ps principal

sulcus, sts superior temporal sulcus, a anterior, v ventral, CC corpus

callosum, M primary motor area, S primary somatosensory area; PE,

PEc, MIP, PG, PFG, PF, PGm, 31, V6, V6Ad, V6Av, areas PE, PEc,

MIP, PG, PFG, PF, PGm, area 31, V6, V6Ad, V6Av. (Galletti et al.

1996; Morecraft et al. 2004; Scheperjans et al. 2008)

Brain Struct Funct

123

dura mater retracted, and neuronal tracers applied directly

to the cortex based on visualisation of the sulcal pattern.

The cortical midline and parieto-occipital sulcus were

retracted to expose the regions of interest, allowing injec-

tions through a Hamilton microsyringe, which had been

fitted with a glass micropipette attached to the needle. At

the end of the surgery, the exposed cortex was covered with

ophthalmic film (Gelfilm) and a thin layer of Gelfoam. The

bone was replaced, and the wound was sutured. Analgesics

(Ketorolac, 1 mg/kg, i.m., or Carprofen, 5 mg/kg, s.c., for

2–3 consecutive days) and antibiotics (Erythromycin,

1–1.5 ml/10 kg, or Norocillin, 0.1 ml) were administered

postoperatively. In all cases, the University veterinary staff

monitored physiological parameters during surgeries, as

well as the animal’s recovery in subsequent days.

Injections guided by electrophysiological recordings

In three animals (M17R and L, M18L and M21R), the

tracer injections were placed at the conclusion of long-

lasting (several months) single-unit recording experiments,

using a ‘recording syringe’ to target physiologically iden-

tified sites. During the recording sessions, the animals sat

in a primate chair performing fixation and motor tasks,

ls pos

ipslf

cs

ars

ps

V6AdV6AvV6

sts

V6AvV6

pos

ls

ips

pom

V6Ad

11LA3R

A3aL

A1R

M21R

A4bR

A4aR

M17R

M17L

V6Ad

V6Av

V6

injection core

M17R

A3bL

MF1L

MF2L

M18L

10°

70°V1V2

V6Av

poscin

1

2

3

4

5

6

7

8

1

NV

NV

NV2

34

5

6

7

8

ipsi contra

80°

NVpos

lsips

sts

cspsars

250µm

5mm

A

B

V6AdV6Av

a

v

Fig. 2 Injection sites. a Injection sites are illustrated on the right on a

two-dimensional reconstruction of the rostral bank of parieto-occipital

sulcus of the left hemisphere of a reference monkey brain (http://

www.nitrc.org/projects/caret/, Van Essen et al. 2001) shown on the

left. The dashed contours represent the approximate cytoarchitectonic

borders of V6Ad, V6Av, and V6. The ‘‘halo’’ and ‘‘core’’ zones of

injection sites are shown as coloured and black areas, respectively,

with the name of cases reported (see also Table 1). b Reconstruction

of an injection performed under electrophysiological guidance (case

M21R). The recording site was in V6Av. The ‘‘halo’’ and ‘‘core’’

zones of the injection site are shown on the parasagittal section to the

left as white and black ovals, respectively. The enlargement to the

right of the section reports the type of cells encountered in V6Av

along the penetration. Black circles indicate non-visually responsive

(NV) cells, and white circles visually responsive cells. The receptive

fields of V6A visual cells are reported to the right, together with those

of cells recorded in the primary and second visual areas, while passing

through the occipital lobe. V1 primary visual area, V2 second visual

area, ipsi ipsilateral visual field, contra contralateral visual field.

Other abbreviations are as in Fig. 1

Brain Struct Funct

123

with the head restrained, while glass-coated Elgiloy

microelectrodes (Suzuki and Azuma 1976) were advanced

through the intact dura mater using a remote-controlled

microdrive. Eye position was recorded by an infrared oc-

ulometer (Bach et al. 1983). Visual stimuli of different

form, colour, size, orientation, direction, and speed of

movement were used for testing the visual responsiveness

of recorded cells, and for mapping visual receptive fields

(Fig. 2b). Areas V6 and V6A were identified using well-

established physiological criteria (Galletti et al. 1996,

1999a, b), including the size and pattern of progression of

receptive fields, and pattern of activity during motor tasks.

Cells were assigned to the ventral or dorsal part of V6A

(V6Av, V6Ad) post mortem after microelectrode recon-

structions from cyto- and myeloarchitectural material

(Luppino et al. 2005), as detailed by Gamberini and col-

leagues (Gamberini et al. 2011).

Histological procedures

After a variable survival period [14 days for fluorescent

tracers, 10 days for gold-conjugated cholera toxin subunit B

(CTB-gold), and 2 days for horseradish peroxidase (HRP)],

the animals were anaesthetized with ketamine hydrochlo-

ride (15 mg/kg, i.m.) or alfaxalone (10 mg/kg, i.m.). Fol-

lowing loss of consciousness, they received a lethal dose of

sodium thiopental (i.v.), and, upon cardiac arrest, were

perfused with 3 l of normal saline solution, followed by 5 l

of 4 % paraformaldehyde in 0.1 M phosphate buffer at pH

7.4 (3.5 % in the case of the HRP injection), and 4 l of 5 %

glycerol in the same buffer (except for cases MF1 and

MF2). The brains were removed from the skulls, photo-

graphed from all views, and cryoprotected by immersion in

0.1 M phosphate buffer solutions containing glycerol (10

and 20 %; most cases), or sucrose (10–30 %; MF1 and

MF2). The brains were then snap-frozen, and stored at -

80 �C. Sections (50–60 lm) were obtained using a freezing

microtome or a cryostat. In most cases, the brain was sec-

tioned in the parasagittal plane (only exception: case 11L in

coronal plane). This choice was dictated by the need to

determine the histological boundaries of V6, V6Av and

V6Ad, which are best visualised in parasagittal sections.

Five series of sections were obtained, one of which was

always stained for Nissl substance, and another for myelin

(Gallyas 1979). In animals MF1 and MF2 a third series was

stained for cytochrome oxidase (Wong-Riley 1979). The

other series were left unstained for fluorescence observa-

tion, processed to reveal CTB-gold by the silver-intensifi-

cation protocol (Kritzer and Goldman-Rakic 1995), or

processed to reveal HRP using the tetra-methyl-benzidine

method (Mesulam and Rosene 1979). All sections were

coverslipped with DPX after quick steps of dehydration in

100 % ethanol, and clearing with xylene.

Data analysis

The sections were examined for labelled neurons using

microscopes (Zeiss Axioscope or Axio Imager) equipped

Table 1 Injection sites and neuronal tracers employed in the experiments

Animal Cutting

plane

Injected

area

Tracer Amount and

concentration

Functional

study

Total of cortical and

thalamic labelled cells

M17L Parasagittal V6 WGA-HRPa 0.10 ll, 4 % in distilled water Yes 16,892

M17R Parasagittal V6 (V2 leakage) FBb 0.20 ll, 3 % in distilled water Yes 5,151

M17R Parasagittal V6Av CTB-goldc 0.8 ll, 0.5 % in distilled water Yes 11,977

A4aR Parasagittal V6Av CTB-redd 1.7 ll, 1 % in PBS No 11,667

A4bR Parasagittal V6Av CTB-greend 1.7 ll, 1 % in PBS No 5,350

M21R Parasagittal V6Av FBb 0.20 lL, 3 % in distilled water Yes 2,162

MF1L Parasagittal V6Av/V6 FBb 1 crystal No 11,695

MF2L Parasagittal V6Av/V6Ad FBb 1 crystal No 4,546

11L Coronal V6Ad WGA-HRPa 0.20 ? 0.28 ll, 4 % in distilled water No 106,656

A1R Parasagittal V6Ad CTB-redd 1.5 ll, 1 % in PBS No 9,567

A3R Parasagittal V6Ad FB2 0.20 ll, 3 % in distilled water No 5,468

A3aL Parasagittal V6Ad CTB-redd 1.5 ll, 1 % in PBS No 878

A3bL Parasagittal V6Ad CTB-greend 1.5 ll, 1 % in PBS No 4,599

M18L Parasagittal V6Ad/V6Av (V2 leakage) WGA-HRPa 0.08 ll, 4 % in distilled water Yes 4,333

a Sigma Aldrich SrLb Polysciences Europe GmbH, Germanyc List, Campbell, Californiac Molecular Probes

Brain Struct Funct

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with 109 and 209 objectives. For each case, the entire

hemisphere ipsilateral to the injection site was examined

for retrograde label. Although anterograde label from some

of the injections was visualised, only the retrograde label

has been quantified for the purpose of the present report.

The section outlines and the location of labelled neurons

were plotted at 250–300 micron intervals, using a com-

puterised system linked to X/Y transducers mounted on the

microscope stage.

The histological criteria used for the definition of the

boundaries of areas around the injection sites have been

fully described in previous studies (Galletti et al. 2001;

Luppino et al. 2005; Gamberini et al. 2009; Passarelli et al.

2011). The present report focuses on injections which were

found to be confined to a single architectonic area,

although data from injections that crossed areal boundaries

have been used as comparison and/or confirmation of

particular aspects of the data, as detailed in the ‘‘Results’’

section.

To identify the thalamic nuclei in coronal sections, we

used the atlas of Olszewski (1952), and for parasagittal

sections, we referred to Ilinsky and Kultas-Ilinsky (1987).

Figure 3a, b shows examples of data plotted on parasagittal

and coronal sections, respectively. For the nomenclature of

some thalamic nuclei, to harmonise the names and abbre-

viations between the two different planes of cutting, we

also referred to the review by Mai and Forutan (2012) (see

the details in Table 2). To define the labelled thalamic

nuclei, a camera lucida attachment was used to bring

stained histological sections into register with the corre-

sponding drawings containing the positions of labelled

cells.

Results

We report on the results of tracer injections in areas V6 and

V6A (V6Av and V6Ad) of nine animals. As shown in

Fig. 2, two injections were placed in area V6. Based on the

location of visual receptive fields mapped with the

recording syringe (see ‘‘Materials and methods’’), and on

the location of labelled neurons in V1, these injections

covered different retinotopic regions of area V6: the near-

peripheral part of the visual field in M17L (between 10�and 20� from the fovea; see Fig. 4h), and the far-peripheral

part of the visual field in M17R (between 35� of eccen-

tricity and the monocular crescents; see Fig. 4h). In case

M17R, leakage of tracer was observed along the needle

track in the posterior bank of the parieto-occipital sulcus at

the level of the second visual area (V2), where the lower

visual field approximately 10� from the fovea is repre-

sented (see Fig. 5c) (see also Gattass et al. 1981). Four

injection sites were entirely confined within the limits of

V6Av, and five injections within those of V6Ad. In animals

in which functional studies were carried out (see Table 1),

the visual field representation at the injection sites was

indicated by the location of receptive fields mapped with

the recording syringe (see example of Fig. 2b). Data from

injections that crossed the borders between V6Av and

V6Ad (two cases, Table 1) or between V6Av and V6 (one

case, Table 1) will only be briefly summarised.

In all cases, projecting cells were found in a relatively

small number of thalamic nuclei. In agreement with the

results of Markov et al. (2011) in other cortical areas, we

found that the number of labelled neurons in the thalamus

represented a small fraction of the overall cortical and

thalamic afferents to an area (V6, 3.4 ± 0.7 %; V6Av,

1.6 ± 0.9 %; V6Ad, 4.0 ± 3.4 %). For the present analy-

ses, we considered input from a given thalamic nucleus to

an area as significant when it corresponded to at least 1 %

of all labelled cells in the thalamus; projections that did not

reach this threshold will not be discussed further.

Thalamic afferents to V6

Figure 4 illustrates the distribution of labelled cells in the

thalamus after V6 injections. In both cases, the majority of

labelled cells were found in two distinct clusters in the

visual nuclei of the pulvinar complex, that included the

PuL, dorsally, and the PuI, ventrally.

In the near-peripheral case, labelled cells were found in

the portion of both PuL and PuI that corresponds to the

visual field representation at the injected cortical region,

that is 10�–20� of the lower visual field representation,

between the representation of the horizontal and vertical

meridians (Fig. 5a). In the far-peripheral case (Fig. 5d),

labelled cells were also found in about the same portion of

PuL and PuI. This incongruence may derive from the low

magnification factor at peripheral representations, and/or

by the inherent imprecision in comparing results across

animals without direct electrophysiological recordings.

However, since the pulvinar region labelled in this case

included the part of the visual field represented in the

region of V2 involved by the leakage of neuronal tracer

(see Fig. 5c), some of these labelled cells could also be due

to the tracer leakage.

After V6 injections, labelled cells were also found in

the LGN (Figs. 4b, e, 5), mostly in the interlaminar lay-

ers. In the near-peripheral case, labelled cells were found

in the portion of LGN that corresponds to the near-

peripheral visual field representation (see Fig. 5b), in

agreement with the region of V6 we injected. In the far-

peripheral case, labelled cells were only found in the

portion of LGN that corresponds to the paracentral lower

Brain Struct Funct

123

visual field representation (see Fig. 5e), which, as dis-

cussed above, is the part of the visual field represented in

the region of V2 where there was leakage of neuronal

tracer (see Fig. 5c).

Near-peripheral V6 also received dense projections from

the central densocellular nucleus of the thalamus (Cdc;

Fig. 4d, i), and moderate projections (\10 %) from other

thalamic nuclei (paracentral, PC; LP; ventral anterior pars

magnocellularis, VAmc; mediodorsal, MD; Fig. 4c, d, i).

These projections were not evident in the case of far-

peripheral field injection, suggesting that the peripheral

representation of V6 receives a less diverse set of thalamic

afferents than the central representation of this area.

Thalamic afferents to V6A

Thalamic afferents to V6Ad and V6Av showed a similar

pattern, although in our materials the afferents were gen-

erally sparser after injections in the ventral portion of V6A

(e.g. Fig. 6a, b, f, g). Figure 7 shows a quantitative com-

parison of the thalamic afferents after injections in the two

subdivisions of V6A.

After injections in V6Av, the majority of labelled

cells were located in the LP and PuM nuclei. Fig-

ure 7a shows the quantitative distribution of thalamic

labelled cells in three cases with injections restricted

to V6Av. The thalamic input was similar for the main

cs

ps arsips

pos

ls

sts

pos

ipscs

ps cal

otsios

a

v

V6AdCase A3R

A B

MGpc

VPL PuM

LPVL

VPI

MGpc

VAdcR

bsc

VPL Pul

LP

VL

VPISTN

7,25mm

from Ilinsky & Kultas-Ilinsky, 1987

VLm

VLoX

VLc

Pcn

MD

LGN

cs

ps

ars

ips

cin

posls

sts

lf

ari

pcscs

cinips

lf

sts

ots

m

v

V6AdCase 11L

VLm

GLvo

GLd

+ 9.3mm

MD

Cdc

ADAV

Csl

Can

VLo X

VLc

Pcn

AM

R

from Olszewski, 1952

Fig. 3 Assignment of labelled cells to thalamic nuclei. a Parasagittal

section of the brain taken at the level indicated on the brain silhouette

shown in the middle. The rectangle represents the thalamic region

enlarged on the bottom. Inset from the atlas (Ilinsky and Kultas-

Ilinsky 1987) shows thalamic nuclei at the same approximate level of

the section. Locations of labelled cells are shown as black circles.

b Coronal section of the brain taken at the level indicated on the brain

silhouette shown on the top right. The rectangle represents the

thalamic region enlarged in the centre. An inset from Olszewski atlas

(Olszewski 1952), bottom, shows the thalamic nuclei at the level of

the section. Labelled cells are shown as black dots. m medial. Other

details and abbreviations are as in Figs. 1 and 2 and in the list of

abbreviations

Brain Struct Funct

123

afferents (LP and PuM). Projections from the VL

nucleus were very weak and were found in only one

case (Fig. 7a).

Figure 3a shows the main afferents to V6Ad in a brain

that was cut in the parasagittal plane, while Figs. 6c–e and

3b show the distribution of labelled cells in another case,

which yielded coronal sections. The strongest connection

of V6Ad was with the LP nucleus (Figs. 3a, 6d). The

remaining labelled cells were nearly equally distributed

between the VL (Figs. 3b, 6c, d) and PuM (Fig. 6e) nuclei.

This connection pattern revealed similar afferents from the

LP to those observed in V6Av, but the projection from VL

to V6Ad was stronger than that to V6Av, whereas the

connection between the PuM and V6Ad seemed to be

relatively de-emphasised. The histogram in Fig. 7b shows

the fraction of labelled cells in various thalamic nuclei after

injections in lateral (case 11L, see also Figs. 3b and 6c–e),

central (average of cases A3L and A3R, see also Fig. 3a),

and medial (case A1R) parts of V6Ad (white, grey, dark

columns, respectively). In case 11L (Figs. 6c–e, 3b), we

also observed labelled cells in the MD, Li, Pcn (equivalent

to PC nucleus in the nomenclature of Ilinsky and Kultas-

Ilinsky 1987, see Table 2) and Cdc nuclei. The thalamic

projection patterns of V6Av and V6Ad were further sup-

ported by cases in which the injections sites partially

crossed into adjacent areas (3 cases, Fig. 7c).

Discussion

The aim of this study was to examine the thalamic

afferents to the areas that occupy the rostral bank of the

parieto-occipital sulcus in the caudal-most part of the

superior parietal lobule, namely areas V6 and V6A (the

latter including ventral and dorsal subdivisions). Our

results show that each area receives input from a specific

set of thalamic nuclei. Conversely, several of the labelled

thalamic nuclei send projections to more than one area,

albeit with different strengths. This information is sum-

marised in Fig. 8. The LP nucleus and the pulvinar

complex form the main projections in all cases, although

the connections to V6 and V6Ad/V6Av originate in dif-

ferent subdivisions of the pulvinar complex (PuI/PuL

versus PuM). We detected sparse projections from the

LGN only to V6, whereas V6A (in particular, the dorsal

subdivision) received additional inputs from the VL

nucleus. In addition, V6 and V6Ad received relatively

weak projections from other thalamic nuclei, including

those from the caudal part of the MD nucleus and intra-

laminar complex nuclei.

Overall, these results conform to the expectation that

the thalamo-cortical projections, as a whole, obey a

global topographic order, for example, with rostral

nuclei projecting to rostral areas, and caudal nuclei

projecting to caudal areas (e.g. Hohl-Abrahao and

Creutzfeldt 1991). As shown in Fig. 9, the percentage

of labelled neurons in nuclei located in the caudal third

of the thalamus increases progressively from V6Ad, to

V6Av, to V6. However, no trend is apparent along the

mediolateral dimension. As expected from the previous

literature on posterior occipital and parietal cortices, the

areas we studied mainly receive from the lateral and

posterior parts of the thalamus, (Adams et al. 1997;

Shipp 2003).

Table 2 Correspondence of

nomenclature of the thalamic

nuclei involved in this study

For details see the list of

abbreviations

Ilinsky and Kultas-Ilinsky (1987) Olszewski (1952) Present study

Medial region MDdc MDdc MD

MDmc MDmc

MDpc MDpc

Cdc Cdc Cdc

Li Li Li

Lateral region

Motor Thalamus

VAmc VAmc VAmc

VL Area X VL

VPLo

VLc

VLps

Intralaminar Formation

Anterior Group

PC Pcn PC

CL CL

Posterior region Pul Pul. m PuM

Pul Pul. l PuL

Puli Pul. i PuI

LG GL LGN

Brain Struct Funct

123

V6 near-peripheralCase M17L

V6 far-peripheralCase M17R

D

A

csps

arsips

pos

lssts

lf

A

cal

PuL

PuI

LGN

10,5mm

B

calPuL

PuI

LGN

10mm

VPL

C

MD

VAmc

PCAM

2mm

D

MDCdc

PC

AM

0,3mm

cspsars ips

pos

lssts

lf

GE

V6 near-peripheral

30°

H

60°

V6 far-peripheral

ipsi contra

70°

Cdc MD LP PuL PuI

LGN

0

10

20

30

40

Thalamicafferents to V6

M17L-V6

I

% L

abel

led

thal

amic

cel

ls

PC

VAmc

near-peripheral

11mm

PuL

LGN

E

cal

10mm

PuL

PuI

LGN

VPL

F

cal

8,5mm

PuLVPL

MG

VL

G

cal

Fig. 4 Thalamic afferents to area V6. Four parasagittal sections (a–

d) from case M17L, with V6 injection in the near-peripheral visual

field representation. Three parasagittal sections (e–g) from case

M17R, with V6 injection in the far-peripheral representation. Sections

were taken at the levels indicated on the brain schematics shown on

the bottom. Bottom h Receptive fields of the cells recorded from the

injection sites (central and peripheral visual field representations of

V6) (Galletti et al. 2001). Top i Histogram of the relative percentage

of cells found in the different thalamic nuclei in the case injected in

the near-peripheral visual field representation of V6 (case M17L).

Other details and abbreviations are as in Figs. 1, 2 and 3, and the list

of abbreviations

Brain Struct Funct

123

60°

V2 central

V6 far-peripheral

ipsi contra

70°

halocore

V6

V6AV2

V1

calpom

pos

pn

a

v

V1

C

E10mm

LGN

V6 far-peripheralCase M17R

B10mm

LGN

PuI

V6 near-peripheral

30°

ipsi contra

30°

V6 near-peripheralCase M17L

PuI

PuL

20°

+

−

10°5°

2°

PuI

PuL

+

−

5°

2°

20°10°

2,5°

17°

50°20°10°

5°2°

+

−

from Bender, 1981

from Malpeli & Baker, 1975

csps

arsips

pos

lssts

lf

BA

cspsars

ipspos

lssts

lf

C

E

A

calLGN

10,5mm

10mm

LGN

VPL

D

cal

Brain Struct Funct

123

Possible functional role of thalamic afferents

to the caudal superior parietal lobule

Thalamic afferents to V6 are largely typical of those to a

topographically organised visual area. Thus, major pro-

jections arrive from the two retinotopically organised

regions of the pulvinar complex (lateral and inferior pul-

vinar, respectively; see Fig. 8). The visuotopic organisation

of these two pulvinar regions is well established and it has

been shown that they both project to multiple extrastriate

areas with similar pattern of connections (Bender 1981;

Ungerleider et al. 1984; Shipp 2001; Soares et al. 2001;

Shipp 2003; Kaas and Lyon 2007). In our material, there

was little differentiation between the locations of patches

of labelled neurons from V6 injections in different parts of

the peripheral visual field (\30� versus[30�) in V6. In the

near-peripheral case labelled cells were found in the por-

tions of pulvinar that are congruent with the part of the

visual field included in the injected region of V6 (see

Figs. 4h, 5a). In the far-peripheral case, labelled cells were

found more or less in the same part of the pulvinar.

Although we recognise the difficulty in reaching conclu-

sions based on only two cases, it is possible that the

labelled cells in the same pulvinar region in this case

mainly reflect the low magnification factor in the pulvinar

at peripheral representations, or projections from V2, due

to the tracer leakage in the caudal bank of the parieto-

occipital sulcus. The comparison of our data with receptive

field maps (see Fig. 5a, d) seems reasonably consistent

with the interpretation that afferents to V6 (and/or V2)

originate in both of the two visual maps represented in PuL

and PuI (Bender 1981). In both V6 injection cases, the

more dorsal cluster of labelled cells could have included

the reported location of the vertical meridian representation

which forms the border between the two maps. However,

no firm conclusion can be reached in this respect given

individual variability, and the inexact correspondence

between our data and the parasagittal planes illustrated in

Bender’s (1981) study.

The paucity of projections from the pulvinar to the

topographically appropriate region of V6 in the far-

peripheral case could be a reflection of the marked

emphasis on central visual field representation, in the

pulvinar nuclei, as also apparent in studies of the marmoset

monkey, where injections in the far peripheral representa-

tion of the middle temporal area (MT) resulted in very

small numbers of labelled cells in the pulvinar complex

(Palmer and Rosa 2006). In addition, the same study

reported that injections in the far peripheral representation

of area MT result in label in a more restricted set of cortical

areas, in comparison with injections in the central repre-

sentation. A similar trend was observed in our study, in

which a larger number of thalamic nuclei projected to the

near-peripheral injection site. Finally, it is worth noting

that the PuI region that projects to V6 is adjacent to the

LGN, in the rostral and lateral portion of ventral pulvinar.

This likely overlaps with the region that projects to area

MT (Shipp 2001, 2003; Soares et al. 2001).

The presence of labelled cells in the interlaminar layers

of the LGN after the near-peripheral field injection of V6

represents further evidence that area V6 is primarily a

visual area. The primary visual area was classically con-

sidered the main target of LGN in primates (Hubel and

Wiesel 1972), though there is currently considerable evi-

dence of sparse connections from the LGN to extrastriate

areas (Wong-Riley 1976; Benevento and Yoshida 1981;

Yukie and Iwai 1981; Bullier and Kennedy 1983; Lysa-

kowski et al. 1988; Hernandez-Gonzalez et al. 1994;

Sincich et al. 2004; Warner et al. 2010; Lyon and Rabideau

2012). Present results are in line with this evidence, which

may be important to explain the residual visual function

that remains in cases of cortical blindness after striate

cortex lesions (Schmid et al. 2010; Yu et al. 2013). Notice

that small numbers of neurons in the LGN have been found

in all studied primates after injections in DM (Beck and

Kaas 1998), the New World monkey homologue of area V6

(Rosa and Tweedale 2001), although the labelling was not

consistent, being found in less than half of the studied

cases. Projections from LGN neurons to V6 were also

inconsistent in our study; given that the number of labelled

cells in the LGN is small, these afferents could easily have

been missed due to methodological factors.

b Fig. 5 Distribution of labelled cells in pulvinar and LGN. a Parasag-

ittal section taken at the level of the pulvinar (see the brain silhouette

on the top) showing locations of labelled cells and the corresponding

visuotopic organisation of the pulvinar (modified from Fig. 12 by

Bender 1981). On the right, receptive fields of cells recorded from the

V6 injection site in case M17L (V6 near-peripheral) are reported.

b Parasagittal section taken at the level of the LGN (see the brain

silhouette on the top) showing locations of labelled cells and the

corresponding portion of the visual field represented in that part of the

LGN (modified from Fig. 12 by Malpeli and Baker 1975). On the left,

the insert shows schematically the representation of visual hemifield

with the symbols used by Bender 1981, on the left, and Malpeli and

Baker 1975, on the right. c Reconstruction on a parasagittal brain

section of the injection carried out with the recording syringe in case

M17R (V6 far-peripheral). Notice that there was a leakage of tracer in

the primary and second visual area (V1 and V2; grey areas). On the

right, receptive fields of cells recorded from the V2 region of leakage

and the V6 injection site are reported. pn penetration. d Parasagittal

section taken at pulvinar level (see the brain silhouette at the centre)

showing the locations of labelled cells and the corresponding

visuotopic organisation of the pulvinar (modified from Fig. 12 by

Bender 1981). e Parasagittal section taken at LGN level (see the brain

silhouette at the centre) showing the locations of labelled cells and the

corresponding portion of the visual field represented in that part of

LGN (modified from Fig. 12 by Malpeli and Baker 1975). Other

details and abbreviations are as in Figs. 1, 2 and 3, and the list of

abbreviations

Brain Struct Funct

123

Further input arrived in V6 from the VAmc, MD nucleus

and from the thalamic midline nuclei, in particular from

Cdc, and to a lesser degree, from the intralaminar para-

central nucleus (PC or Pcn). These inputs are similar to

those of DM of the New World monkey brain (Beck and

Kaas 1998; Rosa et al. 2009). To date, few studies have

focused on these thalamic nuclei and their specific

functions are still not completely known (Hsu and Price

2007; Hsu et al. 2014). As suggested by Huerta and Kaas

(1990) for supplementary eye field, area V6 could use the

Cdc afferents to provide visual input for movement guid-

ance, thanks to the connections with skeletomotor-related

areas, such as V6A and MIP, in addition to visual con-

nections with extrastriate cortex (Galletti et al. 2001). A

VPLo

VLc

VPI

PcnMD

C

VPLcLP

VLpsMD

GMpcLGN

D

PuL

MD

SG

PuI

PuM

E

cs

psars

ips

cinpos

ls

lf

ari

E

C

sts

V6AdCase 11L

B

VLVAdc

PuM

CL

CM

VPM

VPL

VPI

A

MGpc

VPL PuM

LPVL

7,25mm + 8,1mm

+ 4,5mm5,2mm

+ 2,1mm

V6AvCase M21R

VL

VAdc

PuM

VPM

VPL

VPI

LP

STN

G6mm

MGpc

VL

PuMVPM

VPL

LP

F6,7mm

V6AvCase A4R

GF posps

ars

csips

sts ls

pos

lsips

sts

cspsars

lf

BA

Fig. 6 Thalamic afferents to

area V6A. Left Injections in

V6Av. a, b Parasagittal sections

from case M21R. Right

Injections in V6Ad. c–e Coronal

sections from case 11L. Bottom

injections in V6Av. f,g Parasagittal sections from case

A4R. Black circles represent

labelled cells after injections of

either CTB red or CTB green,

both within the limits of area

V6Av. Sections were taken at

the levels indicated on the brain

silhouettes shown on the centre.

Other details and abbreviations

are as in Figs. 1, 2 and 3, and

the list of abbreviations

Brain Struct Funct

123

clear topographical organisation of central nuclei has not

been yet described. Schlag and Schlag-Rey (1984) and

Schlag-Rey and Schlag (1984) reported that the neurons of

the central thalamus show visual- and oculomotor-related

properties, while Wyder et al. (2003) have suggested that

the central thalamic nuclei integrate cortical and subcorti-

cal information related to eye movement. The MD nucleus

also seems to be involved in the control of eye movement

(Watanabe and Funahashi 2004), as well as VAmc nucleus,

which corresponds to the nigral input zone (Ilinsky et al.

1985). The pulvinar complex is known to contain neurons

which are modulated by eye position (Robinson et al.

1990). In summary, the present data support the view that

thalamic afferents could be part of the circuit responsible

for the high incidence of gaze modulation observed in V6

(Galletti et al. 1995).

Another aspect worthy of note is the similarity of the

thalamic pattern of connections of the two subdivisions of

V6A, which contrasts with the heterogeneity of their cor-

tico-cortical connections: V6Av is preferentially connected

to visual areas (Passarelli et al. 2011), whereas V6Ad has

preferential connections with other parietal and premotor

areas (Gamberini et al. 2009). An analogous observation

was made by Boussaoud et al. (1992) in the medial superior

temporal area, where the two functionally distinct subre-

gions of the area in terms of central versus peripheral

vision representation showed different cortico-cortical

patterns, but overlapping subcortical connections. Other

parietal areas show label in the same thalamic nuclei (e.g.

pulvinar complex, see Grieve et al. 2000), perhaps hinting

at a more general role of the thalamic circuit to caudal

MF2L V6Av/V6Ad inj

0

10

20

30

40

50

60

70

80

LGNCdc PC VL LP PuL PuI

Thalamic afferents in cases withinjections involving nearby areasC

% L

abel

led

thal

amic

cel

ls

M18L V6Ad/V6Av inj, V2 leakageMF1L V6Av/V6 inj

PuM

Thalamic afferents to V6Av

0

10

20

30

40

50

60

70

80

VL LP

A4aRA4bR

PuM

A

% L

abel

led

thal

amic

cel

ls M21R

Thalamic afferents to V6Ad

LPMD PC VL MuPcdC

11L

A3R & A3L

A1R

0

10

20

30

40

50

60

70

80B

% L

abel

led

thal

amic

cel

ls

Li

Fig. 7 Thalamic afferents to areas V6Av and V6Ad. a Thalamic

afferents to V6Av in cases A4aR, A4bR and M21R. b Thalamic

afferences from cases with lateral (case 11L), central (cases A3R and

A3L) and mesial (A1R) injections in V6Ad. c Thalamic afferents

from three cases M18L, MF1L and MF2L with injection sites

partially crossed into adjacent areas. In all cases, only labelling that

represented [1 % of the thalamic afferents is reported. For other

details see the list of abbreviations

VAmc VLPC LP IuPcdC PuL LGN

V6V6AvV6Ad

0

10

20

30

40

50

60

70

80

% L

abel

led

thal

amic

cel

ls

Thalamic afferents to

MD PuM

Fig. 8 Summary of the thalamic afferents to areas V6, V6Av, and

V6Ad. Average percentages of labelled cells in thalamic nuclei after

tracer injections in V6, V6Av, and V6Ad. Vertical bar SD. For area

V6, only the case M17L (near-peripheral injection) is reported

because in the other case the injected tracer was not restricted to area

V6. Only labelling that represented[1 % of the thalamic afferents are

reported. Other details and abbreviations as for Fig. 7

Brain Struct Funct

123

parietal areas in multimodal/sensorimotor integration. Our

recent work (Gamberini et al. 2011) has suggested that

V6Ad and V6Av have different functional emphases, but

are likely to work together as a single functional entity,

thereby presenting a sensory-motor gradient without sharp

segregation. The overlapping thalamic input to these V6A

territories highlights a possible common functional multi-

modal/sensorimotor role, such that they could be consid-

ered as a single functional area (Gamberini et al. 2011).

Strong thalamic projections to both subdivisions of area

V6A originated in the LP nucleus. It is believed that LP

provides information on somatic and attentional stimuli for

guiding motor acts towards targets of interest. In the rat, LP

is a key node in circuits involved in mediating directed

attention (Kamishina et al. 2008, 2009). In cats trained to

perform a reaching movement toward a moving target spot,

lesions localised in LP severely disrupt accuracy and reac-

tion time (Fabre-Thorpe and Levesque 1991). V6A could

make use of different visual and somatosensory stimuli, as

well as attentional signals, for guiding intentional motor

acts. In this regard, it is worth noting that the activity of

V6A neurons can be modulated by both visual and

somatosensory stimuli (Breveglieri et al. 2002; Gamberini

et al. 2011), by prehension acts (Fattori et al. 2001, 2004,

2010; Gamberini et al. 2011), and by directional shifts of

attention (Galletti et al. 2010). The present data suggest that

these neuronal activities may derive from modulating sig-

nals that could reach V6A through LP afferents.

Area V6A also receives input from the PuM nucleus.

The pulvinar complex is traditionally subdivided into

medial, lateral, inferior, and anterior nuclei (Olszewski

1952). The medial subdivision is connected with the cin-

gulate, posterior parietal and prefrontal cortices (for a

review, Grieve et al. 2000; Saalmann and Kastner 2009).

Whereas PuL is considered to be a visual nucleus, PuM is

viewed as a multimodal, associative nucleus (Ma et al.

1998). Several lines of evidence suggest that PuM is a

subcortical component of the brain attentional network

(Shipp 2003) and, accordingly, it has been reported that

lesions to this thalamic nucleus result in deficits of spatial

attention and neglect (Karnath et al. 2002). This attentional

role of the PuM agrees well with the strong influence of

attention reported in area V6A in monkeys and humans

(Galletti et al. 2010; Ciavarro et al. 2013).

Area V6A receives important input from the VL com-

plex, which is regarded as having a primarily motor

function, sending fibres to the primary and secondary

motor areas (Ilinsky and Kultas-Ilinsky 2002; Kultas-Ilin-

sky et al. 2003; Burman et al. 2014). The strong input from

VL to V6Ad is in line with the proposed involvement of

V6Ad in the on-line control of motor acts (Gamberini et al.

2011).

Finally, minor inputs from the intralaminar and MD

nuclei were found after V6Av injections. The eye-related

neuronal activities that arise from these nuclei (Schlag and

Schlag-Rey 1984; Schlag-Rey and Schlag 1984; Wyder

et al. 2003; Watanabe and Funahashi 2004) agree well with

the functional properties found in visuomotor area V6A

(Galletti et al. 1995; Kutz et al. 2003; Hadjidimitrakis et al.

2011; Breveglieri et al. 2012), suggesting that this area

plays a critical role in the control of eye- and hand-

movements during the preparation and the execution of

lateral

medial

rost

ral

caud

al

CORTEX(left hemisphere)

Thalamic afferents

0

10

20

30

40

50

60

70

80

90

rostral central caudal medial lateral

V6Ad

V6Av

V6

% L

abel

led

thal

amic

cel

ls

medial

lateral

rost

ral

caud

al

late

ral

med

ial

rostral

caudalTHALAMUS(left hemisphere)

Fig. 9 Gradients of thalamo-cortical afferents along the rostrocaudal

and mediolateral axes of the thalamus. Top Dorsal view of the left

hemisphere of a reference monkey brain (http://www.nitrc.org/

projects/caret/, Van Essen et al. 2001) and schematic representation

of the left thalamus. Note that the cortex is linked to the thalamus so

that the one (represented as a two-dimensional reconstruction of the

dorsal portion of the brain) forms a mirror image of the other with the

cortex turned 90� anticlockwise relative to the thalamus. Bottom

average percentages of labelled cells in topographical portions of the

thalamus, irrespective of nuclear thalamic boundaries, after tracer

injections in V6, V6Av, and V6Ad. Rostrocaudal axis of the thalamus

is represented in green, mediolateral one in red. Only labelling that

represented[1 % of the thalamic afferents are reported. Other details

and abbreviations as for Figs. 1 and 7

Brain Struct Funct

123

actions focused on exploration of the world around us

(Galletti et al. 2003).

Concluding remarks

Thalamic afferents to the areas of the rostral bank of the

parieto-occipital sulcus in the caudal part of the superior

parietal lobule are in line with the functional roles sug-

gested for these areas by a large series of electrophysio-

logical experiments carried out on behaving animals, that

is, a visual role for area V6 (Galletti et al. 1999a, 2005),

and an associative and visuomotor role for area V6A

(Gamberini et al. 2011). The similarity of inputs to V6Ad

and V6Av further reinforces the view that these are best

regarded as subdivisions of the same cortical area. Tha-

lamic afferents may contribute to the integration of visual,

somatosensory, attentional, and premotor information

needed for the guidance of motor acts.

Acknowledgments The authors wish to thank M. Verdosci, F.

Campisi and G. Placenti for the technical assistance, and R. Tweedale

for corrections to the manuscript. This research was supported by

European Union Grant FP7-PEOPLE-2011-IOF 300452, National

Health and Medical Research Council, grants 1020839 and 1082144,

Australian Research Council grant DP140101968, and by Ministero

dell’Universita e della Ricerca and Fondazione del Monte di Bologna

e Ravenna, Italy.

Conflict of interest The authors declare that they have no conflict

of interest.

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