Download Projections from the superior temporal sulcus to the agranular frontal

European Journal of Neuroscience, Vol. 14, pp. 1035±1040, 2001
ã Federation of European Neuroscience Societies
SHORT COMMUNICATION
Projections from the superior temporal sulcus to the
agranular frontal cortex in the macaque
Giuseppe Luppino, Roberta Calzavara, Stefano Rozzi and Massimo Matelli
Istituto di Fisiologia Umana, UniversitaÁ di Parma, Via Volturno, 39, I-43100 Parma, Italy
Keywords: motion information, motor cortex, temporal cortex
Abstract
The aim of this study was to investigate the organization of the projections from the superior temporal sulcus (STS) to the
various areas forming the agranular frontal cortex. Injections of retrograde neuronal tracers were made in the various agranular
areas, in nine macaque monkeys. The results showed that two rostral premotor areas, F6 (pre-SMA) and F7, and the
ventrorostral part of area F2 (F2vr) are targets of projections from the upper bank of the STS (uSTS). F6 and the dorsorostral
part of F7 (supplementary eye ®eld, SEF) are targets of projections from the rostral part of the uSTS, corresponding to the socalled `superior temporal polysensory area' (STP). In contrast, the ventral part of area F7 (not including the SEF) and F2vr are
targets of afferents from the caudal part of the uSTS. Ventral F7 is the target of weak afferents from the caudalmost and
dorsalmost part of the uSTS (area 7a), whilst F2vr is the target of projections from a relatively more rostral and ventral sector of
the uSTS, close to the fundus of the sulcus. This sector should correspond to area MST. In conclusion, F6 and SEF receive high
order information from STP, whereas ventral F7 and F2vr receive information from areas of the dorsal visual stream.
Introduction
The upper bank of the superior temporal sulcus (uSTS) can be
functionally subdivided into a caudal and a rostral sector. The caudal
sector is considered to be part of the so-called `dorsal visual stream'
and is largely occupied by the middle superior temporal area (MST),
which extends over about the ventral half of the bank (Desimone &
Ungerleider, 1986). Area MST is a major target of the adjacent
middle temporal area (MT; Ungerleider & Desimone, 1986b) and
appears to play an important role in motion perception (Komatsu &
Wurtz, 1988; Andersen et al., 1997). The dorsalmost part of the
caudal uSTS, referred to as the `posterior parietal' area (PP) by
Desimone & Ungerleider (1986), corresponds to a visually responsive
region considered by some authors to be part of area 7a of the inferior
parietal lobule (Andersen et al., 1990; see Felleman & Van Essen,
1991).
The rostral sector of the uSTS, including also the corresponding
part of the fundus, is generally referred to as the `superior temporal
polysensory area' (STP) and is a site of convergent projections from
somatosensory, auditory and visual areas of both the dorsal and the
ventral visual stream (Bruce et al., 1981; Felleman & Van Essen,
1991). Functional data showed that neurons in this area have
somatosensory, auditory or visual receptive ®elds and that many
visually responsive neurons have very complex properties (Bruce
et al., 1981; Perrett et al., 1989; see also Carey et al., 1997).
Previous data showed that a major target of the uSTS, in the frontal
lobe, is the prefrontal cortex (Seltzer & Pandya, 1989), although there
is also some evidence that the uSTS may also project directly to the
agranular frontal cortex (Seltzer & Pandya, 1989; Boussaoud et al.,
Correspondence: Professor Giuseppe Luppino, as above.
E-mail: [email protected]
Received 20 February 2001, revised 18 June 2001, accepted 9 August 2001
1990; Maioli et al., 1998). Recent evidence, however, showed that the
agranular frontal cortex is formed by a multiplicity of independent
areas with different anatomical connections and different functional
roles in motor control (Rizzolatti et al., 1998; Luppino & Rizzolatti,
2000). Thus, the issue addressed in the present study was to identify
the agranular areas which are targets of projections from the uSTS
and to de®ne also the areas, within the superior temporal sulcus
(STS), which are the origin of these projections. Preliminary data
have been presented elsewhere in abstract form (Luppino et al.,
2000).
Materials and methods
All experimental procedures used in the present study were approved
by the Veterinarian Animal Care and Use Committee of the
University of Parma and complied with the European law on the
care and use of laboratory animals. In nine macaque monkeys (six
Macaca nemestrina and three Macaca fascicularis) injections of
retrograde tracers were made in all the various agranular frontal
areas, de®ned according to Matelli et al. (1985, 1991). Data from
Case 4 have already been presented elsewhere (Luppino et al., 1993).
In this study, they have been re-analysed and presented together with
the other cases in order to obtain a comprehensive view of the
projections from the STS to all the various premotor areas.
In all monkeys but two (Cases 2 and 4), the injection sites were
chosen by using sulci and dimples as landmarks. Each animal was
anaesthetized with ketamine hydrochloride (15 mg/kg i.m.). Under
aseptic conditions, the bone was removed from over the appropriate
cortical region and the dura opened. In Cases 2 and 4 the location of
the injection sites was selected on the basis of chronic electrophysiological experiments (see Luppino et al., 1993; Matelli et al.,
1036 G. Luppino et al.
TABLE 1. Monkey species, localization of the cortical injections and tracers employed in the experiments
Monkey
Species
Hemisphere
Area
Tracer (%)
Amount (mL)
Case 2
M. Fascicularis
Case 4
M. Fascicularis
Case 10
Case 11
M. Nemestrina
M. Nemestrina
Case 12
M. Nemestrina
Case 13
M. Fascicularis
Case 14
Case 18
M. Nemestrina
M. Nemestrina
Case 20
M. Nemestrina
Left
Right
Right
Left
Left
Right
Right
Left
Left
Left
Left
Left
Left
Left
Left
Left
F7-SEF
F3
F6
F6
F2d
F2vr
F7±not SEF
F2d
F4
F7±not SEF
F5
F1
F5
F2vr
F4
F1
FB (3)
WGA-HRP (4)
FB (3)
DY (2)
FB (3)
FB (3)
DY (2)
DY (2)
FB (3)
FB (3)
DY (2)
TB (5)
FB (3)
CTB-gold (0.5)
FB 3)
CTB-gold (0.5)
1
8
1
1
1
1
2
1
1
1
1
2
1
1
1
1
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
0.2
0.08
0.2
0.2
0.2
0.35
0.2
0.15; 1 3 0.2
0.2
0.2
0.2
0.2
0.2; 1 3 0.3
1
0.2
1
SEF, supplementary eye ®eld; F2vr, ventrorostral part of F2; F2d, dimple region of F2.
1998). Once the appropriate cortical site was chosen, ¯uorescent
tracers (Fast Blue, FB, 3% in distilled water, True Blue, TB, 5% in
distilled water, Diamidino Yellow, DY, 2% in 0.2 M phosphate buffer
at pH 7.2; EMS-POLYLOY GmbH, Gross-Umstadt, Germany),
wheatgerm agglutinin, peroxidase-conjugated (WGA-HRP; 4% in
distilled water, Sigma, St Louis, MO, USA), or cholera toxin B
subunit, gold-conjugated (CTB-gold, 0.5% in distilled water; LIST,
Campbell, CA, USA) was slowly pressure-injected through a glass
micropipette (tip diameter 50±100 mm) attached to a 1-mL Hamilton
microsyringe (Reno, NV, USA). Table 1 summarizes the locations of
injections, the injected tracers and their amounts. The tracers injected
into the cortical convexity were delivered 1.5 mm below the cortical
surface, whilst those injected in the posterior bank of the arcuate
sulcus or in the areas of the mesial wall of the hemisphere were
delivered at various depths from the cortical crown. After the
injections had been made, the dural ¯ap was sutured, the bone
replaced and the super®cial tissues sutured in layers. After appropriate survival periods (12±14 days following ¯uorescent tracer injections, 7 days following injection of CTB-gold and 2 days following
injections of WGA-HRP), each animal was anaesthetized with
ketamine hydrochloride (15 mg/kg i.m.) followed by an i.v. lethal
injection of sodium thiopental and perfused through the left cardiac
ventricle with saline, and then with one of the following procedures:
(i) 4% paraformaldehyde, 10% sucrose plus 1.5% dimethyl sulfoxide
(Cases 2 and 4); (ii) 4% paraformaldehyde, 5% glycerol (Case 10); or
(iii) 3.5% paraformaldehyde, 5% glycerol (Cases 11±14, 18 and 20).
All solutions were prepared in phosphate buffer 0.1 M pH 7.4. Brains
were then blocked coronally, removed from the skull and placed for
one day in cold sucrose buffer (Cases 2 and 4) or in 10% buffered
glycerol for 3 days and 20% glycerol for 4 days (Cases 10±14, 18 and
20). Finally, they were cut on a freezing microtome in a coronal plane
at 60 mm. In all monkeys, at least one section of each ®ve was
mounted, air-dried and quickly coverslipped for ¯uorescence
microscopy. In Case 2, one section of each ®ve was processed for
WGA-HRP histochemistry with tetramethylbenzidine as chromogen
(Mesulam, 1982). In Cases 18 and 20, in one section of each ®ve,
CTB-gold was revealed by the silver intensi®cation protocol
described by Kritzer & Goldman-Rakic (1995). In all cases the
extent of the injection sites was evaluated and their location was
attributed to cytoarchitectonic areas by using adjacent sections
stained with the Nissl method. The injection sites presented in this
study were all restricted within the limits of a single cytoarchitectonic
area. Figure 1 (upper part) summarizes the cytoarchitectonic location
of all the injection sites, plotted onto a dorsolateral and a mesial view
of a single hemisphere.
Retrogradely labelled neurons were plotted in each section every
600 mm. 2-D reconstructions of the distribution of cortical labelling
were obtained according to the procedure described by Matelli et al.
(1998). The 2-D reconstructions of the STS were obtained by aligning
the unfolded sections through the sulcus at the fundus, in its rostral
part, and at the midpoint of the ¯oor, in its caudal part.
Results
The results showed that only the two rostral premotor areas, F6 (preSMA) and F7, plus the ventrorostral part of area F2 (F2vr) were
found to be targets of projections from the STS (Fig. 1, upper part,
®lled circles).
Area F6 was injected in two cases. In Case 4l (injection site shown
in Fig. 1, lower part), DY-labelled cells were located in the fundus of
the sulcus, slightly extending also in the dorsal bank, in correspondence of the rostral end of the ¯oor and therefore in area STP
(Fig. 2A). Very similar results were observed following FB injection
in Case 4r (not shown). In both cases the labelling observed within
the STS was relatively weak.
Area F7 was injected in three cases. In Case 2l, FB was injected in
the dorsal part of F7 corresponding to the supplementary eye ®eld
[F7-supplementary eye ®eld (SEF), Fig. 1, lower part], as de®ned
following extensive physiological mapping. In Cases 11r (injection
site shown in Fig. 1, lower part) and 13l, tracers injections involved
the ventral and caudal parts of F7 (F7±not SEF), respectively.
Following F7-SEF injection, the labelling in the STS was much
stronger than that observed in F6 injections. Almost all the labelling
was located in the rostral two-thirds of the uSTS, in correspondence
with the fundus, but also extending in the whole extent of the dorsal
bank and therefore occupying a large part of area STP (Fig. 2B).
Within this region, labelled cells were relatively more concentrated in
two separate sectors: a caudal one, coinciding with the sector labelled
following injections in F6, and a more rostral one.
ã 2001 Federation of European Neuroscience Societies, European Journal of Neuroscience, 14, 1035±1040
STS projections to the motor cortex
1037
much weaker and located in the caudalmost and dorsalmost part of
uSTS. It also extended to the adjacent parietal convexity. Whilst in
Case 11r DY (Fig. 2C) the labelling was almost restricted to the
caudalmost and dorsalmost part of the uSTS, in Case 13l (not shown)
most of the labelling was found in the cortical convexity of the
inferior parietal lobule. The territory labelled following both these
cases appears to very likely correspond to area 7a (Andersen et al.,
1990; Felleman & Van Essen, 1991).
Area F2 was injected in four cases. Labelling within the uSTS was,
however, observed only following injections in F2vr (Cases 18l and
11r FB), but not following injections near the superior precentral
dimple (F2d). The labelled cortical sector was markedly different
from those labelled following F6 and F7 injections. The results of
Case 18l are shown in Fig. 2D (injection site shown in Fig. 1, lower
part). Relatively dense labelling was concentrated in the caudal and
ventral part of the uSTS, at a level caudal to the end of the lateral
®ssure. This labelling extended, ventrally, up to the border with the
¯oor, slightly invading the dorsalmost part of the ¯oor itself. The
location of this labelling corresponds to that of area MST, as
described by Desimone & Ungerleider (1986). Similar results were
also observed using a different retrograde tracer (FB, Case 11r, not
shown). Also in this case the labelling was relatively dense and its
location appeared to coincide with that of Case 18l, although slightly
shifted in a more caudal position. Sparse labelling was also observed
in the caudalmost and dorsalmost part of uSTS.
Discussion
FIG. 1. (Upper part) Schematic view of the location of the injection sites
plotted onto a dorsolateral and a mesial view of a single hemisphere.
Numbers inside the circles refer to the injected cases (see Table 1). Dashed
lines mark the cytoarchitectonic borders of the motor areas according to
Matelli et al. (1985, 1991). Filled circles indicate injection sites which
produced labelling within the STS or in adjacent parietal cortex. (Lower
part) Coronal sections from the representative cases illustrated in Fig. 2,
showing location and extent of injection sites with respect to
cytoarchitectonics. AI, inferior arcuate sulcus; AS, superior arcuate sulcus;
C, central sulcus; CC, corpus callosum; Cg, cingulated sulcus; L, lateral
sulcus; IP, intraparietal sulcus; P, principal sulcus. Scale bar, 5 mm.
In contrast with the results of F7-SEF injection, the labelling
observed following injections in other parts of area (F7±not SEF) was
The present data indicate that the projections from STS to the motor
cortex are restricted to the two rostral premotor areas F6 and F7, plus
F2vr. In particular, areas F6 and F7±not SEF receive afferents from
rostral regions of the uSTS, whereas F7±not SEF and F2vr are targets
of more caudal regions of the uSTS. The differential pattern of
connectivity of different sectors of areas F2 (F2vr vs. F2d) and F7
(F7-SEF vs. F7±not SEF) is in line with previous observations on
differential parietal connections of these two frontal areas (Matelli
et al., 1998) as well as with evidence on their differential functional
properties (see Rizzolatti et al., 1998). In spite of these hodological
and functional differences, so far no clear cytoarchitectonic evidence
has been provided in favour of a further subdivision of F7 and F2.
Thus, the possibility that the different sectors of F7 and F2 represent
separate areas or represent different modules within a given
architectonic area needs further studies using architectonic techniques
other than Nissl method.
The rostral part of the uSTS corresponds to a cortical region,
termed `superior temporal polysensory' area (STP; Bruce et al.,
1981). According to Seltzer & Pandya (1978) and Cusick et al. (1995)
area STP is architectonically not homogeneous. Functional studies,
however, in which the distribution of multimodal STP neurons was
correlated with architectonics, did not provide evidence that
architectonic subdivisions may correspond to different functional
entities (see, e.g. Bayliss et al., 1987). Hodological data indicate that
STP is target of projections from somatosensory, auditory and visual
areas. In particular, this region appears to be a privileged site of
convergent inputs from visual areas belonging to both the dorsal and
ventral visual streams (Boussaoud et al., 1990; Baizer et al., 1991;
see also Felleman & Van Essen, 1991). Based on connectional
differences Felleman & Van Essen (1991) proposed a subdivision of
STP in a rostral (STPa) and a caudal (STPc) region. Although the
limits of these two STP subdivisions cannot be set with certainty, it
could be of some interest to note that, in our F7-SEF injection,
ã 2001 Federation of European Neuroscience Societies, European Journal of Neuroscience, 14, 1035±1040
1038 G. Luppino et al.
ã 2001 Federation of European Neuroscience Societies, European Journal of Neuroscience, 14, 1035±1040
STS projections to the motor cortex
separate clusters of labelled cells were observed in the rostral and the
caudal part of STP (possibly corresponding to STPa and STPc,
respectively), whereas following F6 injections only the caudal part
(possibly STPc) was labelled. Rostral and a caudal spots of labelling
in STP were also found by Huerta & Kaas (1990) following SEF
injection.
Several electrophysiological studies have shown that neurons in
area STP have complex sensory properties. Firstly, although STP
neurons are predominantly purely visual, a signi®cant proportion of
them have also somatosensory and/or auditory responses (Bruce et al.,
1981; Bayliss et al., 1987). Secondly, visually responsive neurons
usually have complex functional properties (for a review of the data,
see, e.g. Carey et al., 1997). It has been proposed that area STP is
involved in visuomotor functions and in integration of information
within and across modalities (Bruce et al., 1981; Bayliss et al., 1987).
Furthermore, according to the studies of Perrett and colleagues
(Perrett et al., 1989; see also Carey et al., 1997) complex visual
neurons in STP could be responsible for coding the visual appearance
of the body, for coding particular types of body motion, for coding
movements which are not consequence of the monkey's own action
or for coding body movements as goal-directed actions. This highorder information, which can be of crucial importance in the social
behaviour of primates, can be conveyed to the cortical motor system
through the posterior parietal cortex or through a relay in the ventral
dorsolateral prefrontal cortex (Seltzer & Pandya, 1989). Present data
indicate that STP out¯ow has also a direct access to area F6 and the
SEF.
Area F6 (pre-SMA) is a rostral premotor area mainly concerned
with the control of arm movements. Functional properties of F6
suggest that this area plays a key role in selection and preparation of
movements and in learning and organizing complex movement
sequences (for a review of these data, see Tanji et al., 1996; Rizzolatti
et al., 1998; Hikosaka et al., 1999). The SEF is an electrically
excitable oculomotor ®eld (Schlag & Schlag-Rey, 1987), located in
the dorsal part of area F7. The functional properties of the SEF
suggest that this area plays a more complex role in the organizazion
of eye movements than that of the frontal eye ®eld. SEF is not
necessary for producing accurate visually guided saccades, but it
appears to play an important role in learning conditional oculomotor
responses, in encoding saccades relative to an object centred frame of
reference, or in monitoring the consequences of eye movements as
part of a brain's supervisory control system (see Stuphorn et al.,
2000). The notion that F6 and the SEF play a role in the control of
arm or eye movements at a high hierarchical level is supported by
data on the cortical connections of these two areas. Both these areas
are target of very weak parietal input but, in contrast, they receive
rich projections from cingulate area 24c, as well as from the dorsal
and ventral parts of the dorsolateral prefrontal cortex (Huerta & Kaas,
1990; Luppino et al., 1993). Therefore, area F6 and the SEF are the
only motor areas in which cognitive and motivational information
may be integrated and conveyed to other arm representations, with
the exclusion of that of F1 (in the case of F6), or to the frontal eye
®eld (in the case of the SEF). The projections from STP to F6 and the
1039
SEF, shown in this study, provide further support in favour of their
peculiar functional role in motor control.
Two areas occupy the caudal part of the uSTS; area MST, lying in
the ventral half of the bank, and a dorsal and caudal cortical sector
called area PP by Desimone & Ungerleider (1986), but included by
Andersen et al. (1990) within the architectonic limits of area 7a.
Area MST is target of projections from area MT (Maunsell & Van
Essen, 1983; Ungerleider & Desimone, 1986b) and plays an
important role in visual motion processing (Komatsu & Wurtz,
1988; see also Andersen et al., 1997). In particular, MST neurons
appear to be more selective for motion patterns that occur with self
motion (see Andersen et al., 1997) and, by combining visual and
vestibular signals, they are able to enhance self-movement detection
and disambiguate optic ¯ow that results from either self-movement or
the movements of large objects near the observer (Duffy, 1998).
Thus, MST appears to be very important for navigation using motion
cues (see Andersen et al., 1997).
The labelling observed in the caudal uSTS, following injections in
F7±not SEF and in F2vr, was spatially segregated. Whilst F7±not SEF
is a target of area 7a, F2vr is most probably a target of area MST as
de®ned by Desimone & Ungerleider (1986). According to these
authors, MST occupies `most of the bottom half of the upper bank of
the caudal STS and a small portion of the adjacent ¯oor'. Area MST
is myeloarchitectonically not homogeneous, with a densely myelinated zone (DMZ) occupying its dorsalmost part, at the border with
area PP or area 7a (Desimone & Ungerleider, 1986; Ungerleider &
Desimone, 1986a; Andersen et al., 1990). Our material was not
stained for myelin, so that it was not possible to correlate the location
of the labelling observed following F2vr injections with that of DMZ.
However, if one compares the location of the labelling observed in
the present study (see Fig. 2D, sections 150 and 152) with the
location of MST, as shown by previous authors in coronal sections
(see, e.g., Ungerleider & Desimone, 1986a; Boussaoud et al., 1990),
it seems quite reasonable to attribute the labelling to this area. If this
is accepted, one should conclude that F2vr is the only premotor area
that receives a direct input from an area speci®cally devoted to
motion perception.
This ®nding supports the recent evidence that F2vr is hodologically
and functionally independent of F2d (see Caminiti et al., 1996;
Rizzolatti et al., 1998; Luppino & Rizzolatti, 2000). In contrast with
F2d, F2vr is the target of visual or somatosensory and visual areas of
the superior parietal lobule (MIP and V6A), is the target of a minor
but consistent projection from the dorsal part of DLPF and contains
visually responsive neurons. Thus, F2vr appears to be involved in
planning and controlling arm movements on the basis of visual and
somatosensory information. This information could be used for the
visual guidance of the arm trajectory when, for example, reaching
towards moving objects or reaching objects during self-movements of
the body.
Acknowledgements
Work supported by MURST, CNR and HSPO.
FIG. 2. Distribution of retrogradely labelled neurons in the STS following injections in areas (A) F6, (B) supplementary eye ®eld (F7-SEF), (C) F7±not SEF
and (D)ventrorostral part of area F2 (F2vr). For each case, in the left part of the ®gure a view of the hemisphere shows the location of the injection sites and
the cytoarchitectonic borders of the injected area. The middle part of the ®gure shows the unfolded view of the STS and the distribution of labelled neurons.
Each dot corresponds to one neuron. The right part of the ®gure illustrates selected coronal sections showing the distribution of the labelled neurons within
the STS. The levels of the sections are also reported on the unfolded view of the STS and on the view of the brain. Abbreviations as in Fig. 1.
ã 2001 Federation of European Neuroscience Societies, European Journal of Neuroscience, 14, 1035±1040
1040 G. Luppino et al.
Abbreviations
CTB-gold, cholera toxin B subunit, gold-conjugated; DY, Diamidino Yellow;
F2d, precentral dimple part of area F2; F2vr, ventrorostral part of area F2; FB,
Fast Blue; MST, middle superior temporal area; MT, middle temporal area;
PP, posterior parietal; SEF, supplementary eye ®eld; STP, superior temporal
polysensory area; STS, superior temporal sulcus; TB, True Blue; uSTS, upper
bank of the superior temporal sulcus; WGA-HRP, wheatgerm agglutinin,
peroxidase-conjugated.
References
Andersen, R.A., Asanuma, C., Essick, G. & Siegel, R.M. (1990)
Corticocortical connections of anatomically and physiologically de®ned
subdivisions within the inferior parietal lobule. J. Comp. Neurol., 296, 65±
113.
Andersen, R.A., Snyder, L.H., Bradley, D.C. & Xing, J. (1997) Multimodal
representation of space in the posterior parietal cortex and its use in
planning movements. Annu. Rev. Neurosci., 20, 303±330.
Baizer, J.S., Ungerleider, L.G. & Desimone, R. (1991) Organization of visual
inputs to the inferior temporal and posterior parietal cortex in macaques.
J. Neurosci., 11, 168±190.
Bayliss, G.C., Rolls, E.T. & Leonard, C.M. (1987) Functional subdivisions of
the temporal lobe neocortex. J. Neurosci., 7, 330±342.
Boussaoud, D., Ungerleider, L. & Desimone, R. (1990) Pathways for motion
analysis: cortical connections of the medial superior temporal and fundus of
the superior temporal visual areas in the macaque. J. Comp. Neurol., 296,
462±495.
Bruce, C., Desimone, R. & Gross, C.G. (1981) Visual properties of neurons in
a polysensory area in superior temporal sulcus of the macaque.
J. Neurophysiol., 46, 369±384.
Caminiti, R., Ferraina, S. & Johnson, P.B. (1996) The sources of visual
information to the primate frontal lobe: a novel role for the superior parietal
lobule. Cerebral Cortex, 6, 319±328.
Carey, D.P., Perrett, D.I. & Oram, M.W. (1997) Functional anatomy of human
motor cortical areas. In Boller, F. & Grafman, J. (eds), Handbook of
Neuropsychology, Vol. 11. Elsevier, Amsterdam, pp. 111±129.
Cusick, C.G., Seltzer, B., Cola, M. & Griggs, E. (1995) Chemoarchitectonics
and corticocortical terminations within the superior temporal sulcus of the
rhesus monkey: evidence for subdivisions of superior temporal polysensory
cortex. J. Comp. Neurol., 360, 513±535.
Desimone, R. & Ungerleider, L.G. (1986) Multiple visual areas in the caudal
superior temporal sulcus of the macaque. J. Comp. Neurol., 248, 164±189.
Duffy, C.J. (1998) MST neurons respond to optic ¯ow and translational
movement. J. Neurophysiol., 80, 1816±1827.
Felleman, D.J. & Van Essen, D.C. (1991) Distributed hierarchical processing
in primate cerebral cortex. Cerebral Cortex, 1, 1±47.
Hikosaka, O., Sakai, K., Nakahara, H., Lu, X., Miyachi, S., Nakamura, K. &
Rand, M.K. (1999) Neural mechanisms for learning of sequential
procedures. In Gazzaniga, M.S. (ed.), The New Cognitive Neurosciences.
MIT Press, Cambridge, USA, pp. 553±572.
Huerta, M.F. & Kaas, J.H. (1990) Supplementary eye ®eld as de®ned by
intracortical microstimulation: connections in Macaques. J. Comp. Neurol.,
293, 299±330.
Komatsu, H. & Wurtz, R.H. (1988) Relation of cortical areas MT and MST to
pursuit eye movements. I. Localization and visual properties of neurons.
J. Neurophysiol., 60, 580±603.
Kritzer, M.F. & Goldman-Rakic, P.S. (1995) Intrinsic circuit organization of
the major layers and sublayers of the dorsolateral prefrontal cortex in the
rhesus monkey. J. Comp. Neurol., 359, 131±143.
Luppino, G., Calzavara, R., Rozzi, S. & Matelli, M. (2000) Projections from
the superior temporal sulcus to prefrontal recipient premotor areas in the
macaque. Soc. Neurosci. Abstr., 26, 1712.
Luppino, G., Matelli, M., Camarda, R. & Rizzolatti, G. (1993) Corticocortical
connections of area F3 (SMA proper) and area F6 (pre-SMA) in the
macaque monkey. J. Comp. Neurol., 338, 114±140.
Luppino, G. & Rizzolatti, G. (2000) The organization of the frontal motor
cortex. News. Physiol. Sci., 15, 219±224.
Maioli, M.G., Squatrito, S., SamolskyDekel, B.G. & Sanseverino, E.R. (1998)
Corticocortical connections between frontal periarcuate regions and visual
areas of the superior temporal sulcus and the adjoining inferior parietal
lobule in the macaque monkey. Brain Res., 789, 118±125.
Matelli, M., Govoni, P., Galletti, C., Kutz, D.F. & Luppino, G. (1998) Superior
area 6 afferents from the superior parietal lobule in the macaque monkey.
J. Comp. Neurol., 402, 327±352.
Matelli, M., Luppino, G. & Rizzolatti, G. (1985) Patterns of cytochrome
oxidase activity in the frontal agranular cortex of macaque monkey. Behav.
Brain Res., 18, 125±137.
Matelli, M., Luppino, G. & Rizzolatti, G. (1991) Architecture of superior and
mesial area 6 and of the adjacent cingulate cortex. J. Comp. Neurol., 311,
445±462.
Maunsell, J.H.R. & Van Essen, D.C. (1983) The connections of the middle
temporal visual area (MT) and their relationship to a cortical hierarchy in
the macaque monkey. J. Neurosci., 3, 2563±2586.
Mesulam, M.-M. (1982) Principles of horseradish peroxidase
neurohistochemistry and their applications for tracing neural pathways. In
Mesulam, M.-M. (ed.), Tracing Neural Connections with Horseradish
Peroxidase. Wiley, Chichester, pp. 1±152.
Perrett, D.I., Harries, M.V., Bevan, R., Thomas, S., Benson, P.J., Mistlin, A.J.,
Chitty, A.J., Hietanen, J.K. & Ortega, J.E. (1989) Framework of analysis for
the neural representation of animate objects and actions. J. Exp. Biol., 146,
87±113.
Rizzolatti, G., Luppino, G. & Matelli, M. (1998) The organization of the
cortical motor system: new concepts. Electroencephalogr. Clin.
Neurophysiol., 106, 283±296.
Schlag, J. & Schlag-Rey, M. (1987) Evidence for a supplementary eye ®eld. J.
Neurophysiol., 57, 179±200.
Seltzer, B. & Pandya, D.N. (1978) Afferent cortical connections and
architectonics of the superior temporal sulcus and surrounding cortex in
the rhesus monkey. Brain Res., 149, 1±24.
Seltzer, B. & Pandya, D.N. (1989) Frontal lobe connections of the superior
temporal sulcus in the rhesus monkey. J. Comp. Neurol., 281, 97±113.
Stuphorn, V., Taylor, T.L. & Schall, J.D. (2000) Performance monitoring by
the supplementary eye ®eld. Nature, 408, 857±860.
Tanji, J., Shima, K. & Mushiake, H. (1996) Multiple cortical motor areas and
temporal sequencing of movements. Cognitive Brain Res., 5, 117±122.
Ungerleider, L.G. & Desimone, R. (1986a) Projections to the superior
temporal sulcus from the central and peripheral representations of V1 and
V2. J. Comp. Neurol., 248, 147±163.
Ungerleider, L.G. & Desimone, R. (1986b) Cortical projections of visual area
MT in the macaque. J. Comp. Neurol., 248, 190±222.
ã 2001 Federation of European Neuroscience Societies, European Journal of Neuroscience, 14, 1035±1040