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Department of Anatomy, Histology and Embryology, Medical University of Soa, 1431 Soa, Bulgaria
Department of Chemistry, Biochemistry, Physiology and Pathophysiology, Soa University St. Kliment Ohridski, 1407 Soa, Bulgaria
Department of Anatomy, Histology and Embryology, Medical University of Varna, 9002 Varna, Bulgaria
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Medimark Corporation, P.O. Box 2316, Del Mar, CA 92014, USA
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c
A R T I C L E I N F O
A B S T R A C T
Article history:
Received 19 May 2014
Received in revised form 15 August 2014
Accepted 16 August 2014
Available online 23 August 2014
The claustrum is a telencephalic nucleus located ventrolateral to the basal ganglia in the mammalian
brain. It has an extensive reciprocal connectivity with most if not all of the cerebral cortex, in particular,
primary sensory areas. However, despite renewed and growing interest amongst investigators, there
remains a paucity of data concerning its peptidergic prole. The aim of the present study was to examine
the presence, morphology, distribution and ultrastructure of neuropeptide Y-immunoreactive (NPY-ir)
neurons and bers in the claustrum of the cat. Ten adult healthy cats from both sexes were used. All
animals received human and ethical treatment in accordance with the Principles of Laboratory Animal
Care. Subjects were irreversibly anesthetized and transcardially perfused with xative solution
containing glutaraldehyde and paraformaldehyde. Brains were promptly removed, postxed and
sectioned. Slices were incubated with polyclonal anti-NPY antibodies according to the standard avidin
biotinperoxidase complex method adopted by our Department of Anatomy, Histology and Embryology.
NPY-ir neurons and bers were found to be diffusely distributed throughout the claustrum, with no
obvious topographic or functional patterning other than larger numbers in its central/broadest part
(stereotaxic planes A12A16). Neurons were generally classied by diameter into three sizes: small
(under 17 mm), medium (1725 mm) and large (over 25 mm). Staining density is varied with some
neurons appearing darker than others. At the electron-microscopic level NPY immunoproduct was
observed within neurons, dendrites and terminal boutons, each differing relative to their ultrastructural
attributes. Two types of NPY-ir synaptic boutons were found. Lastly, it is of interest to note that genderspecic differences were not observed.
2014 Elsevier B.V. All rights reserved.
Keywords:
Cat
Claustrum
Neuropeptide Y
Light microscopy
Electron microscopy
Ultrastructure
1. Introduction
The claustrum is a telencephalic nucleus in the mammalian
brain that has long been known as a site of extensive reciprocal
heterosensory convergence (Olson and Graybiel, 1980; Ashwell
et al., 2004; Hinova-Palova et al., 2007, 2008). Typically, it is
subdivided into the dorsal claustrum (or insular claustrum) and
ventral claustrum (or endopiriform nucleus) (Guirado et al.,
2003; Edelstein and Denaro, 2004a; Ashwell et al., 2004). The
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3. Results
3.1. Light microscopy
Neurons and bers immunopositive for NPY-ir were found
throughout the claustrum, from rostral to caudal planes (Figs. 1
and 2). In general, the NPY-ir neurons were typically stained with
immunoproduct visible in the cell cytoplasm and processes, while
the nucleus remained free of label (Fig. 3). Labeling intensity,
however, varied. Some neurons were lightly stained (Fig. 4), while
in others the staining was so dense that they appeared as if they
were silver impregnated (Fig. 5). Immunopositive neurons were
also found proximal to and within the external and extreme
capsules (Fig. 6).
Although NPY-ir neurons were seen throughout the claustrum,
their distribution displayed a lack of uniformity. Based on our
morphometric analysis, approximately 70% of labeled cells were
located in stereotaxic planes A12A16. Of these cells, the majority
appeared clustered within the claustrums central triangle region
(planes A13A15; Fig. 7), with but a handful found proximal to the
external and extreme capsules. Most commonly, the neurons were
situated parallel to the ber tracts, though some were positioned in
a perpendicular fashion. Moving caudally, the number of NPY-ir
neurons gradually diminished (Fig. 8), and at the level of
stereotaxic planes A10A11 only 15% of all counted NPY-ir
neurons were identied. Approximately 10% of all NPY-ir neurons
Fig. 1. Coronal section through claustrum in different planes from rostral to caudal:
(A) 19 mm in front of the interaural line (arrows delineate claustrum). Nissl staining
20; (B) 15 mm in front of the interaural line (arrows delineate claustrum). Nissl
staining 20; (C) 11 mm in front of the interaural line (arrows delineate claustrum).
Nissl staining 20.
109
Fig. 2. Schematic drawings of 5 coronal sections through the cat claustrum showing
the distribution of NPY-positive neurons (black dots) from rostral to caudal planes.
Cn caudate nucleus, Ic internal capsule, Put putamen, Sp septum pellucidum,
Pal pallidum (globus pallidus), Amg amygdala, Th thalamus, Ac anterior
commissure, Hy hypothalamus, Ent entopeduncular nucleus, NII second
cranial nerve (optic).
110
Fig. 5. Large spiny NPY-positive darkly stained neuron with long dendrites. Scale
bar = 50 mm.
Fig. 8. Low magnication of the caudal part of claustrum showing a lesser number
of NPY-positive neurons. Scale bar = 1 mm.
Fig. 9. Large spiny NPY-positive neuron with fusiform cell body. Scale bar = 50 mm.
Fig. 10. Large spiny pear-shaped NPY-positive neuron. Scale bar = 50 mm.
111
Fig. 12. Small spiny NPY-positive neurons with long spiny dendrites. Scale
bar = 50 mm.
Fig. 11. Two medium spiny NPY-positive neurons with long bifurcated dendrites
rich with spines. Scale bar = 50 mm.
Fig. 13. Large aspiny NPY-positive neuron with long prominent bulbous dendrites
(arrows show the varicosities) Scale bar = 50 mm.
Fig. 14. Medium aspiny multipolar NPY-positive neuron with varicose dendrites
(arrows). Scale bar = 50 mm.
112
Fig. 15. Small aspiny elliptical NPY-positive neuron with short varicose dendrites.
Scale bar = 50 mm.
Fig. 16. Two dwarf cells with irregular cell bodies and intensely branching short
varicose dendrites (arrows). Scale bar = 50 mm.
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Fig. 19. Two small NPY-positive neurons. One of them contains heavy a deposition
of immunoproduct (D), the other, less so (L). Scale bar = 5 mm.
Fig. 20. Large NPY-positive dendrite (D) on which terminate two unlabeled boutons
(T). Scale bar = 1 mm.
Fig. 21. Large NPY-positive dendrite (D) on which terminates a large NPY-positive
synaptic terminal (T). Scale bar = 0.5 mm.
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Fig. 24. Labeled NPY-positive large round synaptic bouton (T) terminates on two
unlabeled medium dendrites (D). Scale bar = 1 mm.
Fig. 22. NPY-positive terminal bouton (T) establishes synaptic contact with a large
labeled NPY-positive dendrite (D). Scale bar = 1 mm.
Fig. 23. NPY-positive dendrite (D) on which terminate two unlabeled boutons (T).
Scale bar = 2 mm.
Fig. 25. Labeled NPY-positive bouton (T) contacting an NPY-positive neuron. Scale
bar = 1 mm.
4. Discussion
To the best of our knowledge, the present study is the rst to
provide detailed insight into the topographical distribution and
morphological characteristics of NPY-ir neurons in the cat
claustrum at the light- and electron-microscopic level. Overall,
our ndings are consistent with those reported for the squirrel
monkey, Saimir sciureus (Smith et al., 1985), cat (Edelstein et al.,
2011b) and human (Edelstein et al., 2010) in which NPY-ir neurons
were recognized in the claustrum of those species.
In this investigation, we report the existence of at least seven
readily distinguishable types of NPY-ir neurons in the cat
Fig. 26. NPY-positive dendrites (D) and terminal boutons of differing size and shape
(arrows). Scale bar = 1 mm.
Fig. 27. Heavy labeled en passant NPY-positive bouton (arrows) terminates on the
periphery of an NPY-positive neuron. Scale bar = 2 mm.
115
116
neuronal excitability, cardiovascular homeostasis, hormone secretion and circadian rhythms (Baraban et al., 1997; Colmers and
Bleakman, 1994; Hokfelt et al., 1998; Inui, 1999; Munglani et al.,
1996; Vezzani et al., 1999; Wahlested and Reis, 1993). In addition,
it has been suggested that NPY plays a role in psychiatric disorders
including depression, eating disorders, anxiety and epilepsy
(Baraban et al., 1997; Colmers and Bleakman, 1994; Grundemar
et al., 1992; Hokfelt et al., 1998; Munglani et al., 1996; Wahlested
and Reis, 1993). What more, hypothalamic injections of NPY
increase food intake (Stanley and Leibowitz, 1985); in the
hippocampus, NPY has been suggested as an endogenous antiepileptic (Colmers et al., 1991); in the cortex NPY is co-expressed in
many inhibitory GABAergic neurons that modulate pyramidal cell
function in the other regions of the brain (Kubota et al., 2011); NPY
cells play a role in cardiovascular function and emotion (Colmers
and Wahlested, 1993).
From a clinical perspective, given that the claustrum and NPY
have been implicated in the development, symptoms and/or
sequelae of serious maladies such as autism, schizophrenia,
epilepsy, Alzheimers disease, Parkinsons disease, and Huntingtons disease (Wegiel et al., 2014; Cascella and Sawa, 2014; Venneri
and Shanks, 2014; Kalaitzakis, 2014; Corcoran, 2004; Halliday
et al., 1990; Koide et al., 1995; Croom and Taylor, 2001; Flint and
Martin, 1986; Ramos et al., 2006), it behooves both basic and
clinical investigators to learn as much as possible about the
interplay between the two.
5. Conclusion
In conclusion, this is the rst detailed investigation of the light
and electron-microscopic features of NPY-ir neurons and bers in
the cat claustrum. It is hoped that our results and wide-ranging
discussion will provide deeper insight into the functional
neuroanatomy of the claustrum, further elucidating its involvement with a host of critical physiological parameters and biologic
processes, especially those impacted by the aforementioned
neurological disorders. Lastly, much work remains to be done in
terms of studying the claustrum from an ontogenetic and
phylogenetic perspective, with respect to homologues in nonmammalian species as well as its contribution in the context of
higher cortical functions and prevalent hypotheses (Smythies
et al., 2012, 2014a,b). In this regard, it must be mentioned that one
of the greatest minds in modern biology, the late Nobel laureate
and co-discoverer of the structure of DNA, Francis Crick, spent the
last hours of his remarkable life dictating corrections to a draft of
what was to become his nal paper, entitled What is the function
of the claustrum? (Crick and Koch, 2005; Edelstein and Denaro,
2004b). Francis Crick and his co-author Christof Koch have laid the
foundation for future investigative efforts into the claustrums
putative role in that most complex and elusive of neurophysiologic
attributes, consciousness.
Ethical statement
All animals in this study were afforded human care in
compliance with the Principles of Laboratory Animal Care
formulated by the National Society for Medical Research and the
Guide for the Care and Use of Laboratory Animals prepared by
the National Institutes of Health (NIH publication No. 86-23,
revised 1996).
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