Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a PHA-L study of subcortical projections.

The subcortical projections of the centromedian (CM) and the parafascicular (Pf) thalamic nuclei were examined in the squirrel monkey (Saimiri sciureus) by using the lectin Phaseolus vulgaris-leucoagglutinin (PHA-L) as an anterograde tracer. Both CM and Pf project massively to the striatum where they arborize in a complementary fashion. On the one hand, CM innervates most of the putamen caudal to the anterior commissure, a dorsolateral rim of the putamen rostral to the anterior commissure, discrete areas of the head of the caudate nucleus close to the internal capsule, and a lateral sector of the body of the caudate nucleus. On the other hand, Pf provides a heavy input to the head, body, and tail of the caudate nucleus, and to the rostral putamen, excluding the areas innervated by CM. In addition, Pf projects more discretely to the nucleus accumbens and the olfactory tubercle. Therefore, the projections from both CM and Pf cover the entire striatum, with those from CM arborizing into the "sensorimotor" striatal territory and the ones from Pf innervating the "associative-limbic" striatal territory. Furthermore, CM and Pf project to extrastriatal subcortical structures, such as the globus pallidus, the subthalamic nucleus, and the substantia nigra, where they also terminate in a complementary fashion. Topographically and cytologically, Pf is closely related to the subparafascicular nucleus (sPf). The Pf-sPf complex projects to the hypothalamus, the substantia innominata, the peripeduncular nucleus, and the amygdala. It also gives rise to descending efferents arborizing in various brainstem structures, including the inferior olivary complex. Additional studies with retrograde double-labeling methods show that distinct cell groups within CM project to the motor cortex and the striatum. Likewise, separate neuronal populations within the CM-Pf-sPf complex give rise to striatal and brainstem projections, the former arising from CM and Pf and the latter mainly from sPf. The complementary nature of CM and Pf projections to the striatum and other basal ganglia components suggests that this thalamic complex participates in a highly ordered manner in the parallel processing of the information that flows through the basal ganglia.     

Projections from substantia nigra and zona incerta to the cat's nucleus of Darkschewitsch

The goal of the present experiments was to examine the relationships of the nucleus of Darkschewitsch (ND) with the substantia nigra pars reticulata (SNr), the zona incerta (ZI), and the oculomotor nuclei by using wheat germ agglutinin-horseradish peroxidase (WGA-HRP) as a retrograde and anterograde neuronal tracer injected into various sites of the cat's brain. To eliminate the possibility that fibres of passage from the motor cortex passing through the SNr and ZI were responsible for the ND label, WGA-HRP also was injected into the SNr or the ZI after a large area of the frontal cortex, including the motor area, was destroyed. Retrograde axonal transport demonstrated that many cells of the rostromedial part of the ZI project to the ND, with the ipsilateral projections being dominant. Some cells of the caudomedial part of the SNr project to the ND, again, with the ipsilateral projection being dominant. A few small cells in the ND project bilaterally to the oculomotor nucleus. Anterograde tracer demonstrated that the SNr-ND terminal fields are less dense than the ZI-ND terminal fields. A few fine terminal fibres were observed bilaterally in the oculomotor, trochlear, and abducens nuclei. Electron microscopic examination demonstrated that these fine, labelled terminals contain pleomorphic vesicles and have symmetrical synaptic contacts with dendrites. These results indicate that the ND, a structure that is known to be important for the control of axial muscles (i.e., eye, head, and body muscles), is the target of projections from restricted areas of the SNr and ZI: areas that, during saccadic eye movement, may lead to disinhibition of the ND-oculomotor projection. Accordingly, the ND may function to inhibit the activity of extraocular muscles during saccades. J. Comp. Neurol. 396:461–482, 1998. © 1998 Wiley-Liss, Inc.     

Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity.

The organization of the thalamostriatal projections arising from the centromedian (CM) and parafascicular (Pf) thalamic nuclei in the squirrel monkey (Saimiri sciureus) was studied at both light and electron microscopic levels. Following selective injections of the anterograde axonal tracer Phaseolus vulgaris-leucoagglutinin (PHA-L) into the CM or Pf, patterns of terminal arborization within the striatum were compared to the biochemical heterogeneity of the striatum as revealed by immunohistochemical staining for the calcium-binding protein calbindin D-28k (CaBP), and histochemical staining for the enzymes acetylcholinesterase (AChE) and nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-diaphorase). The PHA-L-labeled axon terminals within the striatum were further analyzed at the ultrastructural level to characterize their pattern of synaptic organization. Dense and heterogeneous terminal fields occur in the "sensorimotor" territory of the striatum after CM injections, or in the "associative" striatal territory following Pf injections. In the associative territory labeled axons arborize in a diffuse manner predominantly within areas enriched with CaBP, AChE, or NADPH-diaphorase, representing the matrix compartment, and tend to avoid areas poor in these substances, corresponding to the patch/striosome compartment. In the sensorimotor territory labeled axons form bands that occupy a subregion of the NADPH-diaphorase-rich zone in the putamen. The terminal pattern of the CM-striatal projection suggests the existence of a more complex mosaic organization within the sensorimotor territory. Ultrastructural analysis of PHA-L-labeled elements within the striatum reveals that both CM and Pf projections form asymmetric synapses upon dendrites and spines of striatal cells. A total of 339 PHA-L-labeled boutons were examined after CM injections and compared to 293 boutons following Pf injections. After CM injections, 29% of PHA-L-labeled terminals form synapses on dendritic spines and 66% on dendritic shafts, whereas after Pf injections only 12% of synapses occur on dendritic spines compared to 81% on dendritic shafts. Labeled terminals forming axosomatic or axoaxonic synapses were not seen within the striatum following either CM or Pf injections. It is concluded that in the squirrel monkey: 1) Pf-striatal fibers profusely arborize within the matrix compartment of the associative territory, 2) CM-striatal fibers form bands that occupy a subregion of the NADPH-diaphorase-rich zone within the sensorimotor territory, and 3) that both Pf- and CM-striatal projections establish asymmetric synapses with dendrites and spines of medium-sized spiny cells.(ABSTRACT TRUNCATED AT 400 WORDS)     

Three-dimensional cartography of functional territories in the human striatopallidal complex by using calbindin immunoreactivity

This anatomic study presents an analysis of the distribution of calbindin immunohistochemistry in the human striatopallidal complex. Entire brains were sectioned perpendicularly to the mid-commissural line into 70-microm-thick sections. Every tenth section was immunostained for calbindin. Calbindin labeling exhibited a gradient on the basis of which three different regions were defined: poorly labeled, strongly labeled, and intermediate. Corresponding contours were traced in individual sections and reformatted as three-dimensional structures. The poorly labeled region corresponded to the dorsal part of the striatum and to the central part of the pallidum. The strongly labeled region included the ventral part of the striatum, the subcommissural part of the external pallidum but also the adjacent portion of its suscommissural part, and the anterior pole of the internal pallidum. The intermediate region was located between the poorly and strongly labeled regions. As axonal tracing and immunohistochemical studies in monkeys show a similar pattern, poorly, intermediate, and strongly labeled regions were considered as the sensorimotor, associative, and limbic territories of the human striatopallidal complex, respectively. However, the boundaries between these territories were not sharp but formed gradients of labeling, which suggests overlapping between adjacent territories. Similarly, the ventral boundary of the striatopallidal complex was blurred, suggesting a structural intermingling with the substantia innominata. This three-dimensional partitioning of the human striatopallidal complex could help to define functional targets for high-frequency stimulation with greater accuracy and help to identify new stimulation sites.     

Golgi study of the primate substantia nigra. II. Spatial organization of dendritic arborizations in relation to the cytoarchitectonic boundaries and to the striatonigral bundle

The spatial organization of Golgi-stained dendritic arborizations of the substantia nigra was studied in three dimensions by using a video computer system. Dendritic orientation was analyzed in relation to the cytoarchitectonic boundaries and to the direction of the axons of the striato-pallidonigral bundle. All the brains, humans and macaques, were sectioned according to the same ventricular planes. The striatal bundle is made up of dense fascicles of very thin parallel axons. Sixty neurons located in the pars reticulata, lateralis, and compacta were reconstructed from serial sections. In the anterior pars reticulata and lateralis, the dendritic arborizations spread in all directions inside the striatal bundle. Below the pars compacta fringes, the dendrites of pars reticulata neurons extend ventrolaterally in the bundle. Because one nigral arborization can cover the whole thickness of the striatal bundle, we are led to believe that nigral neurons exert a role of convergence of the corticostriatal information similar to that of pallidal neurons (Percheron et al., '84a,b). The pars reticulata neurons appear to receive information mainly from the associative striatal territory. The pars lateralis neurons, conversely, appear to receive information from the sensorimotor territory. The anterior pars compacta neurons are organized in such a way that their ventral dendrites, located inside the pars reticulata, are ventrolaterally oriented, perpendicular to the striatal bundle. Their dorsal dendrites remaining in the pars compacta can receive other input. At more caudal levels, the posterior pars compacta neurons have dendrites radiating outside the striatal bundle.     

Corticostriatal innervation of the patch and matrix in the rat neostriatum

The distribution of rat corticostrial axons in the patch (striosome) and matrix compartments of the neostriatum was studied by using axonal labeling with biotinylated dextran amine (BDA) and identifying patch and matrix in the same section with calbindin immunocytochemistry. Small injections of BDA were made in the anterior cingulate, medial agranular, lateral agranular, or somatosensory cortex. Each area projected to both the patch and matrix compartments, except for the somatosensory cortex, which had only matrix projections. Within the remaining cortical areas, injections in layers Vb and VI preferentially labeled axons in patches whereas injections in layers III-Va preferentially labeled matrix axons. Axons from these injections formed varicosities preferentially, but not exclusively, in one compartment. There was a population of axons that crossed compartmental boundaries and arborized in both patch and matrix. Two distinct patterns of corticostriatal axonal arborizations were observed. Small, discrete foci of innervation were seen in the patch compartment and in some regions of the matrix. The focal arborizations in the matrix were observed through the rostrocaudal extent of the neostriatum but were most obvious in the caudal one-third. They resembled the matrisomes observed in cat and primate corticostriatal projections. The second pattern of innervation consisted of extended axonal arborizations that covered large regions of the rostral neostriatal matrix. These results support the concept of multiple classes of corticostriatal neurons having different targets within the neostriatum, following different topographical rules, and having different but overlapping distributions across cortical areas. © 1996 Wiley-Liss, Inc.     

The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat

Combined neuroanatomical techniques were used to examine the organization of the striatal projection to the substantia nigra in the rat. Both double anterograde axonal tracing methods (Phaseolus vulgaris leuco-agglutinin (PHA-L) and 3H-amino acid tract tracing) and double fluorescent retrograde axonal transport tracing methods were used to examine the relationship among striatal neurons projecting to separate areas of the substantia nigra. Additionally, the distributions of retrogradely labeled striatonigral projection neurons were charted relative to the neurochemically distinct striatal "patch" compartment, identified by substance P- or leu-enkephalin-like immunoreactivity, and the complementary "matrix" compartment, identified by somatostatin-like immunoreactive fibers. These studies show two distinct types of organization in the striatonigral projections. One type is topographic in that the mediolateral relationships among these striatal efferent neurons are roughly maintained by their termination patterns in the substantia nigra, while the dorsoventral relationships are inverted. Projections from any part of the striatum, however, are distributed throughout the rostrocaudal axis of the substantia nigra. Despite their general topographic organization, the variable and dispersed nature of such projections from individual striatal loci results in partial overlap of afferent fields from separate striatal areas. The second type of organization is nontopographic and provides a different system for convergence of inputs from separated striatal areas that is superimposed on the rough topographic system. In this other projection system the mediolateral and dorsoventral relationships typical of the topographically ordered system are not maintained and are sometimes reversed. For example, PHA-L injected into the dorsal striatum labels a topographic (inverted relationship) projection to the ventral substantia nigra pars reticulata but also a smaller and separate projection to the dorsal pars reticulata and adjacent pars compacta. Retrograde tracer deposits in the pars compacta label neurons in the ventral striatum (the inverted relationship) but also clusters of neurons in the dorsal striatum. These clusters are in the neurochemically defined patch compartment whereas neurons in the matrix are labeled by injections into the pars reticulata. The dendrites of both retrogradely filled patch and matrix neurons are confined to the compartment containing their cell bodies, suggesting a restriction that would functionally segregate extrinsic striatal afferents shown in other studies to be confined to either patches or matrix.(ABSTRACT TRUNCATED AT 400 WORDS)     

Quantitative analysis of dopaminergic loss in relation to functional territories in MPTP-treated monkeys

1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) intoxication in primates results in a heterogeneous loss of dopamine in the striatum, predominating in the dorsal and caudal parts of the structure, causing functional impairment that appears to be essentially motor and cognitive. The aim of the present study was to quantify the loss of dopamine in relation to the anatomo-functional subdivisions of the striatum, and also of the pallidum and cortex of MPTP-treated monkeys. A severe loss of dopaminergic innervation was observed in both the sensorimotor and associative territories of all these structures in MPTP-treated monkeys. Comparatively, the limbic territories of all these structures were little affected. The preservation of dopaminergic innervation of the limbic part of cerebral structures may explain the preservation of motivational processes mediated by these limbic regions in MPTP-treated monkeys.     

An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch

Area X is a nucleus within songbird basal ganglia that is part of the anterior forebrain song learning circuit. It receives cortical song-related input and projects to the dorsolateral medial nucleus of thalamus (DLM). We carried out single- and double-labeled immunohistochemical and pathway tracing studies in male zebra finch to characterize the cellular organization and circuitry of area X. We found that 5.4% of area X neuronal perikarya are relatively large, possess aspiny dendrites, and are rich in the pallidal neuron/striatal interneuron marker Lys8-Asn9-neurotensin8-13 (LANT6). Many of these perikarya were found to project to the DLM, and their traits suggest that they are pallidal. Area X also contained several neuron types characteristic of the striatum, including interneurons co-containing LANT6 and the striatal interneuron marker parvalbumin (2% of area X neurons), interneurons containing parvalbumin but not LANT6 (4.8%), cholinergic interneurons (1.4%), and neurons containing the striatal spiny projection neuron marker dopamine- and adenosine 3',5'-monophosphate-regulated phosphoprotein (DARPP-32) (30%). Area X was rich in substance P (SP)-containing terminals, and many ended on area X neurons projecting to the DLM with the woolly fiber morphology characteristic of striatopallidal terminals. Although SP+ perikarya were not detected in area X, prior studies suggest it is likely that SP-synthesizing neurons are present and the source of the SP+ input to area X neurons projecting to the DLM. Area X was poor in enkephalinergic fibers and perikarya. The present data support the premise that area X contains both striatal and pallidal neurons, with the striatal neurons likely to include SP+ neurons that project to the pallidal neurons.     

The Primate Striatum: Neuronal Activity in Relation to Spatial Attention Versus Motor Preparation

The primate basal ganglia are known to be involved in the initiation and control of visually guided movements. However, the precise role of these structures is not clear, partly because most neurophysiological studies have not dissociated neuronal activity related to visuomotor processing from that reflecting other aspects of behaviour, such as shifts of spatial attention. Moreover, the way the basal ganglia function together with the frontal cortex during movement initiation and execution is still a matter of debate. In an effort to clarify these issues, we recorded single neurons from the striatum (caudate nucleus and putamen) in two rhesus monkeys trained to perform a conditional visuomotor task, and compared their properties with those of the frontal cortex. The experimental paradigm was designed to distinguish neuronal activity associated with shifts of attention from that reflecting motor preparation. In a given trial, an identical visual stimulus could serve as a cue for the reorientation of spatial attention or as a cue for establishing a motor set depending on when it occurred during that trial. Additional aspects of the paradigm were designed to identify neurons whose activity differed when various stimulus configurations instructed the same action (stimulus effect), as well as neurons whose activity differed when two different actions were instructed by the same stimulus (movement effect). The majority of cells (60%) were preferentially active after instructional cues, 38% discharged preferentially after attentional cues, and the remaining 2% of cells discharged equally after both types of cue. Neurons active after instructional cues were further analysed for stimulus and movement effects. During movement preparation, the activity of the vast majority of striatal cells (putamen, 81%; caudate, 76%) varied significantly when different stimuli instructed the same action. Likewise, when different movements were instructed by the same stimulus, preparatory activity of a majority of cells (putamen, 92%; caudate, 82%) changed. Consequently, a substantial proportion of cells showed combined stimulus and movement effects. Comparison of these neuronal properties with those of the dorsal premotor cortex showed significantly higher proportions of cells in the striatum whose activity reflected sensory or sensorimotor processing. These results suggest that the basal ganglia are involved in shifting attentional set and in high-order processes of movement initiation, including the linking of sensory information with behavioural responses.     

GABAergic elements in the neuronal circuits of the monkey neostriatum: a light and electron microscopic immunocytochemical study

An antibody raised in rabbits against a GABA-BSA conjugate was used together with the PAP technique to label elements in the neostriatum of three Old World monkeys. Light microscopy revealed numerous immunoreactive medium-size neurons of various staining intensities, some of which had indented nuclei, as well as an occasional large cell. The neuropil showed a plexus of fine processes with frequent puncta. Ultrastructurally, the medium-size GABA-positive neurons were of two types: one with smooth nuclei and scanty cytoplasm, similar to spiny I cells, the other with invaginated nuclear envelopes and more abundant perikaryon, resembling the aspiny type. Correspondingly, labeled dendrites were either spiny or varicose. Some stained axons were myelinated, and the boutons had either large and ovoid, or small and pleomorphic vesicles. All of these boutons formed symmetric synapses, the former type with GABA-positive dendritic shafts but also with unlabeled dendrites; the latter type usually with GABA-negative elements, either dendrites, dendritic spines, or somata. Synapses were also observed between unreactive boutons and immunostained dendrites. Terminals with densely packed, small round vesicles that established asymmetric synapses with spines were always GABA-negative. Glial elements were consistently unlabeled, save for some astroglial endfeet. These findings provide positive evidence for the existence of two classes of GABAergic striatal neurons corresponding to a long-axoned spiny I type and an aspiny interneuron. Furthermore, the simultaneous labeling of GABA-immunoreactive presynaptic and postsynaptic profiles offers possible morphologic bases for the various kinds of intrastriatal inhibitory processes, including the feedforward, feedback, and "autaptic" types.     

Influence of the predicted time of stimuli eliciting movements on responses of tonically active neurons in the monkey striatum

Changes in activity of tonically active neurons of the primate striatum are determined both by the behavioural significance of stimuli and the context in which stimuli are presented. We investigated how the responses of these neurons are modified by the temporal predictability of stimuli eliciting learned behavioural reactions. Single neurons were recorded from the caudate nucleus and putamen of two macaque monkeys performing a visual reaction time task under conditions in which the timing of the trigger stimulus was made more or less predictable. The monkeys' ability to predict the trigger onset was assessed by measuring arm movement reaction times and saccadic ocular reactions. Of 171 neurons responding to the unsignalled presentation of the trigger stimulus, 32% lost their response when an instruction cue preceded the trigger by a highly practised 1.5 s interval, and the response reappeared when this interval was varied randomly from 1 to 2.5 s or prolonged to 3 or 4. 5 s. Although 43% of the neurons remained responsive irrespective of task condition, the responses were stronger with longer intervals than with the accustomed 1.5 s interval. In addition, a number of neurons responding to the instruction lost their response when the trigger appeared more distant from the instruction. These findings demonstrate that neuronal responses to a movement-triggering signal become more numerous and pronounced when the degree of temporal predictability of that signal was decreased. We conclude that tonic striatal neurons are sensitive to temporal aspects of stimulus prediction.     

Topography of the projection from the central complex of the thalamus to the sensorimotor striatal territory in monkeys.

The distribution of axons arising from the central complex (or centre médian-parafascicular complex) and terminating in the striatum was studied in seven macaques and one squirrel monkey. Deposits of anterograde tracers were made in the two lateral-most subdivisions of the central complex, i.e., the middle part (or pars media) and the lateral part (or pars paralateralis). All injections avoided the pars parafascicularis. The intrastriatal distribution of labeled axonal endings was mapped in relation to the standard ventricular (CA-CP) system of coordinates. Labeled endings were observed in the major posterior and dorsal parts of the putamen (excluding its anteromedial and ventral parts) and also in a restricted ventrolateral part of the caudate nucleus. The topography of the central territory of the striatum, defined as the striatal space receiving axons from the central complex, was found to correspond exactly to that of the cortical sensorimotor territory delineated after cortical injections. The termination pattern of the central axons within the striatum was patchy. Viewed as a whole, the irregular and hazy patches formed oblique streaks, parallel one with the other. The three-dimensional reconstructions of data from transverse sections revealed that the streaks were bi-dimensional pictures of three-dimensional parasagittal layers covering the whole anteroposterior extent of the cortical sensorimotor territory of the striatum. Our work shows that the pars media of the central complex, which receives selectively pallidal afferent axons (Fran?ois et al., '88: Brain Res. 473:181-186), is the main source of the centroputaminal projection. The probable implication of this in a closed sensorimotor loop of the basal ganglia is discussed.     

Down-regulation of metabotropic glutamate receptor 1alpha in globus pallidus and substantia nigra of parkinsonian monkeys

Enhanced glutamatergic neurotransmission via the subthalamopallidal or subthalamonigral projection seems crucial for developing parkinsonian motor signs. In the present study, the possible changes in the expression of metabotropic glutamate receptors (mGluRs) were examined in the basal ganglia of a primate model for Parkinson's disease. When the patterns of immunohistochemical localization of mGluRs in monkeys administered systemically with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) were analysed in comparison with normal controls, we found that expression of mGluR1alpha, but not of other subtypes, was significantly reduced in the internal and external segments of the globus pallidus and the substantia nigra pars reticulata. To elucidate the functional role of mGluR1 in the control of pallidal neuron activity, extracellular unit recordings combined with intrapallidal microinjections of mGluR1-related agents were then performed in normal and parkinsonian monkeys. In normal awake conditions, the spontaneous firing rates of neurons in the pallidal complex were increased by DHPG, a selective agonist of group I mGluRs, whereas they were decreased by AIDA, a selective antagonist of group I mGluRs, or LY367385, a selective antagonist of mGluR1. These electrophysiological data strongly indicate that the excitatory mechanism of pallidal neurons by glutamate is mediated at least partly through mGluR1. The effects of the mGluR1-related agents on neuronal firing in the internal pallidal segment became rather obscure after MPTP treatment. Our results suggest that the specific down-regulation of pallidal and nigral mGluR1alpha in the parkinsonian state may exert a compensatory action to reverse the overactivity of the subthalamic nucleus-derived glutamatergic input that is generated in the disease.     

Role of glutamate receptor subtypes in the differential release of somatostatin,neuropeptide Y,and substance P in primary serum-free cultures of striatal neurons

The spiny and aspiny neuronal populations of the striatum display differential vulnerability to the toxic effects of glutamatergic agonists. Substance P–containing spiny neurons appear to be more vulnerable to NMDA-receptor–mediated toxicity and less susceptible to kainate toxicity than the somatostatin- and neuropeptide Y (NPY)-containing aspiny population. We studied whether selective glutamatergic agonists might have similar differential effects on neuropeptide release from the substance P- and somatostatin/NPY-containing neuronal populations. After collection of a baseline sample, striatal neurons in primary culture were treated with one of the following: phosphate-buffered saline, 56 mM potassium chloride (KCl), 100 μM N-methyl-D-aspartate (NMDA), 100 μM quisqualate, 100 μM kainate, or 100 μM glutamate. Baseline and treatment samples were measured by radioimmunoassay for somatostatin, NPY, and substance P. KCl and kainate provoked a selective release of somatostatin and NPY, whereas substance P measured in the same samples showed no response. By contrast, NMDA elicited a selective release of substance P without a similar increase of either somatostatin or NPY. Quisqualate evoked comparable responses in the three peptides. These results indicate that the glutamatergic regulation of somatostatin and NPY release from aspiny striatal neurons in primary culture is preferentially mediated by the kainate receptor, whereas substance P release is selectively mediated by the NMDA receptor. These findings suggest a preferential expression of functional kainate receptors on the aspiny somatostatin/NPY neurons and of NMDA receptors on the substance-P–containing spiny neurons. Synapse 27:161–167, 1997. © 1997 Wiley-Liss, Inc.     

Medium spiny neurons of the neostriatal matrix exhibit specific, stereotyped changes in dendritic arborization during a critical developmental period in mice

In mice, the matrix compartment of the striatum (caudate/putamen) undergoes major developmental changes during the second postnatal week, including the establishment of corticostriatal and nigrostriatal afferents, the maturation of parvalbumin-positive interneurons and the appearance of perineuronal nets. It is not known if any of these events influence the dendritic structure of medium spiny neurons, the principal output cells of the striatum. To determine whether any measurable changes in the dendrites of matrix medium spiny neurons occur during this important developmental period, we labeled individual cells at different time points flanking the second postnatal week. These cells exhibit distinct dendritic morphologies from the earliest postnatal time points examined. Furthermore, our data show that the dendritic arbors of these neurons change in length, branch points, diameter and tortuosity, regardless of morphological type. The increase in dendritic length is accompanied by a decrease in the number of branch points that occur in different, but consistent, parts of the dendritic arbor. All of these changes are most pronounced during the second postnatal week, coinciding with a number of developmental events considered important for consolidating circuitry within the striatal matrix. Our results further support the critical importance of this early postnatal period in striatal development.     

Organization of the avian “corticostriatal” projection system: A retrograde and anterograde pathway tracing study in pigeons

Birds have well-developed basal ganglia within the telencephalon, including a striatum consisting of the medially located lobus parolfactorius (LPO) and the laterally located paleostriatum augmentatum (PA), Relatively little is known, however, about the extent and organization of the telencephalic “cortical” input to the avian basal ganglia (i. e., the avian “corticostriatal” projection system). Using retrograde and anterograde neuroanatomical pathway tracers to address this issue, we found that a large continuous expanse of the outer pallium projects to the striatum of the basal ganglia in pigeons. This expanse includes the Wulst and archistriatum as well as the entire outer rind of the pallium intervening between Wulst and archistriatum, termed by us the pallium externum (PE). In addition, the caudolateral neostriatum (NCL), pyriform cortex, and hippocampal complex also give rise to striatal projections in pigeon. A restricted number of these pallial regions (such as the “limbic” NCL, pyriform cortex, and ventral/caudal parts of the archistriatum) project to such ventral striatal structures as the olfactory tubercle (TO), nucleus accumbens (Ac), and bed nucleus of the stria terminalis (BNST). Such “limbic” pallial areas also project to medialmost LPO and lateralmost PA, while the hyperstriatum accessorium portion of the Wulst, the PE, and the dorsal parts of the archistriatum were found to project primarily to the remainder of LPO (the lateral two-thirds) and PA (the medial four-fifths). The available evidence indicates that the diverse pallial regions projecting to the striatum in birds, as in mammals, are parts of higher order sensory or motor systems. The extensive corticostriatal system in both birds and mammals appears to include two types of pallial neurons: (1) those that project to both striatum and brainstem (i. e., those in the Wulst and the archistriatum) and (2) those that project to striatum but not to brainstem (i. e., those in the PE). The lack of extensive corticostriatal projections from either type of neuron in anamniotes suggests that the anamniote-amniote evolutionary transition was marked by the emergence of the corticostriatal projection system as a prominent source of sensory and motor information for the striatum, possibly facilitating the role of the basal ganglia in movement control. © 1995 Wiley-Liss, Inc.