Download Basal Forebrain Projections to Somatosensory Cortex in

JOURNALOFNEUROPHYSIOLOGY
Vol. 64, No. 4, October 1990. Printed in U.S.A.
Basal Forebrain Projections to Somatosensory Cortex in the Cat
KRISTIN
E. BARSTAD
AND
MARK
F. BEAR
The Center for Neural Science, Brown University, Providence, Rhode Island 02912
SUMMARY
AND
CONCLUSIONS
1. This investigation was designed to identify the source of
cholinergic basal forebrain projections to somatosensory cortex in
the cat.
2. Injections of horseradish peroxidase (HRP) into cortical
areas 3a, 3b, and 1 after a 36 to 48-h survival period, labeled
neurons in the basal forebrain. The distribution of retrogradely
labeled neurons was compared with the distribution of cells labeled by choline acetyltransferase immunocytochemistry. Most
retrogradely labeled neurons in the basal telencephalon were
found on the border between the globus pallidus and adjacent
structures. Sometimes labeled neurons were also found in both
limbs of the diagonal band of Broca.
3. Excitotoxin lesions of these regions of the basal telencephalon led to a profound depletion of acetylcholinesterase-containing
axons in primary somatosensory cortex.
4. These data lay necessary groundwork for tests of the hypothesis that the cholinergic projection modulates experience-dependent modifications in adult cat somatosensory cortex.
INTRODUCTION
A problem of extraordinary interest concerns the mechanisms by which cortical synapses are modified by sensory
experience. The cat striate cortex has proven to be a useful
model for this enquiry. As Wiesel and Hubel first showed
in 1963, the synaptic organization of cat visual cortex can
be readily modified by sensory experience during the first 3
mo of postnatal development. For example, temporary
closure of one eyelid in kittens renders most neurons in
striate cortex unresponsive to stimulation of the deprived
eye (Hubel and Wiesel 1970). This change in ocular dominance seems to require that animals attend to visual stimuli
and use vision to guide behavior (Singer 1979, 1982; Singer
et al. 1982), prompting the idea that experience-dependent
modifications in neocortex depend on the presence of
“gating” signals, which convey information about the behavioral state of the animal (Singer 1979). The neural substrate of these gating signals appears to be the noradrenergic projections of the locus coeruleus (Kasamatsu and Pettigrew 1979) and the cholinergic projections of the basal
forebrain (Bear and Singer 1986) because destruction of
these two projections interferes with normal experiencedependent modifications in the visual cortex (Bear and
Singer 1986). An important extension of this idea is to
determine whether these modulatory projections play a
central role in the modification of neocortex generally or
whether their effects are restricted to the visual cortex during early postnatal development. We have therefore turned
our attention to another model of cortical plasticity-adult
cat somatosensory cortex.
It is well documented that the cortical representation of
the body surface can be modified by manipulations of the
sensory periphery in adult mammals including cats (Kalaska and Pomerantz 1979), raccoons (Rasmusson 1982;
Rasmusson and Turnball 1983), rats (Wall and Cusick
1984), and monkeys (Merzenich et al. 1983). As in immature cat visual cortex, experience-dependent modifications
of somatosensory cortex appear to be modulated by behavioral state (Merzenich 1987). Dykes (1990) proposed that
the cortical cholinergic projection is one neural substrate of
this modulation. This hypothesis is based in part on the
findings that acetylcholine (ACh) is released in cortex on
arousal and sensory stimulation (Celesia and Jasper 1966;
Phillis and Chong 1965), and that iontophoretically
applied ACh alters neuronal excitability such that cortical
neurons become more responsive to peripheral stimulation. Metherate et al. (1987) have found that this enhancement of neuronal responses in somatosensory cortex can
last for periods of up to 1 h after cessation of the ACh
application, leading to the hypothesis that ACh plays a
permissive role in the use-dependent shifts in the adult
cortical somatotopic map (Dykes 1990).
A direct test of this hypothesis requires that the cortical
effects of ACh be eliminated at the same time that somatosensory cortex is challenged to undergo experience-dependent modification. One strategy to deplete cortical ACh
involves the destruction of cortically projecting cholinergic
neurons with the excitotoxin N-methyl aspartate (NMA)
(Bear et al. 1985; Bear and Singer 1986). The application of
this method to studies of somatotopic map plasticity requires information about the precise location of the cholinergic neurons projecting to primary somatosensory cortex. The aim of this study was to provide this information
and to test the feasibility of destroying the cholinergic projection to somatosensory cortex in the cat. The accompanying articles (Tremblay et al. 1990a,b) used this information to manipulate the release of ACh from cholinergic
basal forebrain axons in cat somatosensory cortex.
METHODS
Experimental
design
The cholinergic innervation of cat visual cortex appears to be
entirely extrinsic in origin, arising largely, if not exclusively, from
neurons distributed in the basal telencephalon (Bear et al. 1985).
Our strategy in this study was to retrogradely label with horseradish peroxidase (HRP) those basal forebrain neurons that project
to somatosensory cortex and to compare this distribution with
that of neurons containing choline acetyltransferase (ChAT), the
rate-limiting enzyme in the synthesis of ACh. Once the source of
the basal forebrain projection to somatosensory cortex was iden-
0022-3077190 $1 SO Copyright 0 1990 The American Physiological Society
1223
1224
K. E. BARSTAD
AND M. F. BEAR
14.68
FIG. 1. A, C, E, and G: drawings of coronal sections through a cat basal telencephalon that was processed for choline
acetyltransferase immunocytochemistry. Each dot represents a single immunoreactive neuron. Approximate stereotaxic
plane ofeach section is indicated (in millimeters anterior to the interaural line). On the righf ofeach panel (B, D. F, and H) is
a photomicrograph of a Nissl-stained section adjacent to the one processed for immunocytochemistry. AC, anterior
commissure; Ca, caudate nucleus; DBH, horizontal limb of the diagonal band of Broca; DBV, vertical limb of the diagonal
band of Broca; F, fornix; GP, globus pallidus; lC, internal capsule; MSN, medial septal nuclei: Put, putamen.
BASAL
FOREBRAIN
PROJECTION
IN
CAT
CORTEX
1225
17.24
tified, we next sought to destroy this projection with stereotaxic
injections of NMA. The successof the lesions was monitored by
the use of acetylcholinesterase (AChE) histochemistry, as avail-
able evidence indicates that this simple method is sufficient to
reveal the entire distribution of cholinergic axons in adult cat
neocortex (Bear et al. 1985; Stichel and Singer 1987).
1226
K. E. BARSTAD
AND M. F. BEAR
Gmm
14.8
5mm
FIG. 2. Plots of coronal sections through the basal telencephalon of cut C-147 showing the location of HRP-containing
neurons after a large unilateral pressure injection into somatosensory cortex (indicated by cross-hatched regions in insets).
See Fig. 1 legend for abbreviations.
ChA T experiment
One cat was used to prepare an atlas of ChAT immunoreactive
neurons in the basal forebrain. This animal was deeply anesthe-
tized with pentobarbital sodium and perfused through the ascending aorta with saline followed by 2 1 of fixative and, finally, 2 1 of
0.1 M sodium phosphate buffer (pH 7.4) containing 20% sucrose.
The ChAT fixative was 4% paraformaldehyde in 0.1 M phosphate
BASAL FOREBRAIN
PROJECTION
IN CAT CORTEX
1227
.
16.5
16.1
c 149
5mm
FIG. 3. Plots of coronal sections through the basal forebrain of cat C-149 showing the location of HRP-containing
neurons after small iontophoretic injections into somatosensory cortex (indicated by cross-hatched regions in the dorsal
reconstruction). See legend of Fig. 1 for abbreviations.
buffer (pH 7.4) and, in the first liter only, 0.1% glutaraldehyde.
The brain was removed and stored in 20% sucrose at 4OC.
The brain was frozen by submersion in 2-methyl butane at
-50°C and cut in the coronal plane at 50 pm. One-half of the
tissue sections were reacted for ChAT immunocytochemistry and
the other half were Nissl stained. The immunocytochemical pro-
cedure was a modification (Stichel and Singer 1987) of the peroxidase-antiperoxidase (PAP) method (Sternberger 1979). First, the
tissue was incubated for 5 min in 10% methanol in 3% H202 to
quench endogenous peroxidases. Next, the tissue was washed
thoroughly with phosphate buffer and incubated overnight in rat
anti-ChAT in a vehicle containing 0.5% triton X- 100, 2% bovine
1228
K.
E. BARSTAD
serum albumin, 20% normal rabbit serum, and 5% sucrose in 0.1
M phosphate buffer. The ChAT antibody was a gift of Dr. Felix
Eckenstein (Eckenstein and Thoenen 1982) and was kindly provided by Dr. Ford Ebner. The following day the sections were
thoroughly rinsed in buffer and incubated for 90 min in rabbit
antirat IgG dissolved in the same vehicle used for the primary
antibody. The tissue was washed again in buffer and incubated for
90 min in rat PAP. After another extensive wash, the sections
were reacted for 20 min in a solution containing 0.05% diaminobenzidene and 0.01% HzOz. The sections were washed a final
time, mounted onto microscope slides, dehydrated in alcohols,
cleared in xylene, and coverslipped.
HRY experiments
Ten adult cats were anesthetized with intravenously administered pentobarbital sodium and placed in a stereotaxic instrument. A large craniotomy was performed to expose the cortex
lying between the fork of the ansate sulcus and the cruciate sulcus.
Multiple injections of lo-30% HRP were made into the somatosensory cortex - 1 mm below the pia either by pressure injection
AND
M.
F. BEAR
by the use of a Hamilton microliter syringe (0.1-0.5 ~1) or by
iontophoresis with the use of a glass micropipette (tip diameter,
-40 pm; 3-4 PA for 15-20 min). The bone flap was replaced, and
the fascia and scalp were sutured closed. After a survival period of
2 days, the animals were reanesthetized with pentobarbital sodium and perfused through the ascending aorta with saline followed by fixative consisting of 1% paraformaldehyde and 1.25%
glutaraldehyde in 0.1 M phosphate buffer (pH 7.4). The fixative
was followed by ice cold phosphate buffer containing 10% sucrose. The brains were removed from the skull, frozen by submersion in 2-methyl butane at -5O”C, and sectioned in a cryostat
at 40 pm in the coronal plane. The tissue sections were reacted for
HRP histochemistry by the use of Mesulam’s (1978) procedure as
described previously (Bear et al. 1985).
Basal forebrain
lesions and AChE histochemistry
Four adult cats were anesthetized with intravenously administered pentobarbital sodium and placed in a stereotaxic instrument. The needle of a Hamilton microliter syringe was lowered
into the regions of the basal telencephalon that the previous HRP
experiments had shown to project to somatosensory cortex. l- to
FIG. 4. A: ChAT-immunoreactive neurons in the regionimmediatelyventral to the
globuspallidus. B: HRP-labeledcells(darkly
stained) in the same region after injections
into somatosensorycortex. This tissue was
lightly counterstainedwith Cresylviolet. Sections photographedin A and Bare at approximately the same coronal plane (-A14.7
mm).
BASAL FOREBRAIN
PROJECTION
5-~1injections of NMA (50 pg/pl) in saline were made at these
locations. The animals were allowed to survive for 1 wk before
being reanesthetized and perfused through the ascending aorta
with 10% phosphate-buffered Formalin (pH 7.4). The brains were
removed and sectioned in a cryostat at 40 pm in the coronal
plane. These sections were reacted for AChE by the use of a
modification of Jacobowitz and Creed’s (1983) procedure as described in detail by Bear et al. (1985).
RESULTS
Distribution ofChAT-containing
neurons
in cat basal telencephalon
The location of ChAT-immunoreactive
neurons was
carefully plotted onto drawings of the basal forebrain and
compared to adjacent N&l-stained
sections (Fig. 1). Intensely immunoreactive
interneurons were consistently
observed in the caudate and putamen in all sections. In
addition, labeled neurons were observed scattered within
the substantia innominata and internal capsule. At coronal
planes between the optic chiasm and anterior commissure
(Fig. 1, A-D), a prominent collection of immunoreactive
neurons was found in the semicircular border zone lying
between the globus pallidus and structures lateral and ventral. ChAT’ neurons were also found in the medial septal
nucleus at these levels. At coronal planes further anterior
(Fig. 1, E-H), most ChAT+ cells were concentrated in the
horizontal and vertical limbs of the diagonal band of
Broca, in addition to the substantia innominata and internal capsule.
Distribution of HRP-backjlled
into somatosensory cortex
neurons after injections
Injections of HRP into the somatosensory cortex led to
retrograde transport by neurons in the ventral posterior
I229
IN CAT CORTEX
thalamus, dorsal claustrum, and basal forebrain. The labeled cells in the basal forebrain fell predominantly within
a neatly circumscribed area. After large cortical injections,
some neurons were observed scattered within the internal
capsule and the vertical and horizontal limbs of the diagonal band; however, most retrogradely labeled cells were
found clustered in an arc along the border zone between
the globus pallidus and putamen, laterally, and substantia
innominata ventrally (Fig. 2).
Decreasing the size of the cortical injection, as was done
in later experiments by the use of iontophoresis, diminished the relative number of HRP-containing cells in the
basal forebrain (Fig. 3), but the distribution
of labeled
neurons remained similar. Again, the highest density of
stained neurons occurred in the region immediately lateral
and ventral to the globus pallidus.
As illustrated in Fig. 4, there is a close correspondence
between the distribution
and morphology of cortically
projecting neurons and ChAT-immunoreactive
cells in the
region ventrolateral to the globus pallidus. This correlation
suggests that this region is a likely source of cholinergic
projections to somatosensory cortex. This hypothesis was
tested by making excitotoxin lesions in this region and
searching for a depletion of AChE-containing axons in somatosensory cortex.
Eflects of basal,forebrain
somatosensory cortex
lesions on AChEi
axons in
There are some laminar differences in the distribution of
AChE+ axons in cat somatosensory cortex (Fig. 5, A and
B). For example the highest density of AChE+ axons occurs
in layer I, and the lowest density occurs in upper layer IV
and layer V. Nonetheless, all layers are richly innervated by
FIG. 5. A: Nissl cytoarchitectureof somatosensory
cortexm a normal cat. B: section adjacent to that shown in A stained
for acetylcholinesterase to reveal the normal pattern and density of AChE’ axons. C: section through somatosensory cortex
of cat C-153, processed for AChE histochemistry. C-l.53 recewed a unilateral lesion ofthe basal telencephalon 7 days earlier
(lesionreconstructedm Fig. 6). Note the striking depletion of AChE+ axons.
1230
K. E. BARSTAD
AChEcontaining
axons. This pattern of AChE-containing
axons is similar to that observed in cat striate cortex (Bear
et al. 1985).
If these AChE+ fibers reflect a cholinergic projection
from the basal telencephalon, our HRP experiments sug-
AND M. F. BEAR
gest that they arise from neurons located in the substantia
innominata, diagonal band of Broca, and the ventrolateral
border of the globus pallidus. To test this hypothesis, we
made lesions of the basal telencephalon with the excitotoxin NMA.
18.50
c 153
1 cm
l&
nn
I
KJ
FIG. 6. Reconstruction of a lesion in the basal telencephalon of cat C-153 after 2 injections of the excitotoxin IVmethyl-aspartate. Cross-hatching indicates regions of cell loss; stars indicate 2 injection sites. See Fig. 1 legend for abbreviations.
BASAL
FOREBRAIN
PROJECTION
The largest of these basal forebrain lesions is reconstructed in Fig. 6. This lesion was made by two NMA
injections, one targeting the region surrounding the globus
pallidus (from the interaural line in mm: A. 15, L. 7, D. 8)
and the other targeting the horizontal limb of the diagonal
*band of Broca (A. 16, L. 3, D. 7). As illustrated in Fig. 5
(C), this lesion produced a striking depletion of AChE+
axons in all layers. Smaller lesions confined to the area of
the globus pallidus also depleted cortical AChE but not as
extensively. Taken together these experiments demonstrate
that the vast majority of cholinesterase containing axons in
cortex arise from an identifiable region of the basal telencephalon and validate the utility of AChE histochemistry
to assessthe integrity of the cortical cholinergic projection.
DISCUSSION
Origin of the cholinergic projection to
somatosensory cortex in the cat
The aim of this study was to identify the location of
neurons in the basal telencephalon that project to somatosensory cortex in the cat. Our retrograde transport experiments revealed that basal forebrain projections to somatosensory cortex arise from neurons that are scattered widely
in the basal forebrain. However, the major source of basal
forebrain projections to somatosensory cortex appears to
be the region immediately ventral-lateral to the globus pallidus. This finding is consistent with a brief report by Ribak
and Kramer (1982) that AChE-containing neurons in this
region project directly to motor cortex in the cat.
Several lines of evidence suggest that this projection is
cholinergic. First, immunocytochemical
experiments show
a high density of large neurons containing ChAT in this
region of the basal forebrain. Second, excitotoxin lesions of
the globus pallidus severely deplete somatosensory cortex
of AChE-positive axons. Third, Tremblay et al. (1990a,b)
find that electrical stimulation of this region of the basal
forebrain evokes responses in cortical area 3b that can be
blocked by the muscarinic cholinergic antagonist atropine.
Taken together, these data support the hypothesis that the
basal forebrain provides a major cholinergic projection to
somatosensory cortex in the cat.
A combination of lesion and histochemical studies led to
a similar conclusion concerning the source of the cholinergic innervation of visual cortex in the cat (Bear et al. 1985).
However, the visual cortical projections appear to arise
mainly from the horizontal limb of the diagonal band of
Broca and from neurons embedded within the internal
capsule (Bear et al. 1985; Bear and Singer 1986) rather than
from the regions identified here. Few neurons in the vicinity of the globus pallidus are labeled after HRP injections
into area 17. Thus it appears that a crude topography exists
in the neocortical projections of the basal forebrain in
the cat.
Lesion experiments reveal that most, if not all, of the
AChE-positive axons in both visual and somatosensory
cortex arise from the basal telencephalon. In cat visual
cortex the elegant immunocytochemical
studies of DeLima
and Singer (1986) and Stichel and Singer (1987) have al-
IN
CAT
CORTEX
1231
lowed a direct comparison of the distribution
of axons
containing ChAT and AChE. The correspondence appears
to be excellent, suggesting that the large majority of AChEpositive axons in the visual cortex are in fact cholinergic.
This encourages us to believe that AChE histochemistry in
somatosensory cortex reveals the full complement of cholinergic axons arising from the basal forebrain, although
ChAT immunocytochemistry
will be required to establish
this definitively.
Comparisons with other species
The organization of basal forebrain projections to primary somatosensory cortex in the cat is similar to that
described for the rat and monkey (Johnston et al. 198 1;
Lehman et al. 1980; McKinney et al. 1983; Mesulam et al.
1983; Saper 1984). For example, in the rat the cholinergic
projection to parietal cortex arises from neurons immediately ventral to the globus pallidus, whereas the projection
to occipital cortex arises from cells in the horizontal limb of
the diagonal band of Broca (McKinney et al. 1983). In the
rhesus monkey the basal forebrain projection to primary
somatosensory cortex originates entirely from the nucleus
basalis of Meynert (Mesulam et al. 1983). The primate
nucleus basalis can be identified in Nissl-stained sections
on the basis of its large, darkly stained neurons, and lies
immediately ventral to the caudal globus pallidus (Heimer
et al. 1989). No homology to the nucleus basalis has been
generally recognized in the cat (Berman and Jones 1982),
but the present results support the interpretation
of
Grofova ( 1970) that the large cells in the dorsolateral aspect
of cat substantia innominata (Fig. 1) can be regarded as
homologous to the primate nucleus basalis.
Functional
implications
The wide distribution of cortically projecting basal forebrain neurons raises the question of whether different parts
of the basal forebrain cholinergic “system” have different
patterns of afferent connectivity. It remains an intriguing
possibility that the cortically projecting cholinergic basal
forebrain actually consists of a series of subsystems that are
specialized to respond under different behavioral conditions. In any case, the scattered distribution of neurons
with projections to somatosensory cortex presents a technical challenge for producing complete lesions of the cortical cholinergic inputs or for any other manipulations of
these neurons. Even the largest lesions in this study, which
included a significant fraction of the substantia innominata, globus pallidus, putamen, and adjacent structures,
never fully depleted the somatosensory cortex of AChEpositive axons. Nonetheless, it is likely that the degree of
depletion attained after these lesions is sufficient to help
elucidate cholinergic contributions to cortical function.
For example, excitotoxin lesions of cat basal telencephalon
have been found to reduce the metabolic activity evoked in
somatosensory cortex by repetitive tactile stimulation (Juliano et al. 1988), an effect that is also mimicked by topical
application of atropine.
This study provides the necessary groundwork for direct
manipulations of the cholinergic basal forebrain projection
1232
K. E. BARSTAD
to somatosensory cortex in the cat. In the accompanying
papers, Tremblay et al. (1990a,b) report that electrical
stimulation of the region we have identified as the cat nucleus basalis leads to facilitation of responses evoked in
area 3b by glutamate iontophoresis and tactile stimulation
(see also Rasmusson and Dykes 1988). These effects are
mimicked by iontophoretically
applied ACh (Metherate et
al. 1987) and are antagonized by the muscarinic receptor
blocker atropine. Together these results support the hypothesis that the basal forebrain exerts a generally facilitatory influence over area 3b and that this cholinergic projection can be regarded as a critical component of the reticular
activating system (reviewed by Dykes 1990; Singer 1979).
Furthermore,
the long-lasting nature of the facilitation
after basal forebrain stimulation suggests that this cholinergic projection can powerfully modulate experience-dependent modifications in the adult cerebral cortex.
The authors thank Dr. I. Matjucha for assistance on aspects of this
study.
This work was supported by ONR contract NO00 14-8 l-K0 136 and a
Sloan Foundation fellowship.
Address for reprint requests: R. W. Dykes, Dept. of Physiology, Pavillon
Principal, Universite of Montreal, C.P. 6 128, succ. A, Montreal, Quebec
H3C 357, Canada.
Received 16 October 1989; accepted in final form 11 June 1990.
REFERENCES
M. F., CARNES, K. M., AND EBNER, F. F. An investigation of
cholinergic circuitry in cat striate cortex using acetylcholinesterase histochemistry. J. Comp. Neural. 234: 41 l-430, 1985.
BEAR, M. F. AND SINGER, W. Modulation of visual cortical plasticity by
acetylcholine and noradrenaline. Nature Lond. 320: 172- 176, 1986.
BERMAN, A. L. AND JONES, E. G. The Thalamus and Basal Telencephalon
of the Cat. Madison, WI: Univ. of Wisconsin Press, 1982.
CELESIA, G. G. AND JASPER, H. H. Acetylcholine released from cerebral
cortex in relation to state of activation. Neurology 16: 1053- 1064, 1966.
DELIMA,
A. D. AND SINGER, W. Cholinergic innervation of cat striate
cortex: A choline acetyltransferase immunocytochemical
analysis. J.
Comp. Neurol. 250: 324-338, 1986.
DYKES, R. W. Acetylcholine and neuronal plasticity in somatosensory
cortex. In: Brain Cholinergic Systems, edited by M. Steriade and D.
Biesold. New York: Oxford Univ. Press, 1990, p. 294-3 13.
ECKENSTEIN,
F. AND THOENEN, H. Production of specific antisera and
monoclonal antibodies to choline acetyltransferase: characterization
and use for identification of cholinergic neurons. EMBO J. 1: 363-368,
1982.
GROFOVA,
I. Ansa and fasiculus lenticularis of Carnivora. J. Comp.
Neurol. 138: 195-208, 1970.
HEIMER,
L., ALHEID, G. F., AND ZABORSZKY,
L. Basal forebrain and
substantia innominata. In: Neuroscience Year, edited by G. Adelman.
Boston, MA: Birkhauser, 1989, p. 2 l-24.
HUBEL, D. H. AND WIESEL, T. N. The period of susceptibility to the
physiological effects of unilateral eye closure in kittens. J. Physiol. Lond.
206: 4 19-436, 1970.
JACOBOWITZ,
D. M. AND CREED, G. J. Cholinergic projection sites of the
nucleus of tractus diagonalis. Brain Res. Bull. 10: 365-37 1, 1983.
JOHNSTON,
M. V., MCKINNEY,
M., AND COYLE, J. T. Neocortical cholinergic innervation: a description of extrinsic and intrinsic components
in the rat. Exp. Brain Res. 43: 159-172, 198 1.
JULIANO,
S. L., MA, W., BEAR, M. F., AND ESLIN, D. Manipulation of
cortical cholinergic innervation alters stimulus-evoked metabolic activity in cat somatosensory cortex. Sot. Neurosci. Abstr. 14: 338.8, 1988.
KALASKA,
L. AND POMERANTZ,
B. Chronic paw denervation causes an
age-dependent appearance of novel responses from forearm in “paw
cortex” of kitten and adult cats. J. Neurophysiol. 42: 6 18-633, 1979.
BEAR,
AND M. F. BEAR
T. AND PETTIGREW, J. D. Preservation of binocularity after
monocular deprivation in the striate cortex of kittens treated with 6-hydroxydopamine. J. Comp. Neurol. 185: 139-162, 1979.
LEHMAN,
J., NAGY, J. I., ALMADJA, S., AND FIBIGER, H. C. The nucleus
basalis magnocellularis: the origin of a choline&
projection to the
neocortex of the rat. Neuroscience. 5: 116 l- 1174, 1980.
MCKINNEY,
M., COYLE, J. T., AND HEDREEN, J. C. Topographic analysis
of the innervation of the rat neocortex and hippocampus by basal forebrain cholinergic system. J. Comp. Neurol. 2 17: 103- 12 1, 1983.
MERZENICH,
M. M. Dynamic neocortical processes and the origins of
higher brain functions. In: The Neural and Molecular Bases of Learning, edited by J-P Changeux and M. Konishi. New York: Wiley, 1987, p.
337-358.
MERZENICH,
M. M., KAAS, J. H., WALL, J., NELSON, R. J., SUR, M., AND
FELLERMAN,
D. Topographic reorganization of somatosensory cortical
areas 3b and 1 in adult monkeys following restricted deafferentation.
Neuroscience 8: 33-55, 1983.
MESULAM,
M.-M. Tetramethyl-benzidene
for horseradish peroxidase
neurohistochemistry. A noncarcinogenic blue reaction product with
superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem. 26: 106- 117, 1978.
MESULAM,
M.-M., MUFSON, E. J., LEVEY, A. I., AND WAINER, B. H.
Cholinergic innervation of cortex by the basal forebrain: cytochemistry
and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus
monkey. J. Comp. Neurol. 214: 170-197, 1983.
METHERATE,
R., TREMBLAY,
N., AND DYKES, R. W. Acetylcholine permits prolonged potentiation of neural responsiveness in cat somatosensory cortex. Neuroscience 22: 75-8 1, 1987.
PHILLIS, J. W. AND CHONG, G. C. Acetylcholine release from the cerebral
and cerebellar cortices: its role in cortical arousal. Nature Lond. 207:
1253-1255, 1965.
RASMUSSON,
D. D. Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J. Comp. Neurol. 205: 3 13-326, 1982.
RASMUSSON,
D. D. AND DYKES, R. W. Long-term enhancement of
evoked potentials in cat somatosensory cortex produced by coactivation
of the basal forebrain and cutaneous receptors. Exp. Brain Res. 70:
276-286, 1988.
RASMUSSON,
D. D. AND TURNBULL,
B. G. Immediate effects of digit
amputation on Sl cortex in the raccoon: unmasking of inhibitory receptive fields. Brain Res. 288: 368-370, 1983.
RIBAK, C. E. AND KRAMER,
W. G. Choline&
neurons in the basal
forebrain have direct projections to sensorimotor cortex. Exp. Neurol.
75: 453-465, 1982.
SAPER, C. B. Organization of cerebral cortical afferent systems in the rat.
II. Magnocellular basal nucleus. J. Comp. Neurol. 222: 3 13-342, 1984.
SINGER, W. Central core control of visual cortex functions. In: The Neurosciences Fourth Study Program, edited by F. 0. Schmitt and F. G.
Worden. Cambridge, MA: MIT Press, 1979, p. 1093-l 109.
SINGER, W. Central core control of developmental plasticity in the kitten
visual cortex: I. Diencephalic lesions. Exp. Brain Res. 47: 209-222,
1982.
SINGER, W., TRETTER, F., AND YINON, U. Central-gating of developmental plasticity in kitten visual cortex. J. Physiol. Lond. 324: 22 I-237,
1982.
STERNBERGER,
L. A. Immunocytochemistry. New York: Wiley, 1979.
STICHEL,
C. C. AND SINGER, W. Quantitative analysis of the choline
acetyltransferase-immunoreactive
axonal network in the cat primary
visual cortex: I. Adult cats. J. Comp. Neurol. 258: 91-98, 1987.
TREMBLAY,
N., WARREN, R. A., AND DYKES, R. W. Electrophysiological
studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. I. Cortical neurons excited by glutamate.
J. Neurophysiol. 64: 1199- 12 11, 1990a.
TREMBLAY,
N., WARREN, R. A., AND DYKES, R. W. Electrophysiological
studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic
stimuli. J. Neurophysiol. 64: 12 12- 1222, 1990b.
WALL, J. T. AND CUSICK, G. D. Cutaneous responsiveness in primary
somatosensory (S-l) hindpaw cortex before and after hindpaw deafferentation in adult rats. J. Neurosci. 4: 1499- 15 15, 1984.
WIESEL, T. N. AND HUBEL, D. H. Single-cell responses in striate cortex of
kittens deprived of vision in one eye. J. Neurophysiol. 26: 1003- 10 17,
1963.
KASAMATSU,