Direct Projections From the Dorsal Premotor Cortex to the Superior Colliculus in the Macaque (Macaca mulatta) Claudia Distler 1 * and Klaus-Peter Hoffmann 1,2,3 1 Department of Zoology and Neurobiology, Ruhr-University Bochum, 44780 Bochum, Germany 2 Department of Animal Physiology, Ruhr-University Bochum, 44780 Bochum, Germany 3 Department of Neuroscience, Ruhr-University Bochum, 44780 Bochum, Germany ABSTRACT The dorsal premotor cortex (PMd) is part of the cortical network for arm movements during reach-related behavior. Here we investigate the neuronal projections from the PMd to the midbrain superior colliculus (SC), which also contains reach-related neurons, to investi- gate how the SC integrates into a cortico-subcortical network responsible for initiation and modulation of goal-directed arm movements. By using anterograde transport of neuronal tracers, we found that the PMd projects most strongly to the deep layers of the lateral part of the SC and the underlying reticular formation corresponding to locations where reach-related neurons have been recorded, and from where descending tecto- fugal projections arise. A somewhat weaker projection targets the intermediate layers of the SC. By contrast, terminals originating from prearcuate area 8 mainly pro- ject to the intermediate layers of the SC. Thus, this pro- jection pattern strengthens the view that different compartments in the SC are involved in the control of gaze and in the control or modulation of reaching movements. The PMD–SC projection assists in the par- ticipation of the SC in the skeletomotor system and provides the PMd with a parallel path to elicit forelimb movements. J. Comp. Neurol. 000:000–000, 2015. V C 2015 Wiley Periodicals, Inc. INDEXING TERMS: dorsal premotor; corticotectal; eye–hand coordination; sensorimotor; reaching; AB_2336827; AB_2315331 Reaching and grasping are everyday activities for all dexterous mammals including humans. Research during the last decades in primates has revealed a widespread network of brain areas involved in various aspects of these actions. In the cerebral cortex, the main players are the primary motor cortex (M1), premotor cortex (PM), and posterior parietal cortex (area 5, AIP and MIP), with their cortical input from visual, somatosen- sory, and prefrontal cortex (Johnson et al., 1996; Hoshi and Tanji, 2007; Padberg et al., 2007; Kaas et al., 2012, 2013 and references therein). Based on electro- physiological recordings, microstimulation, and anatomi- cal investigations, all these areas display topographic organization that, however, is somewhat crude in the premotor and posterior parietal cortex. This led to the concept of functional zones interconnected within and between relevant cortical areas, which would then together control the various sectors, joint angles, orien- tation, etc. of the forelimb during certain movements (Seelke et al., 2012; Kaas et al., 2012, 2013). On functional and anatomical grounds, the premotor cortex (Brodman area 6) can be divided in dorsal (PMd, F2, F7) and ventral (PMv, F4, F5) compartments (Matelli et al., 1985). Area PMv (F5) is mainly connected with the ventral portion of the dorsolateral prefrontal cortex (DLPC) and with the inferior parietal lobule, especially area AIP and PF (Luppino et al., 1999; Hoshi and Tanji, 2007; Borra et al., 2008; Gharbawie et al., 2011). Func- tionally, the PMv is involved in the preparation and exe- cution of arm and hand movements related to grasping and contains not only neurons related to the subject’s own actions but to actions of others (mirror neurons) Grant sponsor: the Deutsche Forschungsgemeinschaft; Grant number: Ho 450/25; Grant sponsor: ZEN grant from the Hertie Stiftung (to K.P.H.). *CORRESPONDENCE TO: Claudia Distler, Allgemeine Zoologie und Neu- robiologie, Ruhr-University Bochum, Universitaetsstr. 150, ND 7/26, 44780 Bochum, Germany. E-mail: [email protected]Received January 21, 2015; Revised March 31, 2015; Accepted April 15, 2015. DOI 10.1002/cne.23794 Published online Month 00, 2015 in Wiley Online Library (wileyonlinelibrary.com) V C 2015 Wiley Periodicals, Inc. The Journal of Comparative Neurology | Research in Systems Neuroscience 00:00–00 (2015) 1 RESEARCH ARTICLE
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Direct Projections From the Dorsal PremotorCortex to the Superior Colliculus in theMacaque (Macaca mulatta)
Claudia Distler1* and Klaus-Peter Hoffmann1,2,3
1Department of Zoology and Neurobiology, Ruhr-University Bochum, 44780 Bochum, Germany2Department of Animal Physiology, Ruhr-University Bochum, 44780 Bochum, Germany3Department of Neuroscience, Ruhr-University Bochum, 44780 Bochum, Germany
ABSTRACTThe dorsal premotor cortex (PMd) is part of the cortical
network for arm movements during reach-related
behavior. Here we investigate the neuronal projections
from the PMd to the midbrain superior colliculus (SC),
which also contains reach-related neurons, to investi-
gate how the SC integrates into a cortico-subcortical
network responsible for initiation and modulation of
goal-directed arm movements. By using anterograde
transport of neuronal tracers, we found that the PMd
projects most strongly to the deep layers of the lateral
part of the SC and the underlying reticular formation
corresponding to locations where reach-related neurons
have been recorded, and from where descending tecto-
fugal projections arise. A somewhat weaker projection
targets the intermediate layers of the SC. By contrast,
terminals originating from prearcuate area 8 mainly pro-
ject to the intermediate layers of the SC. Thus, this pro-
jection pattern strengthens the view that different
compartments in the SC are involved in the control of
gaze and in the control or modulation of reaching
movements. The PMD–SC projection assists in the par-
ticipation of the SC in the skeletomotor system and
provides the PMd with a parallel path to elicit forelimb
Reaching and grasping are everyday activities for all
dexterous mammals including humans. Research during
the last decades in primates has revealed a widespread
network of brain areas involved in various aspects of
these actions. In the cerebral cortex, the main players
are the primary motor cortex (M1), premotor cortex
(PM), and posterior parietal cortex (area 5, AIP and
MIP), with their cortical input from visual, somatosen-
sory, and prefrontal cortex (Johnson et al., 1996; Hoshi
and Tanji, 2007; Padberg et al., 2007; Kaas et al.,
2012, 2013 and references therein). Based on electro-
physiological recordings, microstimulation, and anatomi-
cal investigations, all these areas display topographic
organization that, however, is somewhat crude in the
premotor and posterior parietal cortex. This led to the
concept of functional zones interconnected within and
between relevant cortical areas, which would then
together control the various sectors, joint angles, orien-
tation, etc. of the forelimb during certain movements
(Seelke et al., 2012; Kaas et al., 2012, 2013).
On functional and anatomical grounds, the premotor
cortex (Brodman area 6) can be divided in dorsal (PMd,
F2, F7) and ventral (PMv, F4, F5) compartments (Matelli
et al., 1985). Area PMv (F5) is mainly connected with
the ventral portion of the dorsolateral prefrontal cortex
(DLPC) and with the inferior parietal lobule, especially
area AIP and PF (Luppino et al., 1999; Hoshi and Tanji,
2007; Borra et al., 2008; Gharbawie et al., 2011). Func-
tionally, the PMv is involved in the preparation and exe-
cution of arm and hand movements related to grasping
and contains not only neurons related to the subject’s
own actions but to actions of others (mirror neurons)
Grant sponsor: the Deutsche Forschungsgemeinschaft; Grant number:Ho 450/25; Grant sponsor: ZEN grant from the Hertie Stiftung (toK.P.H.).
*CORRESPONDENCE TO: Claudia Distler, Allgemeine Zoologie und Neu-robiologie, Ruhr-University Bochum, Universitaetsstr. 150, ND 7/26,44780 Bochum, Germany. E-mail: [email protected]
Received January 21, 2015; Revised March 31, 2015;Accepted April 15, 2015.DOI 10.1002/cne.23794Published online Month 00, 2015 in Wiley Online Library(wileyonlinelibrary.com)VC 2015 Wiley Periodicals, Inc.
The Journal of Comparative Neurology | Research in Systems Neuroscience 00:00–00 (2015) 1
RESEARCH ARTICLE
(Rizzolatti et al., 1988; Kakei et al., 2001; Ochiai et al.,
2005; Raos et al., 2006; Hoshi and Tanji, 2007; Theys
et al., 2012; Lehmann and Scherberger, 2013; Bonini
et al., 2014).
By contrast, PMd is connected with the dorsal DLPC
and the dorsal parietal lobule including area 5 and the
MIP. Namely, the caudal part of the PMd (F2 dimple
region and F2 ventrorostral of Matelli et al., 1998;
cPMd of Ghosh and Gattera, 1995) receives its main
input from parietal areas PEc and PEip (F2 dimple), and
the MIP and V6A (F2 ventrorostral), respectively, as
well as from frontal areas SMA, M1, and the cingulate
motor areas (Ghosh and Gattera, 1995; Matelli et al.,
1998). It is also involved in the preparation and execu-
tion of arm movements but shows preparatory activity
and codes for direction, speed, and amplitude of the
arm movement during reaching and eye–hand coordina-
tion (Barbas and Pandya, 1987; Colby et al., 1988; Fu
et al., 1995; Tann�e et al., 1995; Johnson et al., 1996;
Matelli et al., 1998; Messier and Kalaska, 2000; Lup-
pino et al., 2003; Churchland et al., 2006; Pesaran
et al., 2006, 2010; Hoshi and Tanji, 2007; Yamagata
et al., 2012).
Electrical microstimulation in the PMd leads to move-
ments of the upper limb but at significantly higher
thresholds than in the M1 (Weinreich and Wise, 1982;
Preuss et al., 1996; Fujii et al., 2000; Raos et al.,
2003). A systematic survey of the dorsal premotor cor-
tex revealed a topographic order of evoked movements
with simple movements of the contralateral shoulder
mostly elicited from areas close to the precentral dim-
ple, and simple movements of the contralateral distal
forelimb mostly elicited more laterally close to the spur
of the arcuate. In addition, neurons close to the dimple
were mostly active during movements and somatosen-
sory stimulation of the arm, whereas neurons close to
the spur were active during movement and somatosen-
sory stimulation of the distal forelimb (Raos et al.,
2003). About half of the neurons were active during
grasping, and about 37% were active during reaching.
This forelimb-related region contains visual, somatosen-
sory, purely motor, visually modulated, and visuomotor
neurons (Fogassi et al., 1999; Raos et al., 2004). Elec-
trical stimulation of the PMd resulted more often in
suppression (50% of events) in upper limb muscles than
stimulation of the SMA or M1 (20% of events) (Mont-
gomery et al., 2013). With longer stimulation periods
(500 ms), complex and more naturalistic movements of
the arm could be evoked from the PMd (Graziano et al.,
2002).
In recent years, reach-related activity has also been
identified in neurons of the intermediate and deep
layers of the midbrain superior colliculus (SC). These
reach neurons are active before and during arm move-
ments, and their activity is correlated with the direction
of arm movements (Kutz et al., 1997) and/or with the
electromyogram of proximal shoulder and arm muscles
(Werner, 1993; Werner et al., 1997a, b; Stuphorn et al.,
1999, 2000). Furthermore, microstimulation at record-
ing sites of these reach neurons elicits arm movements
(Philipp and Hoffmann, 2014).
The SC receives input from multiple cortical areas.
The superficial layers are targeted mainly by early visual
areas, whereas intermediate and deep layers receive
input from the posterior parietal cortex including the
lateral intraparietal area (LIP), forelimb representation
Abbreviations
A aqueductA8 area 8Amt anterior mediotemporal sulcusAr arcuate sulcusBSC brachium of the superior colliculusCa calcarine sulcusCe central sulcusCi cingulate sulcusDMZ densely myelinated zone of the medial superior temporal areaDpc decussatio pedunculi cerebellarisec ectocalcarine sulcusFEF frontal eye fieldflm fasciculus longitudinalis medialisIC inferior colliculusio infero-occipital sulcusip intraparietal sulcusla lateral sulcusLIP lateral intraparietal areall lemniscus lateralislu lunate sulcusM2 motor area 2MIP medial intraparietal areaMT middle temporal areaNPo n. pontisNRm n. reticularis mesencephaliNRp n. reticularis parvocellularisNRpo n. reticularis pontis oralis
Nru n. ruberNTr n. trapeziusot occipito-temporal sulcusp principal sulcusPAG periaqueductal greypc pedunculus cerebripca pedunculus cerebellaris anteriorpcd precentral dimplepo parieto-occipital sulcusPt pretectumPul pulvinarRd raphe dorsalisSC superior colliculusSN substantia nigraSGI stratum griseum intermedium of the SCSGP stratum griseum profundum of the SCSGS stratum griseum superficiale of the SCSt superior temporal sulcusVIP ventral intraparietal areaV1 primary visual cortexV4t visual area 4 transitional zoneV6 visual area 6V6A visual area 6AIII n. oculomotoriusIV n. trochlearis3a 4, 5, 6, 7a, 8, 23, 24, Brodman areas 3a, 4, 5, 6, 7a, 8, 23, 245v ventral area 5
C. Distler and K.-P. Hoffmann
2 The Journal of Comparative Neurology |Research in Systems Neuroscience
of areas 2, 4, and 6, FEF, PMv, and prefrontal cortex
(Finlay et al., 1976; Kuenzle et al., 1976; Leichnetz
et al., 1981; Fries, 1984, 1985; Komatsu and Suzuki,
1985; Lynch et al., 1985; Lock et al., 2003; Borra
et al., 2014; Cerkevich et al., 2014).
Only in some instances have these anatomical con-
nections been characterized physiologically. The cortico-
tectal projection originating from the primary visual
cortex seems to be involved in the control of intracollic-
ular visual processing (Finlay et al., 1976). The FEF pro-
jection to the SC mainly carries saccade-related and
visual information about the central visual field (Seg-
raves and Goldberg, 1987). By contrast, tectal projec-
tions from the LIP carry mostly visual saccade-related
information from the peripheral field (Par�e and Wurtz,
1997; Gaymard et al., 2003). In contrast, projections
from the dorsolateral prefrontal cortex transmit task-
selective signals to the SC, i.e., neuronal signals selec-
tive for antisaccades that inhibit reflexive prosaccades
(Johnston and Everling, 2006). To date, only little data
for the premotor-tectal projections are available. Electri-
cal microstimulation revealed excitatory as well as
inhibitory influences of the PMd on forelimb muscles
(Montgomery et al., 2013). We presume that at least
part of the PMd output is mediated indirectly, e.g., via
subcortical nuclei including the SC. In a preliminary
ACKNOWLEDGMENTSWe thank E. Brockmann, S. Dobers, H. Korbmacher,
and G. Reuter for expert technical assistance. We are also
grateful to H. L€ubbert for lab space.
CONFLICT OF INTEREST STATEMENT
The authors state they have no conflicts of interest.
ROLE OF AUTHORS
All authors had full access to all the data in the
study and take responsibility for the integrity of the
data and the accuracy of the data analysis. Study con-
cept and design: KPH and CD, acquisition of data: KPH
and CD, analysis and interpretation of data: CD and
KPH, drafting of the manuscript: CD and KPH.
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Direct projections of PMd to superior colliculus
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