Lateral Cervical Nucleus Projections to
Periaqueductal Gray Matter in Cat
LEONORA J. MOUTON,
1
*
ESTHER-MARIJE KLOP,
1
JONAS BROMAN,
2
MENGLIANG ZHANG,
2
AND GERT HOLSTEGE
1
1
Department of Anatomy and Embryology, Faculty of Medical Sciences, Rijksuniversiteit
Groningen, 9713 AV Groningen, The Netherlands
2
Department of Physiological Sciences, Section for Neurophysiology,
BMC F10, S-221 84 Lund, Sweden
ABSTRACT
The midbrain periaqueductal gray matter (PAG) integrates the basic responses neces-
sary for survival of individuals and species. Examples are defense behaviors such as fight,
flight, and freezing, but also sexual behavior, vocalization, and micturition. To control these
behaviors the PAG depends on strong input from more rostrally located limbic structures, as
well as from afferent input from the lower brainstem and spinal cord. Mouton and Holstege
(2000, J Comp Neurol 428:389 – 410) showed that there exist at least five different groups of
spino-PAG neurons, each of which is thought to subserve a specific function. The lateral
cervical nucleus (LCN) in the upper cervical cord is not among these five groups. The LCN
relays information from hair receptors and noxious information and projects strongly to the
contralateral ventroposterior and posterior regions of thalamus and to intermediate and deep
tectal layers. The question is whether the LCN also projects to the PAG. The present study
in cat, using retrograde and anterograde tracing techniques, showed that neurons located in
the lateral two-thirds of the LCN send fibers to the lateral part of the PAG, predominantly at
rostrocaudal levels A0.6 –P0.2. This part of the PAG is known to be involved in flight
behavior. A concept is put forward according to which the LCN-PAG pathway alerts the
animal about the presence of cutaneous stimuli that might represent danger, necessitating
flight. J. Comp. Neurol. 471:434 – 445, 2004. © 2004 Wiley-Liss, Inc.
Indexing terms: emotional motor system; spinomesencephalic; spinocervical; somatosensory;
tectum; colliculus superior
The mesencephalic periaqueductal gray matter (PAG)
plays an important role in the emotional motor system
(Holstege, 1997). Stimulation of the PAG in rat and cat
can elicit analgesia and integrated emotional behaviors
such as threat display, fight, flight, immobility, vocaliza-
tion, micturition, and mating behavior (Sakuma and Pfaff,
1979; Bandler and Depaulis, 1991; Carrive, 1993; Blok
and Holstege, 1996). Also, human electrical stimulation in
the PAG can achieve pain relief, but also feelings of ap-
prehension and impending doom (Richardson and Akil,
1977; Young et al., 1985). To elicit these emotional behav-
iors, the PAG not only receives strong input from more
rostrally located limbic and prefrontal structures, but also
from the lower brainstem and spinal cord. Regarding the
afferent projections from the spinal cord, retrograde trac-
ing studies in many different species showed that all spi-
nal segments contain neurons that send fibers to the PAG
(rat: Beitz, 1982; Menetrey, 1982; Liu, 1983; Harmann,
1988; Lima and Coimbra, 1989; Bernard et al., 1995; rab-
bit: Meller, 1986; cat: Wiberg and Blomqvist, 1984;
Blomqvist and Craig, 1991; Keay and Bandler, 1992;
VanderHorst et al., 1996; Mouton et al., 1997; Mouton and
Holstege, 2000; Mouton et al., 2001; monkey: Mantyh,
1982; Wiberg et al., 1987; Zhang et al., 1990; Blomqvist
and Craig, 1991; VanderHorst et al., 2002). Mouton and
Holstege (2000) showed that in cat over 90% of the spino-
PAG neurons are located in specific clusters. About 50% is
Grant sponsor: Swedish Research Council; Grant number: 14276.
*Correspondence to: L.J. Mouton, Department of Anatomy and Embry-
ology, Faculty of Medical Sciences, Rijksuniversiteit Groningen, A. Deus-
inglaan 1, 9713 AV Groningen, The Netherlands.
E-mail: L.J.Mouton@med.rug.nl
Received 16 September 2003; Revised 23 November 2003; Accepted 27
November 2003
DOI 10.1002/cne.20031
Published online the week of March 1, 2004 in Wiley InterScience (www.
interscience.wiley.com).
THE JOURNAL OF COMPARATIVE NEUROLOGY 471:434 – 445 (2004)
© 2004 WILEY-LISS, INC.