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Schwerdtfeger, Smeets (eds.), The Forebrain of Reptiles. Int. Symp. Recent Advances in Understanding the
Structure and Function of the Forebrain in Reptiles, Frankfurt/M. 1987, pp. 162-177 (Karger, Basel 1988)
The Reptilian Striatum Revisited:
Studies on
Anolis
Lizards'
Neil Greenbergs, Enrique Fonts, Robert C. Switzer, 111b
,
2
aLaboratory of Physiological Ethology, Department of Zoology and Life Sciences
Graduate Program in Ethology; bUniversíty of Tennessee Memorial Health
Research Center, University of Tennessee, Knoxville, Tenn., USA
Within the reptilian forebrain, beneath the prominent anterior dorsal
ventricular ridge, is an array of nuclei some of which are now regarded as
the only truly striatal structures in the forebrain [3]. Although these struc-
tures are often homologized to mammalian basal ganglia, recently shown to
mediate complex behavioral functions (see below), little has been pub-
lished in recent years to resolve the lack of agreement on its subdivisions or
to determine its functions in reptiles [34, 44]. Nevertheless, there are
indications that beyond a clarification of this intrinsically fascinating prob-
lem, two of the ambitions of comparative neurobiology may be partly
realized: An understanding of the basal forebrain of reptiles will illuminate
dark corners of our understanding of the range of the possible mechanisms
of evolutionary change and thereby provide a sense of the intrinsic struc-
tural constraints on the organization of our own brain. Also, this under-
standing may contribute to the development of new animal models and the
identification of `natural experiments' that will clarify areas of human
cerebral function and dysfunction.
The research agenda that is most likely to fulfill these promises takes
impetus from new histochemical techniques to supplement traditional
neuroanatomical methods in concert with detailed and discriminating
1
This work was made possible by a University of Tennessee Faculty Research Grant
and by NSF grant
BIS-
8406028 to Neil Greenberg.
2
We are grateful for Dr. Edward F. O'Connor's thoughtful assistance with the histo-
fluorescence procedures.
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163
ethological analyses of the motor patterns associated with specific neural
sites and their physiology.
This report will first review our limited understanding of behavioral
dysfunction following destruction of selected striatal sites in reptiles, and
then introduce new findings regarding the organization of the striatum in
the lizard,
Anolis carolinensis,
as indicated by correlating the effects of
systemic administration of the dopaminergic neurotoxin IPTP, the find-
ings of catecholamine histofluorescence, and the distribution of acetylcho-
linesterase in the basal forebrain.
Behavioral Functions of the Striatum
From his review of the complex functions of mammalian basal ganglia,
Teuber [54] was convinced that, along with motor difficulties, their impair-
ment resulted in characteristic perceptual and cognitive deficits. Similarly,
Schneider [47] concluded from psychiatric evidence that the basal ganglia
play a profound role in attention structure and sensory gating. In Divac's
[ 11 ] attempt to reconcile conflicting views of neostriatal function, he found
that even though there was topographic evidence for independent function-
al units of neostriatal areas receiving specific neocortical afferents, the
uniformity of neostriatal cytoarchitecture indicates that these units con-
ducted neural processing of information in comparable ways. This view, in
concert with the position of the neostriatum in the chain of neocortical
control of motor mechanisms, converged on the idea that the neostriatum
intermediates between cognition and action. In this regard it is interesting
that Cools and van der Bercken [9] regarded the neostriatum as the substrate
of high-order information processing needed to link two or more behavioral
acts to form an integrated behavioral program [8].
Can we penetrate appearances, misconceptions, and the tangled
nomenclature to the underlying common features that could link the mam-
malian literature with findings in reptiles? In their analysis of the paleo-
striatal system (PS) of
Caiman
and their comparison of this typically
reptilian PS with both avian PS and mammalian basal ganglia, Brauth and
Kitt [5] concluded that overall design and possibly function are comparable
in these three taxa and indicate a common function in spatial orientation
and attention. Such insights, converging with our increasing knowledge of
the stimulus control and adaptive functions of behavior, present neuroe-
thology with a compelling agenda.
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164
Species-Typical Stereotyped Behavior
Highly stereotyped, species-typical behavioral patterns, particularly
social displays, have provided the most robust data to illuminate neural
corollaries of complex behavioral functions. MacLean [28] demonstrated
that lesions of the globus pallidus in the area where fibers converge to form
the ansa lenticularis, or of the ansa itself, impaired a species-typical display
in the squirrel monkey, probably by interrupting the pallidal projection to
the tegmental area.
Behavioral Functions of the Reptilian Striatum
MacLean's [28] finding that the integrity of the striatum is necessary for
the performance of a species-typical display in the monkey encouraged an
investigation of the paleostriatum of a lizard predicated on a close under-
standing of the units of behavior spontaneously emitted in naturalistic
settings. The green anole,
Α.
carolinensis,
was selected because of its avail-
ability, ease of maintenance, and extent of knowledge of its biology and
ecology.
Α
preliminary brain atlas was prepared as well as an ethogram that
operationally distinguished individual units of stereotyped behavior that
could be elicited under controlled conditions [ 14, 15]. The most robust of
the stereotyped behavioral patterns are the social displays termed assertion
(a `general arousal') display consisting mainly of push-ups and dewlap
extension, challenge (much like assertion but adressed to a conspecific male
and incorporating a sagittal expansion of the body profile), and courtship
(like assertion but addressed to a female and with the added element of rapid
head-nodding).
Electrolytic (radiofrequency) lesions were stereotactically placed in the
forebrains of territorial male lizards. Lesions were unilaterally placed to
exploit the fact that in this species, there is an almost complete decussation
of the optic tracts [6]. By testing animals with stimuli selectively restricted to
one eye by means of a rubber eye-patch, each subject effectively functioned
as its own control.
During subsequent testing by exposure of the lesioned subject to the
sight of an aggressive male in an adjacent chamber, those subjects that had
lesions involving the lateral forebrain bundle demonstrated deficits in the
species-typical challenge display [ 18], but general arousal and courtship
displays [20] were unaffected. Greenberg [ 14] characterized the behavioral
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Ano/is
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165
profile of lizards showing such deficits as an inability to recognize appro-
priate stimulus input, a difficulty sometimes characterized as `social agno-
sia'. Interestingly, a striatal role in visual discrimination was already indi-
cated by a lesion study of the forebrain of the turtle,
Chrysemys
[43].
Other findings indicative of striatal function in reptiles may be found in
studies in which many areas of the brain were explored by electrical
stimulation. In the brain of
Iguana iguana,
Distel [ 10] found that some
tongue-flicking behavior was elicited by stimulation of the lateral striatal
area, but the stimulation of more medial sites resulted in the greatest
number of such responses of any site investigated, possibly due to the
proximity to olfactory structures. Locomotion was occasionally elicited but
no stereotyped responses were detected. Work by Sugerman and Demski
[50] on another iguanid lizard species,
Crotaphytus co/tans,
did elicit ster-
eotyped agonistic behavior in response to electrical stimulation at several
sites that roughly formed a column from the telencephalon to the rhom-
bencephalon, but striatal sites were not tested. Tarr [53], on the other hand,
specifically stimulated st
ri
atal sites in the fence lizard,
Sceloporus occiden-
talis,
and observed stereotyped assertion displays at or near the tip of the
lateral ventricle-nucleus accumbens. Points eliciting the more complex
challenge displays, similar to those eliminated following Greenberg's pal-
eostriatal lesions, were just anterior and dorsal to the nucleus sphericus in
the posterior area of the dorsal ventricular ridge. Interpretation of stimu-
lation experiments is complicated, as Distel [ 10] has indicated, by the
difficulty in discriminating direct motor stimulation, sensory excitation,
motivational changes, or general arousal. Much the same criticism could be
levelled at lesion experiments, but still the techniques, in concert with
further knowledge of striatal anatomy, will help point the way to progres-
sively more specific hypotheses that can significantly inform future inves-
tigations of function.
Anatomy of the Striatum
Procedure.
The species employed was
Α.
carolinensis,
a common, easily obtainable
arboreal iguanid lizard found in the Southeastern United States. Adult male lizards were
commercially supplied from Southern Louisiana and individually housed in laboratory
vivaria under a photothermal regimen known to maintain activity. Water was provided
ad libitum and they were fed small crickets twice weekly. To prepare brains for Nissl and
fiber stains, the animals were treated according to the method described by Greenberg et
al. [18].
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166
NAcc v5t
Fig. 1. A. carolinensis
forebrain at the level of the magnocellular nucleus of the basal
forebrain (Nag). The main divisions of the corpus striatum are the medial, containing
nucleus
α
ccumbens (NAcc), and the lateral, containing two components, the dorsal stria-
tum (dSt) and the ventral striatum (vSt). ADVR = Anterior dorsal ventricular ridge;
Ν
LOT = nucleus of the lateral olfactory tract; Pal =
pallium;
Sep = septum. Small dots on
the labeled side indicate the distribution of terminal degeneration in the striatum subse-
quent to IPTP treatment. Four of 21 individuals also showed terminal degeneration in the
ADVR. Bar = 1 mm.
In the basal forebrain of A.
carolinensis,
much like in
Iguana
[32] and
other reptiles [34], two major divisions of the corpus striatum are recogniz-
able in Nissl-stained material (fig. 1): (1) a medial division consisting of a
compact, rounded group of small cells directly underneath the ventral tip of
the lateral ventricle and identified as nucleus
α
ccumbens by most workers
[15, 32, 33, 48], and (2) a lateral division or corpus striatum proper which
can be further subdivided into dorsal (dSt) and ventral (vSt) portions on the
basis of cell size and density. The cells in the dSt are medium to large in size
and exhibit a fairly dense packing. The comparatively cell-poor vSt lies
ventral to the dSt and is bounded medially by the nucleus
α
ccumbens. Three
cell types are recognizable in this striatal division: small rounded cells,
medium-size bipolar cells and giant polygonal cells. These giant cells form a
wedge in the central portion ofthe vSt and are intermingled among the fibers
of the lateral forebrain bundle.
The group of giant cells, which we have termed the magnocellular
nucleus of the basal forebrain (hag), was identified as part of the large-cell
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Striatum
167
hag
Fig. 2. A. carolinensis
forebrain at the same level as figure 1 showing acetylcholines-
terase (AChE) positive components of the corpus striatum with the intervening magnocel-
lular nucleus of the basal forebrain (hag). In hag, the cell bodies (but not the
neuropil)
are highly AChE positive. Bar = 1 mm.
component of the paleostriatum by Greenberg [ 15], but is clearly a separate
nucleus. In fact, Armstrong et al. [ 1 ], working with
Anolis
believed it to be
the forerunner of the mammalian globus pallidus. This notion is supported
by the presence of an enkephalinergic plexus in the basal forebrain of
A. carolinensis
[3 1 ], known to be a characteristic feature of pallidal struc-
tures.
Acetylcholinesterase Histochemistry
Procedure.
One animal was processed to reveal the distribution of this enzyme. The
lizard was overdosed with sodium pentobarbital and perfused through the heart with
ice-cold neutral buffered
formalin.
The brain was removed from the cranium and sections
cut on a freezing microtome at 40
µ
m. Staining was done according to a modification of the
Koelle
method using a silver intensification step [22].
In
A. carolinensis,
AChE stained material manifests a patchy distribu-
tion: hag is flanked by two areas of particularly high AChE activity which
overlap vSt and lateral portions of dSt and nucleus accumbens. Within
hag, the magnocellular elements show intense AChE activity while the
neuropil
is almost devoid of activity. The nucleus of the diagonal band
shows intense AChE activity and the remainder of dSt shows only moderate
AChE activity while the nucleus of the lateral olfactory tract (NLOT) and
the ADVR show no activity at all (fig. 2).
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/Switzer
168
In the turtle,
Chrysemys,
the acetylcholinesterase (AChE)-positive ven-
tral telencephalic cell mass was characterized as the homologue of mam-
malian neostriatum by Parent and Olivier [40]. In the forebrain of
Iguana,
Northcutt [33] noted the heaviest concentrations of AChE in nucleus
accumbens, the nucleus of the lateral olfactory tract, and the striatum. ACNE
activity was also found to be high in the striatum and moderate in the caudal
portion of nucleus accumbens in
Gekko gecko
by Russchen et al. [46]
AChE-positive cell bodies were found in the globus pallidus in a manner
much like that observed in
Anolis.
Hist ojluorescence
Procedure.
One animal was prepared to demonstrate catecholamine hist
ο
fluores-
cence. To enhance cellular fluorescence, the subject was pretreated with intraperitoneal
injections of L-tyrosine (0.05 mg, 53, 34, and 8 h before sacrifice), pargyline (1 mg, 34 h
before sacrifice) and
colchicine
(0.05 mg, 8 h before sacrifice). The animal was overdosed
with sodium pentobarbital, the brain removed, and sections cut at 8
µ
m on a cryostat.
Sections were collected on slides and immediately processed according to the sucrose-
potassium phosphate-glyoxylíc acid procedure of de la Torre and Surgeon [55].
Histofluorescent material reveals two areas richly invested by catechol-
aminergic fibers and terminals in a location that closely parallels the high
AChE activity patches described earlier, a correspondence also noted by
Parent and Olivier [40] in the turtle. Fluorescence is low in the intervening
hag and `baskets' of catecholaminergic fibers are present in the dSt. The
distribution of catecholamine fluorescence is reminiscent of the pattern of
dopamine immunoreactivity presented by Smeets et al. [49] for the striatal
complex of
Gekko.
When taken together, the distribution of AChE activity and catechol-
amine histofluorescence in the striatum of
Ano/is
indicate that its ventral
portion (here referred to as vSt), and in particular the two areas flanking
hag, may be homologized to the mammalian caudate-putamen complex
on the basis of their similar histochemistry. In support of this hypothesis,
the projection indicated by terminal degeneration seen after IPTP treat-
ment (see below) largely overlaps these histofluorescent, cholinesterase-
sensitive areas which probably correspond to the terminus of the meso-
striatal pathway in mammals, the caudate and putamen. In mammals, the
nucleus accumbens and the striatal portions of the olfactory tubercle are
considered ventromedial extensions of the striatum and are collectively
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169
referred to as ventral striatum [23]. Similarly, a ventromedial extension of
the globus pallidus, the ventral
pallidum,
has been recognized [51]. The
recent finding by Russchen et al. [46] using substance P and enkephalin
immunoreactivity of an area comparable to the mammalian ventral
palli-
dum
in the lizard
G. gecko
adds to the complexity of the lacertilian striatum
and stresses the fundamental similarities with other
taxa.
'PTP Findings
Procedure.
The degeneration-sensitive cupric silver method of de Olmos et al. [37] was
used to construct maps of the sites of damage following treatment with the dopaminergic-
specific cytotoxin IPTP or its more potent analog, 2'-CH3-
ΜΡΤΡ,
kindly provided by Dr.
Richard Heikkila.
The meperidine analog N-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyrid-
íne (
ΜΡΤΡ)
produces symptoms similar to idiopathic Parkinson's disease
[30], presumably by means of its selective incorporation into dopaminergic
neurons via the dopamine re-uptake system. While the primary site of cell
death is the pars compacta of the substantia nigra (S
Ν),
the adjacent ventral
tegmental area and other sites are also often affected [27]. The selectivity of
the neurotoxin appears sensitive to both the age of the animal (less selective
in older subjects) [30] and the amount of
ΜΡΤΡ
administered. In fact, at low
levels, many S
Ν
cells may survive while conspicuous mesostriatal axono-
pathies appear and tyrosine hydroxylase immunoreactivity in the striatum
decreases [26].
Behavioral Effects of MP
ΤΡ
Acute behavioral changes in MPTP-treated animals included indica-
tions of a physiological stress response and, in particular, color changes,
including the formation of a postorbital darkening (the `eyespot'), and
nuchal crest erection, both indications of adrenal activation [ 17]. These
effects and a pronounced hypokinesia remitted in all but 8 individuals
which had received in excess of 50 mg/kg of the drug. These individuals also
developed akinesia, postural rigidity, episodic convulsions, and occasion-
ally manifested stereotyped head and neck movements. The absence of
symptoms of acute stress in surviving individuals is consistent with the idea
of functional recovery of involved neural tissue; the individuals that did not
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170
survive may have suffered a crisis of adaptation due to massive and
persevering adrenal activation [2]. Subjects that received smaller doses (and
2 individuals that also received 50mg/kg doses), while showing clear indi-
cations of neurological damage, displayed no behavioral abnormalities;
however, tests of species-typical display behavior are underway to clarify the
possible roles of involved sites.
Neurocytopathology
of MP
ΤΡ
Following administration of
ΜΡΤΡ
to
Anolis,
cytopathological changes
were noted at several loci ranging from the forebrain to the cervical cord
(table I). Three classes of argyrophilic reactions were noted [12]: (1) degen-
erative neurons, densely packed with coarse silver granules; (2) reactive
neurons, the cytoplasm and dendrites of which were outlined by a fine and
light-staining granulation, and (3) degenerative axons and terminals. For
this report we emphasize those changes associated with the striatum. Ter-
minal degeneration observed in the striatum overlaps areas of histofluor-
escence and AChE reactivity as indicated above. The axons in this projec-
tion could be followed to the midbrain substantia nigra and ventral teg-
mental area where reactive neurons were detected, most abundantly in the
ventral tegmental area. This evidence supports the putative homology of the
reptilian striatal afferents and the mammalian mesostriatal pathway.
The extrinsic connections of the striatal complex are currently the
subject of intense interest. The pattern of striatal efferents described in the
lizard
Tupinambis
[24, 56] includes a prominent descending pathway aris-
ing from the ventral striatum and projecting by means of the ventral
peduncle of the lateral forebrain bundle to the ventromedial and entope-
duncular nuclei as well as the substantia nigra. Except for its additional
projections to the dorsal nucleus of the posterior commissure and the lateral
cerebellar nucleus, the striatal efferent system of
Tupinambis
is much like
the mammalian ansa lenticularis; the projection to the nucleus of the
posterior commissure indicates a st
ri
o-pretecto-tectal pathway [34]. Reiner
et al. [44] felt that a pretectal-tectal outflow was the major striatal mode of
influence on motor function in reptiles and birds, while the mammalian
basal ganglia functioned mainly by output to the motor cortex by way of the
thalamus.
Work on
Caiman
by Brauth and Kitt [5] lended support to earlier
findings that reptiles, like mammals, possess ascending pathways connect-
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171
Table L
Percent of individuals manifesting MPTP-induced argyrophilía in forebrain sites
Survival
time, h
Dose
mg/kg
n
DAT'
ADVR
DAT'
vSt
DAT'
LFB
r
DAT'
LFB
C
RN'
PIA
DN'
SCI
RN'
ρνΗ
12*
> 50
6
0
0
0
0 0 0
0
72-96
27-39
3
33
66
33
33 33
33
66
104-125
34
-49
4
50
100 100
75
50
25
50
148-216
32
-44
4
25
75
100
100
0
100
312
32-58
4
0 0
100
100
0 0
0
* Paralyzed at time of sacrifice.
ADVR = Anterior dorsal ventricular ridge; LFB
r
= lateral forebrain bundle
(rostral);
LFB
C
= lateral forebrain bundle (caudal: through diencephalon and mesencephalon); PIA
= preoptíc area; SCI = suprachiasmatíc nucleus;
ρνΗ =
periventrícular hypothalamus/para-
ventricular organ; "St = ventral striatum and nucleus accumbens.
' Argyrophilic effects:
DAT
= degenerating axons or terminals; DI = degenerative neurons;
RN = reactive neurons.
ing catecholaminergic cell groups in the midbrain to structures in the
forebrain [39]. Parent [38] described evidence strongly suggesting that
fluorescent nerve terminals in the strioamygdaloid complex of the turtle,
Chrysemys,
were directly related to fluorescent cell bodies in the rostral
midbrain tegmentum described earlier [41 ]. Ten Donkelaar and De Boer-
van Huizen [52] extended these findings to lizards. More recently, Smeets et
al. [49] supplied evidence that a mesolimbic pathway may be present in
Gekko
in addition to the classical mesostrigtal projection. However, they
indicated that these pathways had been proposed on the basis of circum-
stantial evidence and that they required more detailed tracing experiments
to be confirmed. We believe that the pattern of axonopäthies observed in
our MPTP-treated animals may be the first conclusive demonstration of a
mesostriatal connection in lizards (fig. 3). Further, a mesocortical projec-
tion in addition to the mesostriatal projection is indicated by the detection
of terminal degeneration in the ADVR, particularly in Northcutt's [33]
`area B', probably the terminus of an ascending somatosensory pathway
[42]. While Parent [38] detected some monoamine-indicating fluorescence
in the ADVR of the turtle, Smeets et al. [49] confirmed the presence of a
rather dense dopaminergic innervation of the ADVR of the
Gekko
by means
of antibodies against dopamine. The present study provides evidence that
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172
Fig. 3.
The distribution of degenerating axons and sites of terminal degeneration in
the brain of
Anolis carolinensis
subsequent to IPTP administration. ADVR = Anterior
dorsal ventricular ridge; Cer = cerebellum;
Ela
and
ΕΝρ =
entopeduncular nuclei ante-
rior and posterior, respectively; nDCP = nucleus of the dorsal posterior
commissure;
fpm = nucleus profundus mesencephali; IT = optic tectum; Pal =
pallium;
S
Ν =
substan-
tía nigra; vSt = ventral striatum; VTA = ventral tegmental area.
these rostral levels are involved in a far-reaching monoaminergic system in
Anolis
also.
Finally, terminal degeneration was also observed in the dorsal nucleus
of the posterior commissure (nDCP), as well as two subthalamic sites, the
anterior and posterior entopeduncular nuclei (
ΕΝα
and
ΕΝρ),
which appar-
ently receive collaterals from the ascending mesotelencephalic input. In
Caiman,
ΕΝα
in turn projects back to striatum, a fact that led Brauth and
Kitt [5] to speculate on a possible homology with the mammalian subthal-
amic nucleus.
It appears that the pattern of ascending projections from the catechol-
aminergic groups in the tegmentum faithfully reciprocates descending pro-
jections from the striatum.
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Striatum
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Prospects for Understanding Striatal Function
The striatal complex, because of its association with stereotyped behav-
ior and its central position in both motor control and cognition, is a
prominent candidate to provide insight into the behavioral functions of the
reptilian forebrain. The richness of the complex, often reciprocal relation-
ships between neural, endocrine, and behavioral elements will require the
use of techniques that can correlate behavioral patterns with the interac-
tions between multiple hormones, neurotransmitters, and neurohormones.
For example, spermatogenic activity (and thus perhaps reproductive behav-
ior) appears correlated with the intensity of monoamine-indicating fluores-
cence in the paraventricular hypothalamus of the lizard,
Lacerta
[29]. Work
on other taxa has made it clear that cells can simultaneously secrete multiple
hormones and neurotransmitters capable of orchestrating multiple re-
sponses in targets by means of differential concentrations, ratios of multiple
agents, regulation of post-secretional metabolism, and/or modulation of
receptor responses to specific agents [36]; further, specific activities can
differentially deplete dopamine from individual striatal nuclei [ 13]. Endo-
crine and neuroendocrine agents can act not only to facilitate or inhibit the
ability of cells to control their efferent targets but may be important in even
the differentiation of the target cells or their membrane receptors [21,
35].
The repertoire of stereotyped behavioral patterns that can be elicited
under controlled conditions and thus are amenable to neurobehavioral
investigation has recently expanded. Not only aggression and reproductive
phenomena, but specific behavioral units of social dominance [20] and
exploratory behavior [ 16] have been shown to be sensitive to specific
stimulus control in concert with known psychoactive stress-sensitive and
gonadal hormones. Such phenomena may well be linked to altered arousal
or attentional processes not unlike those identified by Schneider [47] as
central to striatal-related behavioral disorders in humans. In this regard it is
interesting that Iverson [25] noted that motivational and motor arousal
dysfunction appeared associated with the mesolimbic and mesostriatal
systems, respectively.
Clearly, the mesostriatal and other catecholaminergic pathways are
profoundly involved in the organization of the reptilian forebrain. But the
apparently unaffected maintenance behavior of surviving MPTP-treated
lizards indicates that these pathways do not appear to mediate essential
motor functions. These pathways may, however, be important for the
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174
organization of sensory input and thus access of input to appropriate output
mechanisms. Indeed, there is evidence from studies of the striatum in
mammals that the integrity of the caudate/putamen is necessary for adap-
tive functioning of the sensorimotor interface [4, 7]. The difficulty of
extracting causality from correlation in these complex paradigms is most
likely to yield to the increasing knowledge of the manner in which specific
stimuli interact with specific neuroactive agents in the brain.
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Department of Zoology, University of Tennessee, Knoxville, TN 37916 (USA)
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