Download The medial parietal occipital areas in the macaque

Visual Neuroscience (2015), 32, e013, 13 pages.
Copyright © Cambridge University Press, 2015 0952-5238/15
doi:10.1017/S0952523815000103
SPECIAL COLLECTION
Controversial Issues in
Visual Cortex Mapping
REVIEW ARTICLE
The medial parietal occipital areas in the macaque monkey
MICHELA GAMBERINI, PATRIZIA FATTORI, and CLAUDIO GALLETTI
Department of Pharmacy and Biotechnology, University of Bologna, 40126 Bologna, Italy
(Received October 23, 2014; Accepted March 13, 2015)
Abstract
The number, location, extent, and functional properties of the cortical areas that occupy the medial parieto-occipital
cortex (mPOC) have been, and still is, a matter of scientific debate. The mPOC is a convoluted region of the brain
that presents a high level of individual variability, and the fact that many areas of mPOC are located within very
deep sulci further limits the possibility to investigate their anatomo-functional properties. In the present review, we
summarize the location and extent of mPOC areas in the macaque brain as obtained by architectural, connectional,
and functional data. The different approaches lead to a subdivision of mPOC that includes areas V2, V3, V6, V6Av,
and V6Ad. Extrastriate areas V2 and V3 occupy the posterior wall of the parieto-occipital sulcus (POs). The fundus
of POs and the ventralmost part of the anterior wall of the sulcus are occupied by a retinotopically organized visual
area, called V6, which represents the contralateral part of the visual field and emphasizes its periphery. The remaining
part of the anterior wall of POs is occupied by two areas, V6Av and V6Ad, which contain visual as well as arm
reaching neurons. Our analyses suggest that areas V6 and V6Av, together, occupy the cortical territory previously
described as area PO. Functionally, area V6 is a motion area particularly sensitive to the real motion of objects in
the animal's field of view, while V6Av and V6Ad are visuomotor areas likely involved in the visual guidance of arm
movement and object prehension.
Keywords: Medial posterior parietal cortex, Extrastriate cortex, Retinotopy, Neuroanatomy, area V6, area V6A,
Dorso-medial visual stream
(POs). This is a rather convoluted region that has always presented
difficulties of interpretation in anatomical studies because it shows
architectural distortions in any plane of section, making it difficult
to recognize consistent cytoarchitectonic parcellations.
The pioneering cytoarchitectural studies of Brodmann (1909)
at the beginning of last century described in the Cercopithecus
a clear subdivision between the cortex of the occipital and parietal lobes. According to Brodmann (1909), the parieto-occipital
cortex, located at the border between parietal and occipital lobes,
is occupied by two areas, 18 and 19 (colored regions in Fig. 1,
left). In the medial part of the parieto-occipital cortex, that is, in
the cortex hidden within the POs, area 18 occupies the posterior
bank of the sulcus and area 19 the anterior bank. Looking at the
mesial surface of the hemisphere (left, bottom part of Fig. 1),
this dichotomy is clearly visible, with area 18 located posteriorly,
in the cuneate cortex, and area 19 anteriorly, in the precuneate
cortex.
Forty years later, another seminal cytoarchitectural study described
the mPOC areas in Macaca (von Bonin & Bailey, 1947). Von Bonin
and Bailey re-named areas 17, 18, and 19 as areas OC, OB, and
OA, respectively, while changing the proposed location of their borders slightly (Fig. 1, right). In the mPOC in particular, the territory
of area OB was expanded, occupying a larger part of the mesial
surface of the hemisphere (see the right, bottom part of Fig. 1).
The areas of the medial parieto-occipital cortex (mPOC) have
been extensively explored in anatomical and physiological studies,
but their location, extent, and in some cases also their existence
are still rather controversial in different species of primates.
Methodological factors such as location within very deep sulci,
which renders extensive sampling difficult, and the use of different criteria for parcellation have contributed to this disagreement. The aim of this review is to present the current view of the
areal subdivision of mPOC obtained by using cyto- and myeloarchitectural analysis, as well as analysis of neuro-anatomical
connections and neuronal properties studied in anesthetized and
awake, behaving monkeys.
The mPOC
The superior parietal lobule (SPL) in the primate brain occupies the
medial part of the parietal lobe (Fig. 1, top). In the caudal part of
SPL, between parietal and occipital lobes, there is a large region
of cortex, the mPOC, hidden within the parieto-occipital sulcus
Address correspondence to: Prof. Claudio Galletti, Department of
Pharmacy and Biotechnology, Piazza di Porta S. Donato, 2, 40126 Bologna,
Italy. E-mail: [email protected]
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Fig. 1. Brain location of the parietal occipital cortex. Top, posterior view of macaque brain (Macaca fascicularis). SPL: superior parietal
lobule; IPL: inferior parietal lobule; IPs: intraparietal sulcus; Ls: lunate sulcus; POs: parieto-occipital sulcus; STs: superior temporal sulcus;
Lf: lateral fissure; Cs: central sulcus; and Cal: calcarine fissure. Bottom, parcellations of the monkey mPOC based on cytoarchitecture in
Cercopithecus by Brodmann (1909) and in Macaca by von Bonin and Bailey (1947). Dashed lines limit the region of interest, areas
18 and OB are indicated in red, areas 19 and OA in green.
A detailed analysis of the coronal slices reported in that study
showed that area OB occupied not only the posterior bank of the POs,
but also the fundus and the ventralmost part of the anterior bank of
the sulcus (see the right, bottom part of Fig. 1 and the cortical
region indicated by the arrow in the right part of Fig. 2), whereas
area OA occupied most of the remaining dorsal portion of the
anterior bank of POs (Fig. 2, right; see also the medial view of the
hemisphere in the bottom part of Fig. 1, right).
Later, functional studies partly confirmed and partly modified the areal subdivisions proposed by Brodmann and by von
Bonin and Bailey. Area 17, or OC, was recognized as a single
area also from the functional point of view and was named area
The macaque medial parieto-occipital cortex
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Fig. 2. Cytoarchitectonic parcellation of the parietal occipital cortex. Left,
mesial view of Macaca brain by von Bonin and Bailey (1947). The oblique
lines indicate the level of many near-coronal sections. Right, a section taken
at the level of the parieto-occipital cortex, just anterior to the parieto-occipital
sulcus. Gray area highlights the region of interest. Abbreviations: SPs:
subparietal sulcus; IOs: inferior occipital sulcus; OTs: occipito-temporal
sulcus; POm, medial parieto-occipital sulcus; and Cin: cingulate sulcus.
Other details are as in Fig. 1.
V1 (primary visual area) (Daniel & Whitteridge, 1961; Van Essen
et al., 1984). Areas 18/OB and 19/OA, instead, were functionally
subdivided into different areas. Regarding the mPOC, which is
the target of our review, area 18/OB was subdivided into two
areas, named V2 and V3 (Zeki, 1969; Zeki, 1977; Van Essen &
Zeki, 1978; Gattass et al., 1981; Gattass et al., 1988), whereas area
19/OA was initially considered as a single functional area named
PO that occupied the entire anterior bank of POs (Gattass et al.,
1985) (Fig. 3A and 3B).
Areas of the posterior bank of the parieto-occipital sulcus
Areas V2 and V3
Many functional studies have reported the presence of two retinotopically organized visual areas, V2 and V3, in the posterior
bank of the lunate and parieto-occipital sulci of the macaque
(Zeki, 1977; Van Essen & Zeki, 1978; Gattass et al., 1981; Gattass
et al., 1988). According to Gattass et al. (1981, 1988), the parts
of these areas located in the posterior bank of the lunate sulcus
represent the central 10° of the contralateral lower visual field
(see Fig. 4A and 4C) and those located in the posterior bank
of the POs, the periphery of the contralateral lower visual field
(see Fig. 4B and 4C). In both lunate and POs, area V2 borders
on the primary visual cortex (V1) dorsally, where the vertical
meridian is represented, and on V3 ventrally, where the horizontal
meridian is represented (Fig. 4C). The representation in the
anterior border of V3 is less clearly defined in that the vertical
meridian is reported to be represented only in a small part of the
medial extent of the area (see Fig. 4C). The upper visual fields
of V2 and V3 are represented in the ventral part of the brain,
below the level of the calcarine sulcus (Gattass et al., 1981;
Gattass et al., 1988). Van Essen and co-workers (Van Essen et al.,
1986; Felleman & Van Essen, 1987; Felleman et al., 1997) considered the ventral part of V3 as a different cortical area, that
Fig. 3. Brain location of the areas of the parieto-occipital cortex. (A and B)
Mesial and dorsal views of monkey brain with POs, IPs, Ls, STs, IOs, and
OTs partially opened (see gray regions to the right) to show the areas of the
parieto-occipital cortex based on the study of Gattass et al., 1985. (C and D)
Mesial and dorsal views of monkey brain with POs, IPs, and Ls partially
opened to show the areas of the parieto-occipital cortex based on the study
of Colby et al., 1988. (E and F) Enlargements of mesial and dorsal views of
monkey brain shown in C and D with the parcellation of the monkey mPOC
based on the study of Galletti et al. (2003, 2005). Gratings and colored
areas limit the region of interest. The “minus” and the ‘plus’ signs indicate
the lower and the upper visual field representations. Other details are as in
Figs. 1 and 2.
they called VP, because this cortical region, contrary to the dorsal
V3, was not directly connected with V1 and showed a different
pattern of myeloarchitecture as well as of callosal and intrahemispheric connections. These authors suggested that area V3 was
restricted to the dorsal half of the brain and lacked a complete
representation of the visual field.
A series of electrophysiological experiments carried out in
awake macaque monkeys in our laboratory allowed a detailed
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Fig. 4. Retinotopic organization of areas V2 and V3. (A) Lateral view of monkey brain with POs, IPs, Ls, STs, and IOs partially opened.
(B) Mesial view of monkey brain with POs, IOs, and OTs partially opened. Lateral and mesial views show the retinotopic organization
of V2 and V3 in lunate and parieto-occipital sulci, respectively. Gray area in A represents the most central part of the visual field.
(C) Bidimensional map of the parieto-occipital cortex, showing in particular the retinotopic organization of areas V2 and V3. The dashed
lines are isoeccentricity lines. Black circles and white squares indicate the representation of the VM and HM meridians, respectively;
triangles indicate the periphery of the visual field; the anterior border of V3 (stars) corresponds to the region of the visual field shown
with stars in the representation of the contralateral hemifield represented between A and B (modified from Gattass et al., 1981, 1988).
Other details are as in Figs. 1–3.
description of the visual topography of the cortex hidden within the
mPOC (Galletti et al., 1999a; Galletti et al., 1999b; Galletti et al.,
2005). In the posterior bank of the POs, we recognized V2 and
V3 as two strips of cortex which, in agreement with the literature
(see Fig. 4B and 4C), represented the lower contralateral visual
field at eccentricities <30°. According to Gattass and co-workers
(Gattass et al., 1981), V2 continued on the mesial surface of the
occipital lobe and on the upper branch of the calcarine stem, representing progressively higher eccentricities up to the far periphery
(60–70°). Area V3, instead, stopped at the medial margin of the
POs, as previously reported by Gattass and co-workers (Figs. 3B
and 4B) (Gattass et al., 1988).
Fig. 5 shows some examples of the mapping studies that
allowed us to achieve the conclusions reported above. Fig. 5A
shows a very medial parasagittal section of the brain, taken a
few mm from the midline. Here, V2 occupies the posterior bank
and fundus of POs, the ventral convexity of the brain, and the
upper branch of the calcarine sulcus. Receptive field at recording
site 1, near V1/V2 border, is near the vertical meridian. Moving
from recording site 1 to recording site 7, the receptive fields first
approach and then touch the horizontal meridian at the border
with area V6. As the recording sites move caudally along the
ventral convexity of the brain (sites 7–11), the sequence reverses
toward the vertical meridian (V1/V2 border in the upper branch
of the calcarine stem). A similar sequence is observed in the
ventral convexity of the brain in section B, taken some mm more
lateral than section A (Fig. 5B). Here, again, the receptive fields
at sites 9–12 move away from the horizontal meridian going
caudally along the ventral convexity. In the dorsal part of POs,
the receptive fields of V2 move from the vertical meridian (site 1,
at the border with V1) to the horizontal meridian (site 4). Passing
from site 4 to site 5, there is a sudden increase in receptive field
size. Since the two sites were recorded in the same penetration
and the receptive fields were located at the same eccentricity on
the horizontal meridian, this is likely the border between the
areas V2 and V3. This view is supported by the fact that in the
ventralmost part of the posterior bank of POs the receptive
fields remain larger than those of V2 at about the same location
and eccentricity (compare site 4 with sites 5–8). It is worthwhile to note that at the border between V6 and V2–V3 there
is always a representation of the horizontal meridian (Fig. 5A
and 5B).
Section C is taken at the lateral end of POs (Fig. 5C). Here, the
V2–V3 border is located halfway in the posterior bank of POs,
where the horizontal meridian is represented (sites 3/4). When V3
approaches V6 in the fundus of POs, the receptive fields approach
the vertical meridian at progressively increasing eccentricities
(sites 6 and 7). In the ventral part of the posterior bank of POs,
V3 is located posteriorly (sites from 4 to 7), as in section B, and
V6 merges with V3 anteriorly (sites from 8 to 11). At the V3–V6
border, there is a horizontal meridian representation dorsally (sites
4–8), at about 15° of eccentricity, and a vertical meridian ventrally,
in the fundus of POs (sites 6 and 7), at about 30° of eccentricity.
Note that, given their particular arrangement (see Fig. 5C), both
V3 and V6 span from horizontal to vertical meridian representation, and both border V2 at the level of horizontal meridian
representation.
Fig. 5D summarizes the data from four cases. It shows that
within the POs the lateral part of V3, near lunate sulcus–POs
junction, mainly represents the vertical meridian and nearby regions
of the lower contralateral visual field up to eccentricities of about
30° (C6, C7). In contrast, the medial part of V3, near the interhemispheric midline, mainly represents the horizontal meridian and
nearby regions, again up to about 30° of eccentricity (B5–B8). Our
data well agree with those of Gattass et al., (1988), who reported
that the anterior border of V3 represents the vertical meridian only
in a small part of the medial extent of the area, where the lunate
sulcus joins the POs (see Fig. 4C).
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The macaque medial parieto-occipital cortex
and 3D) (Gattass et al., 1986; Colby et al., 1988). According to this
view, the horizontal meridian representation ran vertically along
the medial part of the anterior bank of POs (Fig. 3C and 3D).
Although the upper and lower field representations were found to be
spatially segregated, area PO showed a complex visual topography
without a point-to-point retinotopic organization, or a clear central
to peripheral trend within the area.
Areas V6 and V6A
Fig. 5. Visual topography of the medial part of area V3. (A, B, and C) Three
parasagittal sections are shown on the left, taken at the levels indicated on
the brain silhouettes reported between them. Crosses, open circles, and plus
on the sections indicate recording sites in V1, V2/V3, and V6, respectively;
the receptive fields mapped at these recording sites are shown on the right.
The part of area V3 located in the POs is colored in green. V3 receptive
fields are colored accordingly. Dashed lines on sections mark the limits
between different cortical areas. (D) Visual field representation of the part
of V3 located in POs (green). The colored region was obtained by outlining the
external borders of superimposed receptive fields of V3 neurons recorded
from four different cases. Some of the receptive fields reported in B and C
are here outlined (the letter refers to the section where that receptive field
belongs to, and the number indicates the number of receptive fields selected
in the corresponding section). White squares and black circles represent
the center of receptive fields located, respectively, in the vicinity of the
horizontal and vertical meridians. Other details are as in Figs. 1–4.
Areas of the anterior bank of the parieto-occipital sulcus
It is well known that the definition of areas is a process of constant
refinement, and in many cases larger areas become gradually subdivided into smaller areas as the anatomical and physiological
knowledge progresses. In line with this typical process, the area
PO, that was at first reported to occupy the whole anterior bank of
the macaque POs (Gattass et al., 1985) (Fig. 3A and 3B), some
years later was redefined as a smaller region, corresponding to the
ventral part of the original PO (Fig. 3C and 3D). The re-defined
PO only represented the periphery of the contralateral visual field
beyond 20° of eccentricity, with the lower quadrant in the ventral part
of the anterior wall of POs and the upper quadrant in the ventrocaudal
precuneate cortex, on the mesial surface of the hemisphere (Fig. 3C
The history of areas V6 and V6A, like that of area PO, also reflects
a process of refinement whereby large areas become subdivided
into smaller ones. The term “V6” was first introduced by Zeki
(1986) to describe a visual cortical region delimited by strong callosal connections, which occupied almost the entire anterior bank
of the POs, thus overlapping considerably with the original PO
of Gattass et al., 1985. A few years later, Galletti et al. (1991),
recording from the same region in alert behaving monkeys, found
a dorsal region containing visual and nonvisual cells and a ventral
region containing only visual neurons. These results were reminiscent
of those previously reported on anesthetized monkeys that described
a visual area PO in the ventral part of the anterior bank of POs and
a region less sensitive to the visual stimulation dorsal to it (Colby
et al., 1988). Following electrophysiological studies carried out in
awake macaque monkeys confirmed that the anterior bank of the
POs contains two functionally distinct areas: a ventral one, that
was named V6, and a dorsal one, named V6A (Fig. 3E and 3F)
(Galletti et al., 1996; Galletti et al., 1999a; Galletti et al., 1999b;
reviewed in Galletti et al., 2003).
V6 is a visual motion area whose neurons are very sensitive
to the direction, orientation, and speed of motion (Galletti et al.,
1996) and to the real movement of objects in the visual space
(Galletti & Fattori, 2003). It is also an area that emphasizes the
representation of the periphery of the visual field (Galletti et al.,
1999a). At first glance, area V6 seems to correspond to the revised
area PO of Colby et al., 1988. However, a more careful comparison
suggested that this is unlikely to be the case (Galletti et al., 2005).
While PO was reported to represent only eccentricities higher than
20–30° and to contain a complex visuotopic map (Neuenschwander
et al., 1994; Colby et al., 1988), V6 contains a point-to-point complete representation of the contralateral visual field, including the
central 20° but with an over-representation of the visual field
periphery (Galletti et al., 1999a). Also the location and extent of V6
do not exactly match those proposed for area PO (Fig. 3E and 3F)
(Galletti et al., 2005). As shown in Fig. 6A–6C, area V6 (yellow
region), if seen in a coronal plane (Fig. 6B), occupies a “C”-shaped
belt of cortex whose upper branch is located within the POs and the
lower one within the medial parieto-occipital sulcus (POm), with
the mesial surface of the brain as a junction zone between the two.
The lower visual field is represented dorsally, in the ventral part
of the anterior bank of POs (Fig. 6E), while the upper visual field
is represented ventrally, in the dorsal bank of POm (Fig. 6D). Also
area PO occupies a “C”-shaped belt of cortex (Fig. 3C and 3D), but
in PO the “C” is horizontally, instead of coronally, displaced with
the lower visual field represented laterally, within the POs, and
the upper visual field medially, on the mesial surface of the brain
(Colby et al., 1988). It is worthwhile to note that area PO, in contrast to V6, was not reported to include the cortex hidden within the
POm (see Fig. 3C), although the inspection of sections reported by
Colby and colleagues clearly shows that PO involved also the POm
(see Figs. 2 and 3 of Colby et al., 1988). It results that the upper
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Gamberini et al.
Fig. 6. Brain location of areas V6, V6Av, V6Ad, and visual topography of V6 on 3D reconstruction of the brain. (A and C)
Topographical arrangement of areas V6, V6Av, and V6Ad along the anterior bank of POs in medial (A) and dorsal (C) views of
a macaque right hemisphere. Area V6 is represented in yellow, V6Av in blue, and V6Ad in pink. (B) 3D reconstructions of the
caudalmost part of the SPL obtained from coronal sections. The part of SPL shown in B is that within the parallelepiped in A. In
B, the occipital pole is cut away to show the anterior bank of the POs. Dorsal is up and mesial is on the left. (D and E) Mesial view
and enlargement of a dorsal view of the brain of a macaque right hemisphere to respectively visualize the lower and upper field
representation of area V6 in POm (D), and the lower field representation of area V6 in POs (E). White, orange, and red indicate
the eccentricities represented in different parts of V6 according to the color coding shown in the middle. White squares and black
circles represent the horizontal (HM) and vertical (VM) meridians of area V6, respectively; (F) center of gaze (modified from
Galletti et al., 1999a; Pitzalis et al., 2013). Abbreviations: ARs: arcuate sulcus; Ps: principal sulcus; a: anterior; v: ventral; m: medial.
Other details are as in Figs. 1–4.
field representation in PO is located on the exposed mesial surface of
the hemisphere (Colby et al., 1988), with the horizontal meridian
representation running vertically along the anterior bank of POs
(Fig. 3D). In contrast, the upper field representation of V6 is mostly
hidden within the POm (Fig. 6D).
As described in detail by Galletti and co-authors (Galletti et al.,
1999a), most of the extent of V6 is devoted to the representation
of the periphery of the visual field, the lower quadrant in the
ventralmost part of the anterior bank of POs (Fig. 6E), and the
mesial surface of the hemisphere (Fig. 6D), the upper quadrant
mainly in the upper branch of POm (Fig. 6D). Moving laterally
within the POs, the V6 moves down from the anterior bank to
the fundus of POs, and then up along the posterior bank of POs
where it merges with the cortex of area V3 (Figs. 5C and 6E).
This part of V6, representing the central 20–30° of the lower visual
field (Galletti et al., 1999a), was originally not attributed to PO
(Colby et al., 1988; see Galletti et al., 2005). Area V6 represents
the horizontal meridian posteriorly and the vertical meridian
anteriorly (Fig. 6E). As shown in the top part of Fig. 7, the receptive field size in V6 increases with eccentricity, as it is usual in visual
areas.
Area V6 is the target of strong projections directly from V1
(Galletti et al., 2001), with projecting cells mainly confined
within layer 4B (Fig. 8A, see panels “a” and “b”). Layer 4B cells
are known to receive from layer 4Cα, which in turn directly
receives a magnocellular input from the lateral geniculate nucleus (Lund et al., 1975). This input could be responsible for the
strong orientation and motion direction selectivity observed in
V6 (Galletti et al., 1996). About half of the cortical inputs to V6
comes from the visual areas of the occipital lobe (V1, V2, V3,
and V3A), the other half from the parietal areas of the ‘dorsal
visual stream’: 30% from visual areas of the dorso-lateral visual
stream (V4T, MT/V5, MST, and LIPv) and the remaining 20%
from bimodal sensory (visual and somatosensory) areas of the
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An area very similar to V6, called dorso-medial area (DM), is also
present in the medial parieto-occipital region of the New World
monkeys (Rosa & Tweedale, 2001). Similar to macaque V6, DM
has a point-to point retinotopic representation of the contralateral
visual field, with the horizontal meridian located posteriorly and
the vertical meridian anteriorly, and the most peripheral part of the
upper quadrant on the medial surface of the hemisphere. DM, as
V6 (Galletti et al., 1996; Galletti & Fattori, 2003), contains many
orientation- and direction-selective cells (Baker et al., 1981; Rosa &
Schmid, 1995). Moreover, area DM shows a pattern of cortical
connections very similar to that of area V6 (Krubitzer & Kaas,
1993; Beck & Kaas, 1999; Rosa & Tweedale, 2000; Rosa et al.,
2009).
Areas V6Av and V6Ad
Fig. 7. Receptive-field size versus. eccentricity in the areas of the mPOC,
and visual field representation in areas V6Av and V6Ad. Top, regression
lines representing the receptive field size versus eccentricity in areas, V6
(466 cells), V6Av (586 cells), and V6Ad (325 cells). ANCOVA analysis
established that the two regression lines of areas V6Av and V6Ad were
significantly different in slope (F905 = 14.73; P < 0.0001) and in elevation
(F905 = 49.23; P < 0.0001). Bottom, density maps of receptive-field
distribution in areas V6Av and V6Ad. Color scale indicates the relative
density of receptive fields covering that specific part of the visual field. In
the white region, 140 (V6Av) and 120 (V6Ad) RFs are superimposed in the
same grid square.
dorso-medial visual stream (V6Av, MIP, and VIP; see Fig. 8B)
(Galletti et al., 2001). Area V6 is not directly connected with the
“ventral visual stream” or with the mesial and frontal cortices.
It has been suggested that V6 transfers visual information relative to form and motion to parietal and frontal cortices involved
in a visual guidance of action (Galletti et al., 2001). In fact, V6
is directly connected with area V6Av (Passarelli et al., 2011),
which in turn sends strong projections to area V6Ad (Gamberini
et al., 2009) (see Fig. 8B), and it is well known that both V6Ad
and the dorsal premotor cortex, that receives directly from
V6Ad (Gamberini et al., 2009) (see Fig. 8B), are involved in the
visual guidance of arm reaching movements and objects
grasping (Caminiti et al., 1991; Raos et al., 2004; Fattori et al.,
2005; Bosco et al., 2010; Fattori et al., 2010; Gamberini et al.,
2011).
Area V6 has also been recognized in the human brain
(Pitzalis et al., 2006). Human V6, like macaque V6, is a retinotopically organized visual motion area that represents the contralateral visual field and emphasizes the periphery of the visual
field. As in the macaque, human V6 is located in the POs and the
relationships with neighboring areas are almost the same in the
two species (see Fig. 9). In human, like in macaque, V6 abuts on
area V6Av anteriorly, V2 posteriorly, and V3/V3A laterally.
Details on brain location, functional organization, and properties of human V6 are fully described in the study by Pitzalis
et al. in this issue.
As reported above, electrophysiological studies on awake animals provided evidence that dorsal to V6, in the anterior bank of
POs, there was a visuomor area called V6A (Fig. 3E and 3F)
(Galletti et al., 1996). In a recent study of Luppino et al., 2005,
the cyto- and myeloarchitecture of mPOC were analyzed in
detail using coronal, horizontal, and parasagittal planes of section. This study allowed the recognition of different types of
cortex in this convoluted part of the brain (see Fig. 10A and
10B). It was reported that the whole posterior wall of POs, the
fundus of the sulcus, and the ventralmost part of the anterior
wall of POs contained cortex of occipital type (thick and homogeneous layer IV, light layer V), whereas the dorsal part of the
anterior wall of POs was occupied by cortex of parietal type
(well developed layers III and V, layer IV subdivided into two
sublayers), exactly as described by von Bonin and Bailey (1947)
(see Fig. 1, right; Fig. 2). A comparison between cyto- and myeloarchitecture of the anterior wall of the POs revealed that V6
matched the most strongly myelinated region in the ventralmost
part of the anterior bank of POs. However, it was clear that the
strong myelination continued anterior to the V6 border, overlapping also area V6Av (Fig. 10B). These data suggest that the
strongly myelinated region called area PO (see Fig. 10C) (Colby
et al., 1988) includes areas V6 and V6Av (compare Fig. 10B and
10C) (Luppino et al., 2005). This hypothesis is supported by the
fact that PO was reported to have a complex visual topography,
as predicted by the inclusion in PO of the retinotopically organized V6 and the nonretinotopically organized V6Av (Galletti et al.,
2005; Luppino et al., 2005). Further support comes from a comparison of the anatomical connections of PO and areas V6/
V6Av. Apart from the shared connections, PO was reported to
be directly connected with areas PGm, 7a, and PMd (Colby et
al., 1988) whereas V6 was not connected with these areas
(Galletti et al., 2001), but V6Av was connected with them
(Passarelli et al., 2011) (see Fig. 8B). It is therefore plausible
that the connections with areas PGm, 7a, and PMd observed
after PO injections are due to inclusion of area V6Av in the injection sites.
As shown in Fig. 6A and 6B, V6Av and V6Ad are two
concentric belts of cortex (blue and pink regions, respectively)
that encircle dorsally and anteriorly area V6. Hodological data
showed that V6Av and V6Ad have distinct connectional patterns
(Fig. 8B) (Gamberini et al., 2009; Passarelli et al., 2011). Area
V6Av receives strong inputs from visual- (V2, V3, V4, V6, and
MST) and parietal- (PGm, V6Ad, and MIP) areas. Area V6Ad
receives visual inputs from MST and V6Av, and other inputs from
8
Gamberini et al.
Fig. 8. Laminar pattern of labeling in V1 after V6 tracer injection, and summary of connections of areas V6, V6Av, and V6Ad.
(A) Caudal part of a parasagittal section taken at the level indicated on the brain silhouette at the bottom. Each single dot represents a
retrogradely labeled cell. (a) Inset showing an enlargement of a part of the posterior branch of Cal (squared area on the section). Yellow
triangles are single retrogradely labeled cells. Numbers and letters indicate the cortical layers. (b) Dark-field photomicrograph of
the squared region of Cal cortex shown on the section, containing transported labeled materials after V6 injection. Scale bar, 1 mm.
(B) Summary of connections of areas V6, V6Av, and V6Ad. The boxes representing different areas are organized approximately in a
caudal to rostral sequence, from the bottom part of the figure to the top. The proportion of neurons forming each connection is indicated
by the thickness of the bars linking different areas. Cortico-cortical afferents to area V6 are represented in yellow, to V6Av in blue, and
to V6Ad in pink. Other details are as in Figs. 1–4.
many parietal areas (MIP, PEc, PGm, LIP, VIP, AIP, PG, and
Opt). In addition, a strong input to V6Ad arises from the frontal
lobe, mainly from the premotor area F2 (that contains many reachand grasp-related neurons, Caminiti et al., 1991; Raos et al.,
2004) and F7 (more involved in oculomotor activity, Boussaoud
et al., 1998; Gregoriou et al., 2005), and a weaker but consistent
input arises from the prefrontal area 46 (known to be involved in
working memory, Luebke et al., 2010; Levy & Goldman-Rakic,
1999). These anatomical studies suggest that V6Av is primarily
a visual area that brings visual information from V6 to V6Ad,
whereas V6Ad a visuomotor area that links parietal and frontal
cortices. This flow of information constitutes the dorso-medial
(or dorso-dorsal) stream (Galletti et al., 2003; Rizzolatti &
Matelli, 2003) that integrates different sensory inputs, in particular visual and somatosensory ones, likely for the control of
reaching and grasping activities (Galletti et al., 2004; Gamberini
et al., 2009).
A recent metaanalysis (Gamberini et al., 2011) has taken into
account the functional properties of about 4000 cells recorded
from V6Av and V6Ad in awake animals. The results showed
that visual neurons are significantly more represented in V6Av
(69% in V6Av vs. 59% in V6Ad). The size of receptive field
increases with eccentricity in both V6Av and V6Ad, but in V6Av
the receptive fields are significantly smaller than in V6Ad at any
value of eccentricity (Fig. 7, cyan and pink lines, respectively).
Although both areas V6Av and V6Ad are not point-to-point retinotopically organized, V6Av mainly represents the peripheral
part of the visual field while V6Ad mainly the central part of it
(Fig. 7, lower panels; Fig. 11C). V6Av represents almost exclusively the lower visual field, whereas V6Ad represents both
lower and upper visual fields, with a prevalence of the lower
visual field representation (Fig. 7, lower panels and Fig. 11D).
The horizontal meridian is represented at the border between
V6Av and V6Ad (Fig. 11D).
Like area V6, also area V6Av has been recently recognized
in the human brain (Pitzalis et al., 2013). Human V6Av, like
macaque V6Av, is a visual area that mostly represents the periphery of the contralateral lower visual field. The relationships
of V6Av with neighboring areas are almost the same in the two
species (see Fig. 9D): in human, like in macaque, V6Av abuts
9
The macaque medial parieto-occipital cortex
and subcortical (Gamberini et al., 2015) afferences, as well as
functional properties, so that it was suggested they work together
in the online control of reach-to-grasp actions (Gamberini et al.,
2011).
A summary of mPOC organization
Fig. 9. Brain location of areas V6, V6Av, and V6Ad in monkey and
human. Brain location of V6Av (blue) and V6 (yellow) areas in macaque
(A and B) and human monkeys (C and D). A and B show also the location of macaque area V6Ad. A medial view of the inflated surface (left
column) and a flat map of the posterior brain (right column) are shown.
A and C show the typical topographical arrangement of areas V6Av, and
V6 along the POs. B and D show the spatial relationship among areas
V6Av, V6, and other early visual areas. Light and dark gray areas indicate gyri and sulci (modified from Gamberini et al., 2011; Pitzalis et al.,
2013). pIPs, posterior end of the intraparietal sulcus; l, lateral. Other
details are as in Figs. 1–4.
on area V6 posteriorly and on V3A laterally. More details on
brain location, functional organization, and properties of human
V6Av are fully described in the study by Pitzalis et al. in this
issue.
Many V6A cells are sensitive to somatosensory stimulation
(Breveglieri et al., 2002), with this type of cells being twice as
common in V6Ad than in V6Av (Gamberini et al., 2011). Most of
these cells are modulated by the somatic stimulation of the arm/
hand, in particular by the joint rotation (Gamberini et al., 2011).
The large majority of V6A cells are modulated by active arm
movements, both in reaching- (Galletti et al., 1997; Fattori et al.,
2001; Fattori et al., 2005) and grasping- (Fattori et al., 2009; Fattori
et al., 2010) tasks. Arm-related cells are uniformly distributed in
V6Av and V6Ad (Gamberini et al., 2011). Interestingly, however,
cells sensitive to the precision grip are more present in V6Ad and
cells sensitive to the whole prehension are more present in V6Av
(Gamberini et al., 2011). This fact, together with the high incidence
of central visual field representation in V6Ad and the overrepresentation of the periphery in V6Av, suggests that V6Ad is more
involved in the control of the final part of reach-to-grasp actions
(Fattori et al., 2010) and V6Av in the visual analysis of the transport phase of these actions (Fattori et al., 2010; Gamberini et al.,
2011).
In conclusion, V6Av and V6Ad show a different distribution
of several functional properties, peculiar architectural patterns,
different topographical organizations of the visual domain, and
partially distinct cortico-cortical circuits. In spite of these differences, V6Av and V6Ad also share several cortical (Fig. 8B)
Fig. 12 summarizes the organization of parieto-occipital cortex
according to data from the literature (Gattass et al., 1981;
Gattass et al., 1988) and from our laboratory. In the mPOC,
which is the target of this review, we found three retinotopically
organized visual areas (V2, V3, and V6) and two visuomotor
areas (V6Av and V6Ad) with a complex visual topography.
The parts of areas V2 and V3 located in the posterior bank of
the POs represent the contralateral lower visual field between
10° and 30° of eccentricity. However, while area V2 is a strip
of cortex that represents the vertical meridian dorsally, at the
border with V1, and the horizontal meridian ventrally, at the
border with V3, area V3 shows a more complex visuotopic organization. It represents the horizontal meridian dorsally, at the
border with V2, but the vertical meridian is represented ventrally only in the lateral part of POs, where V3 borders with the
central representation of V6. In the medial part of POs, V3 represents only the horizontal meridian and nearby regions of the
visual field. Here, V3 borders the horizontal meridian representation of V2 dorsally and that of V6 ventrally. As a whole, within
the POs, area V3 represents the lower contralateral visual field
between 10° and 30° eccentricities, with the regions near the vertical meridian represented laterally, and those near the horizontal
meridian medially.
Area V6 is located rostral and laterally to V3. It represents
both central and peripheral parts of the visual field, though
highly emphasizes this latter, in a point-to-point fashion. The
central representation is located laterally within the POs, in the
posterior bank of the sulcus, where V6 merges with area V3,
while the periphery is located in the ventral part of the anterior
bank of POs. The far periphery (>60° of eccentricity) and the
upper visual field representation are located on the mesial surface of the hemisphere and in the depth of the medial parietooccipital sulcus. Areas V6Av and V6Ad are located rostral to
V6, in the dorsal part of the anterior bank of POs and on the
mesial surface of the hemisphere. V6Av mainly represents the
periphery of the contralateral lower visual field, with the vertical meridian that borders on V6 and the horizontal meridian
bordering on V6Ad. V6Ad represents mainly the central part of
the visual field.
Open questions
Although the present data support the hypothesis of V3 inserting, at least partially, between V2 and V6 within the POs, the
alternative hypothesis that V2, instead of V3, borders V6 can
not be completely rejected. In fact, if we do not consider the
change in receptive field size, the neurons we assigned to V3 in
the medial part of POs (see Fig. 5B) could be assigned to V2.
The receptive field sequence in the whole posterior bank of POs
was coherent with this view, moving the receptive fields from
the vertical meridian dorsally, at the border with V1 (site 1), to
the horizontal meridian ventrally, in the fundus of POs (sites 8
and 9), and again toward the vertical meridian posteriorly in the
ventral convexity of the brain. If this were the case, V3 would be
10
Gamberini et al.
Fig. 10. Cyto- and myeloarchitectural subdivisions of the anterior wall of the parieto-occipital sulcus. (A) Parasagittal section taken
at the level of parieto-occipital sulcus, as indicated in the dorsal view of macaque brain shown under the section. Gray regions
highlight the cortical parcellation reported by Luppino et al., 2005. Boxes on the section drawing indicate the location of the photomicrographs shown on the right. Higher magnification views from the same section of cytoarchitectonic areas V3, V6, V6Av, and
V6Ad. Scale bar (shown under V3), 200 μm. (B) Parasagittal section stained for myelin taken at the level of parieto-occipital sulcus
(modified from Luppino et al., 2005). Scale bar, 1 mm. (C) Parasagittal section stained for myelin taken at the level of parieto-occipital
sulcus (modified from Colby et al., 1988). Scale bar, 1 mm. Arrows mark the borders between cytoarchitectonic areas. Other details are
as in Figs. 1–4.
limited to the lunate and the very medial part of POs (Fig. 5C)
and would represent the peripheral 30° of the visual field only
near the vertical meridian (see sites 4–7 in Fig. 5C and 5D),
so lacking in the representation of the complementary part of
the visual field near the horizontal meridian (see sites B5–B8 in
Fig. 5D). To conclude, it remains an open question whether area
V3 stops at the lateral end of POs and represents an asymmetric
part of the visual field, or whether it occupies also the medial
end of the sulcus so representing the whole lower quadrant of
the visual field up to an eccentricity of about 30°. Additional
work involving two- and three-dimensional reconstructions of
data from single cases is needed to clarify this point.
Another issue that has not been resolved in our studies is the
location of the central upper field representation of V6. We have
never recorded cells in V6 with a receptive field located within
the central 20° of the upper visual field. Since this part of the
visual field is represented in what has been described as an anomalous central visual field representation in the medial part of area
11
The macaque medial parieto-occipital cortex
Fig. 11. Visuotopic organization in macaque areas V6 and V6A. (A and
B) Dorsal and postero-medial views of a 3D reconstruction of a macaque
right hemisphere showing in B the locations of areas V6, V6Av, and
V6Ad in the anterior bank of POs, and the nearby area PEc on the dorsal
surface of the SPL. The occipital pole was cut away, as indicated in the
dorsal view of the hemisphere in A, to show the anterior bank of POs.
(C) Distribution in V6A of visual cells with receptive fields in the central (<30°; blue dots) and peripheral (>30°; yellow dots) parts of the
visual field, respectively. Yellow and blue areas in V6 indicate the eccentricities represented in different parts of V6 according to the color
coding shown at the bottom. (D) Distribution in V6A of visual cells with
receptive fields in the lower (green dots) or upper (red dots) visual field.
White dots indicate receptive fields located on the horizontal meridian.
Red and green areas in V6 indicate the visual field quadrants represented in different parts of V6 according to the color coding shown at
the bottom. White squares and black circles represent the HM and VM
meridians of area V6, respectively (modified from Galletti et al., 1999a;
Pitzalis et al., 2013). Other details are as in Figs. 1–4.
V3A, a cortical region that borders V6 (see “?” in Fig. 12)
described by Van Essen and Zeki (1978) in one case, we suggested (Galletti et al., 1999a) that this region is actually the central upper field representation of V6. In agreement with our view,
this central field representation shows receptive fields larger than
those of the lateral part of V3A, that is, receptive fields similar in
size to those of area V6. As this cortical region was not covered
by our recording sites, further experiments are needed to verify
the validity of this hypothesis.
Acknowledgments
The authors wish to thank M. Verdosci, F. Campisi, L. Passarelli, and
G. Placenti for technical assistance. This research was supported by
Fig. 12. Flattened map of the mPOC. Flat map of the mPOC of the right
hemisphere of the macaque atlas brain showing the spatial relationship
among visual areas V2, V3, V3A, and V6, and the visuomotor parietal areas
V6Av and V6Ad (boxed area on the top left). CARET software has been
used for the 2D reconstruction (http://www.nitrc.org/projects/caret/,
Van Essen et al., 2001). Light and dark gray areas indicate gyri and sulci,
respectively. The dashed lines are isoeccentricity lines. Black circles
and white squares indicate the representation of the VM and HM meridians,
respectively; triangles indicate the periphery of the visual field; F, center of
gaze; ?, likely location of the anomalous central representation of V3A.
The location and topography of cortical areas are based on the studies of
several authors (modified from Gattass et al., 1981, 1988; Galletti et al.,
1999a; Galletti et al., 1999b; Pitzalis et al., 2013). Other details are as
in Figs. 1–4, 6, and 9.
European Union Grants, FP6-IST-027574-MATHESIS and FP7-IST217077-EYESHOTS, and by Ministero dell'Università e della Ricerca and
Fondazione del Monte di Bologna e Ravenna, Italy.
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