Corticostriatal Projections Research Articles

Sequence generation in arbitrary temporal patterns from theta-nested gamma oscillations: a model of the basal ganglia–thalamo-cortical loops

A computational model that is able to generate sequences at arbitrary rates in a given serial order is presented for the cortico-basal ganglia (BG)–thalamic neural circuitry. Upon generating a sequence, this model stores information on the serial order of components in a cortical buffer by means of theta-nested gamma frequency oscillations observed experimentally in cortico-striatal neurons. This model assumes the existence of at least two functionally different classes of striatal spiny neurons. One class of striatal projection neurons (S-cells) select the first component in the cortical buffer through a temporal winner-take-all mechanism implemented by lateral inhibition. The inhibition should last for at least a few hundred milliseconds. In reality, it may be mediated by GABA B receptors at the presynaptic terminals of the cortico-striatal projection. The other class of striatal projection neurons (M-cells) retain the currently executed component in a cortico-BG–thalamic loop, for which the strong nonlinearity in transitions between up and down states of striatal neurons is crucial. For sequence generation at the level of striatum, the cortical neurons encoding the component selected for execution are inactivated by the feedback from the activated cortico-BG–thalamic loop. This model predicts that the transition to next component is triggered by a single external signal, i.e. the subthalamic input to the globus pallidum. This input gives a neural substrate for adjusting the rate of sequence generation.

Lack of cortico-striatal projections from the primary auditory cortex in the squirrel monkey

The projections of the superior temporal gyrus to the caudate nucleus were studied in 10 squirrel monkeys ( Saimiri sciureus). It was found that the primary auditory cortex lacks direct connections with the caudate nucleus as well as the putamen. Areas RL and T1 of Burton and Jones, bordering the primary auditory cortex laterally, show a moderate projection to the body and tail of the caudate nucleus; area T2, bordering areas RL and T1, shows an extensive projection into the head, body and tail. A comparison of the temporo-caudate projections of the monkey with those of rodents and carnivores suggests that primary and secondary auditory cortices differ in their connections in primates more than in other mammals, pointing to a greater functional differentiation of these areas in primates.

Corticostriatal projections from distal and proximal forelimb representations of the monkey primary motor cortex

Corticostriatal projections from one distal and two proximal subregions in the forelimb representation of the primary motor cortex (MI) were examined in the macaque monkey. The distal and proximal subregions in the anterior bank of the central sulcus (distal and proximal-bank subregions) and the proximal subregion in the surface of the precentral gyrus (proximal-surface subregion) of the MI were identified using intracortical microstimulation. Different anterograde tracers were then injected into two of these three forelimb subregions of the MI. In the ipsilateral putamen, the distribution areas of corticostriatal fibers from the distal, proximal-bank and proximal-surface subregions were arranged from ventrolateral to dorsomedial in this order. These corticostriatal input zones were largely segregated from one another.

Glutamatergic Modulation of Subcortical Motor and Limbic Circuits

The ventral striatum is a critical component of parallel circuits associated with motor and limbic functions, termed the corticostriatopallidothalamic circuit (CSPT).1 The interconnectivity of the regions comprising these circuits is believed to mediate the processing of sensory information that leads to the modulation of both motor and limbic behaviors. This well-defined circuitry allows for the neurochemical anatomical examination of functionally integrated regions. The striatum is one of the critical integrative areas in the CSPT because of the convergence of its glutamatergic and dopaminergic afferents, and the modulatory effects of its efferents.1 Corticostriatal glutamate projections synapse on mesostriatal dopaminergic projections, and modulate dopamine release in the dorsal and ventral striatum.2 Modulators of all four glutamate receptor subtypes—NMDA, AMPA, kainate, and metabotropic—affect dopamine release in dorsal and ventral striatum. We previously reported that systemic treatment with the NMDA receptor antagonist MK-801 alters D2 receptor mRNA in the ventral tegmental area (VTA) but not the substantia nigra, pars compacta (SNc), or in the dorsal or ventral striatum.2 These data suggest that NMDA receptors exert a tonic effect on dopamine autoreceptor expression preferentially in limbic regions. We now present data from a follow-up experiment to determine the effects of other glutamate receptor modulators on dopamine receptor expression in caudate-putamen (CPu), nucleus accumbens, core (core), and nucleus accumbens, shell (shell). Sprague-Dawley male rates (225–275 g) were treated with seven daily injections of CNQX (an antagonist of both AMPA and kainate receptors), GYKI52466 (an AMPA receptor desensitization facilitator), riluzole (a glutamate release inhibitor), or DMSO (vehicle), and rats were sacrificed 24 hours after the last injection.3 Ten animals were treated per group. In situ histochemistry for preprodynorphin and preproenkephalin transcripts, and D1 and D2 receptor mRNAs was performed as previously described.2 Results are shown in FIGURE 1. D1 and opioid peptide precursor mRNA were not affected by any of the treatments, while D2 mRNA was significantly decreased by riluzole and GYKI52466 treatments. Riluzole and GYKI52466 equally decreased the expression of D2 receptors in both dorsal and ventral striatal regions. This is in contrast to the effects of MK-801,2 and suggests that our previously reported results after NMDA receptor antagonist

Early postnatal development of the rat corticostriatal pathway: an anterograde axonal tracing study using biocytin pellets.

The ontogenetic development of the neocortical projections to the striatum was studied in postnatal rats by sensitive anterograde tracing with biocytin. The developmental status of this mainly glutamatergic pathway is important as it plays a major role in regulation of striatal maturation and induction of excitotoxic striatal neurodegeneration resembling the type found in Huntington's disease. Biocytin pelletts were injected into the motorcortex caudal forelimb area of newborn rats and of rats aged 3, 6, 13, 27 and 61 days followed by sacrifice and visualisation of the tracer 24 h later, at P1, P7, P14, P28 and P62, respectively. Biocytin pellets were also injected into the motorcortex jaw-lip-tongue area and into the cingulate cortex of newborn and 6-day-old rats. The biocytin pellets produced intense anterograde labelling of corticofugal projection fibres from the injection sites, as well as a local Golgi-like labelling of neurons. From postnatal day 1 into adult age efferent fibres from the motorcortex caudal forelimb area displayed a progressively denser innervation of the ipsilateral and contralateral, dorsolateral striatum. The terminating fibres were most dense in the ipsilateral striatum. In the dorsolateral striatum the corticostriatal fibres displayed a patch/matrix-like arrangement from postnatal day 14 onwards. Injections into the motorcortex jaw-lip-tongue area at postnatal days 0 and 6 displayed a progressive, denser innervation of the ipsilateral and contralateral ventrolateral striatum. The cingulate corticostriatal fibre projection, was more developed at birth than the projection from the motorcortex and increased its fibre density in the ipsilateral dorsomedial striatum up to at least day 7. the ipsilateral corticostriatal projections from the rat motorcortex and cingulate areas are present in newborn rats. During postnatal life the pathway develops further and specialisation of the terminating fibres into a patch/matrix like arrangement can be identified by postnatal day 14.

Neuroinvasiveness of pseudorabies virus injected intracerebrally is dependent on viral concentration and terminal field density.

Pseudorabies virus (PRV), a neurotropic swine alpha herpesvirus, has been used extensively for transneuronal analysis ofmultisynaptic circuitry after peripheral injection. In the present analysis, we examined the influence of viral concentration and neuronal architecture on the invasiveness, replication, and transynaptic passage of an attenuated strain of PRV (PRV-Bartha) injected into rat striatum. Different concentrations of PRV-Bartha were injected into the striatum at a constant rate of infusion (10 nl/minute), and animals were killed 50 hours later. Viral concentration was manipulated by either altering the volume of the inoculum (100, 50, 20 nl) or by diluting the inoculum within a constant volume of 100 nl. Immunohistochemical localization of infected neurons revealed dramatic differences in the progression of infection that were dependent directly on the concentration of injected virus. In every case, the pattern of infection was consistent with preferential uptake of virions by axon terminals and retrograde transynaptic passage of virus from the injection site. The known topographically organized corticostriatal projections permitted a precise definition of the zone of viral uptake. This analysis demonstrated that the "effective zone of viral uptake" (i.e., the zone within which viral uptake led to productive replication of virus) varied in relation to the concentration of injected virus, with the highest concentration of PRV invading terminals within a 500 microm radius of the canula. Concentration-dependent changes in the progression of retrograde transynaptic infection also were observed. The highest concentration of virus produced the most extensive infection. The distribution of infected neurons in these cases included those with known afferent projections to striatum as well as those that became infected by retrograde transynaptic infection. Lesser concentrations of PRV-Bartha produced an increasingly restricted infection of the same circuitry within the same postinoculation interval. It is noteworthy that neurons known to elaborate dense striatal terminal fields were less sensitive to reduction in viral concentration than those giving rise to terminal fields of lesser density. Collectively, the data indicate that the onset of viral replication after intracerebral injection of PRV is directly dependent on virus concentration and terminal field density at the site of virus injection.

Laminar segregation of the cortical plate during corticogenesis is accompanied by changes in glutamate receptor expression

We tested the hypothesis that subtypes of glutamate receptors (GluRs) are differentially expressed during corticogenesis. The neocortex of fetal sheep (term = approximately 145 days) was evaluated by immunoblotting and immunohistochemistry to determine the protein expression of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) receptors (GluR1, GluR2/GluR3 [GluR2/3], and GluR4), kainate (KA) receptors (GluR6/GluR7 [GluR6/7]), and a metabotropic GluR (mGluR5). AMPA/KA receptors and mGluR5 were expressed in neocortex by midgestation. GluR1 and mGluR5 expression increased progressively, with expression being maximal just before birth and then decreasing postnatally. GluR2/3 and GluR6/7 levels increased progressively during corticogenesis to reach adult levels near term. GluR4 was expressed at low levels during corticogenesis and in adult neocortex. The localizations of GluRs in the developing neocortex were distinct. Each GluR had a differential localization within the marginal zone, cortical plate, and subplate. GluR subtypes were expressed in laminar patterns before major cytoarchitectonic segregation occurred based on Nissl staining, although connectional patterns were emergent by midgestation based on labeling of corticostriatal projections with DiI. The GluR localizations changed during cortical plate segregation, resulting in highly differential distributions in the neocortex at term. AMPA/KA receptors were expressed transiently in proliferative zones and in developing white matter. Oligodendrocytes in fetal brain expressed AMPA receptors. The expression of ion channel and metabotropic GluR subtypes is dynamic during corticogenesis, with subtype- and subunit-specific regulation occurring during the laminar segregation of the cortical plate and differentiation of the neocortex.

Cellular Localization of Huntingtin in Striatal and Cortical Neurons in Rats: Lack of Correlation with Neuronal Vulnerability in Huntington’s Disease

Immunohistochemistry and single-cell RT-PCR were used to characterize the localization of huntingtin and/or its mRNA in the major types of striatal neurons and in corticostriatal projection neurons in rats. Single-label immunohistochemical studies revealed that striatum contains scattered large neurons rich in huntingtin and more numerous medium-sized neurons moderate in huntingtin. Double-label immunohistochemical studies showed that the large huntingtin-rich striatal neurons include nearly all cholinergic interneurons and some parvalbuminergic interneurons. Somatostatinergic striatal interneurons, which are medium in size, rarely contained huntingtin. Calbindin immunolabeling showed that the vast majority of the medium-sized striatal neurons that contain huntingtin are projection neurons, but only approximately 65% of calbindin-labeled projection neurons (localized to the matrix compartment of striatum) were labeled for huntingtin. Calbindin-containing projection neurons of the matrix compartment and calbindin-negative projection neurons of the striatal patch compartment contained huntingtin with comparable frequency. Single-cell RT-PCR confirmed that striatal cholinergic interneurons contain huntingtin, but only approximately 65% of projection neurons contained detectable huntingtin message. The finding that huntingtin is not consistently found in striatal projection neurons [which die in Huntington's disease (HD)] but is abundant in striatal cholinergic interneurons (which survive in Huntington's disease) suggests that the mutation in huntingtin that causes HD may not directly kill neurons. In contrast to the heterogeneous expression of huntingtin in the different striatal neuron types, we found all corticostriatal neurons to be rich in huntingtin protein and mRNA. One possibility raised by our findings is that the HD mutation may render corticostriatal neurons destructive rather than render striatal neurons vulnerable.

Thalamic input to parvalbumin-immunoreactive GABAergic interneurons: organization in normal striatum and effect of neonatal decortication

The neocortex and thalamus send dense glutaminergic projections to the neostriatum. The neocortex makes synaptic contact with spines of striatal projection neurons, and also targets a distinct class of GABAergic interneurons immunoreactive for the calcium-binding protein parvalbumin. We determined whether the parafascicular thalamic nucleus also targets striatal parvalbumin-immunoreactive interneurons. The anterograde tracer biotinylated dextranamine was injected into the parafascicular nucleus of adult rats. Double-labeled histochemistry/immunohistochemistry revealed overlapping thalamic fibres and parvalbumin-immunoreactive neurons in the neostriatum. Areas of overlap within the sensorimotor striatum were analysed by electron microscopy. Of 311 synaptic boutons originating from the parafascicular nucleus, 75.9% synapsed with unlabeled dendrites, 22.5% with unlabeled spines, and 1.3% had parvalbumin-immunoreactive dendrites as a postsynaptic target. Only 4% of all asymmetric synapses on parvalbumin-immunoreactive dendrites were derived from the parafascicular nucleus. A separate group of animals underwent bilateral neocortical deafferentation on the third postnatal day, prior to injection of anterograde tracer into the parafascicular nucleus of adult animals. These experiments were performed with the dual purpose of (i) reducing the possibility that thalamic inputs to parvalbumin-immunoreactive neurons are the result of transsynaptic uptake of tracer by a thalamo-cortico-striatal route, and (ii) determining whether competitive interactions between developing corticostriatal and thalamostriatal fibres may account for the relatively sparse thalamic input onto parvalbumin-immunoreactive interneurons. In decorticates, 219 striatal synaptic contacts derived from the parafascicular nucleus, out of which 77.2% were on unlabeled dendrites, 20.9% were upon unlabeled spines, and 0.9% targeted parvalbumin-immunoreactive dendrites. We conclude that the thalamic parafascicular nucleus indeed sends synaptic input to parvalbumin-immunoreactive striatal neurons. Parafascicular nucleus inputs to striatal parvalbumin-immunoreactive interneurons are sparse in comparison to other asymmetric inputs, most of which are likely to be of cortical origin. The synaptic profile of thalamostriatal inputs to parvalbumin-immunoreactive neurons and unlabeled elements is unchanged following neonatal decortication. This suggests that competitive interaction between developing thalamostriatal and corticostriatal projections is not a major mechanism determining synaptic input to striatal subpopulations.

Axonal transport of N-terminal huntingtin suggests early pathology of corticostriatal projections in Huntington disease.

Aggregation of N-terminal mutant huntingtin within nuclear inclusions and dystrophic neurites occurs in the cortex and striatum of Huntington disease (HD) patients and may be involved in neurodegeneration. We examined the prevalence of inclusions and dystrophic neurites in the cortex and striatum of 15 adult onset HD patients who had mild to severe striatal cell loss (grades 1, 2 or 3) using an antibody that detects the N-terminal region of huntingtin. Nuclear inclusions were more frequent in the cortex than the striatum and were sparse or absent in the striatum of patients with low-grade striatal pathology. Dystrophic neurites occurred in both regions. Patients with low-grade striatal pathology had numerous fibers with immunoreactive puncta and large swellings within the striatal neuropil, the subcortical white matter, and the internal and external capsules. In the globus pallidus of 3 grade 1 cases, N-terminal huntingtin markedly accumulated in the perinuclear cytoplasm and in some axons but not in the nucleus. Findings suggest that in the earlier stages of HD, accumulation of N-terminal mutant huntingtin occurs in the cytoplasm and is associated with degeneration of the corticostriatal pathway.

Double anterograde tracing of outputs from adjacent “barrel columns” of rat somatosensory cortex. Neostriatal projection patterns and terminal ultrastructure

The sensory input to the neostriatum from groups of cortical cells related to individual facial vibrissae has been investigated at both light- and electron-microscopic resolution. The purpose of the study was to establish the extent to which corticostriatal input maintains the anatomical coding of spatial information that is present in cortex. A double anterograde tracing method was used to identify the output projections from groups of adjacent neurons in different barrel columns, so that the anatomical relationships between two groups could be studied throughout their length. Adjacent whiskers are represented in adjoining cortical barrels and an examination of corticostriatal projections from these reveals two patterns of projection. In one, the anatomical topography is partially preserved; the barrels are represented in adjoining, discrete, areas of the somatosensory neostriatum. In the second projection pattern, the neostriatal innervation is diffuse and adjacent barrels are represented in overlapping regions of the neostriatum. Moreover, the fibres are thinner, have smaller boutons, and are present in both the ipsilateral and contralateral neostriatum. The two systems also enter the neostriatal neuropile separately. The discrete topographic system enters the adjacent neostriatum as collaterals which leave the descending corticofugal fibres at right angles, while the diffuse system enters directly from the corpus callosum at an acute angle. Examination of the neostriatal terminal fields by correlated light and electron microscopy, shows that characteristic axospinous terminals on spiny neurons are made by both groups of cortical fibres, although they differ in their size and morphology. It is concluded that at least two corticostriatal pathways arise from the barrel cortex. One connection maintains some of the anatomical code implicit in the barrel pattern of primary somatosensory cortex, but another, more diffuse, system is overlaid upon it which may carry different information from this complex area of cortex.

Anesthetics Eliminate Somatosensory-Evoked Discharges of Neurons in the Somatotopically Organized Sensorimotor Striatum of the Rat

The somatotopic organization of the lateral striatum has been demonstrated by anatomical studies of corticostriatal projections from somatosensory and motor cortices and by single-cell recordings in awake animals. The functional organization in the rat, characterized thus far in the freely moving rat preparation, could be mapped more precisely if a stereotaxic, and possibly an anesthetized, preparation could be used. Because striatal discharges evoked by innocuous somatosensory stimulation are used in mapping, this study tested whether such discharges can be observed during anesthesia, encouraged by responsiveness during anesthesia in somatosensory cortical layers projecting to the striatum. Electrode tracks through lateral striatum of anesthetized rats (pentobarbital or ketamine) revealed spontaneously discharging neurons but no discharges evoked by somatosensory examination (passive manipulation and cutaneous stimulation of 14 body parts). Similar tracks in chronically implanted rats showed evoked firing at numerous sites during wakefulness but not during anesthesia (pentobarbital or urethane). Comparisons of the activity of individual neurons between wakefulness and anesthesia showed that pentobarbital, ketamine, chloral hydrate, urethane, or metofane eliminated evoked firing and suppressed spontaneous firing. Recovery time was greater for neural than for behavioral measures. Thus, mapping as proposed is ruled out, and more importantly, the data show that somatotopically organized lateral striatal neurons stop discharging in response to natural stimulation during anesthesia. Available data indicate they do not reach threshold in response to depolarizations produced by glutamatergic corticostriatal synaptic transmission projected from the somatosensory cortex. These data and demonstrations of anesthetic-induced imbalances in most striatal neurotransmitters emphasize that many results regarding striatal physiology and pharmacology during anesthesia cannot be extrapolated to behavioral conditions, thus indicating the need for more empirical testing in conscious animals.

Localization of ionotropic glutamate receptors in caudate‐putamen and nucleus accumbens septi of rat brain: Comparison of NMDA, AMPA, and kainate receptors

Changes in binding of selective radioligands at NMDA ([3H]MK-801), AMPA ([3H]CNQX), and kainate ([3H]kainic acid) glutamate (GLU) ionotropic receptors in rat caudate-putamen (CPu) and nucleus accumbens (NAc) were examined by quantitative autoradiography following: 1) unilateral surgical ablation of frontal cerebral cortex to remove descending corticostriatal GLU projections, 2) unilateral injection of kainic acid (KA) into CPu or NAc to degenerate local intrinsic neurons, or 3) unilateral injections of 6-hydroxydopamine (6-OH-DA) into substantia nigra to degenerate ascending nigrostriatal dopamine (DA) projections. Cortical ablation significantly decreased NMDA receptor binding in ipsilateral medial CPu (20%), and NAc (16%), similar to previously reported losses of DA D4 receptors. KA lesions produced large losses of NMDA receptor labeling in CPu and NAc (both by 52%), AMPA (41% and 45%, respectively), and kainate receptors (40% and 45%, respectively) that were similar to the loss of D2 receptors in CPu and NAc after KA injections. Nigral 6-OH-DA lesions yielded smaller but significant losses in NMDA (17%), AMPA (12%), and kainate (11%) receptor binding in CPu. The results indicate that most NMDA, AMPA, and kainate receptors in rat CPu and NAc occur on intrinsic postsynaptic neurons. Also, some NMDA, but not AMPA or kainate, receptors are also found on corticostriatal projections in association with D4 receptors; these may, respectively, represent excitatory presynaptic NMDA autoreceptors and inhibitory D4 heteroceptors that regulate GLU release from corticostriatal axons in medial CPu and NAc. Conversely, the loss of all three GLU receptor subtypes after lesioning DA neurons supports their role as excitatory heteroceptors promoting DA release from nigrostriatal neurons. Synapse 30:227–235, 1998. © 1998 Wiley-Liss, Inc.

AMPA receptor binding and subunit mRNA expression in prefrontal cortex and striatum of elderly schizophrenics.

The dopamine hypothesis of schizophrenia has recently evolved into a model of dysfunctional integration between cortical and subcortical dopaminergic activity. Anatomical data suggest that regional alterations in dopaminergic activity may be linked by means of the rich glutamatergic innervation of the striatum by corticostriatal projections, suggesting a potential role for glutamatergic dysfunction in schizophrenia. Although pharmacological data have implicated the NMDA subtype of glutamate receptor in this illness, disturbance in AMPA receptor expression could potentially lead to the NMDA receptor hypoactivity hypothesized in schizophrenia. To address this possibility, we examined AMPA receptor binding and subunit mRNA levels in prefrontal cortex and striatum of schizophrenics and matched controls. There were no significant differences in AMPA receptor binding or subunit mRNA levels in either prefrontal cortical or striatal regions of schizophrenics. Furthermore, AMPA receptor expression did not seem to be regulated by chronic antipsychotic drug exposure, when neuroleptic treated and drug-free schizophrenics were analyzed separately. These data do not support a role for altered AMPA receptor expression in cortex and striatum in schizophrenia.

Axonal arborization of corticostriatal and corticothalamic fibers arising from prelimbic cortex in the rat.

This study aimed at elucidating the branching pattern of striatal and thalamic projections arising from prelimbic (Cg3) cortex in the rat. Small pools (5-15 cells) of neurons were microiontophoretically injected with biotin-dextran or biocytin and their labeled axons were individually reconstructed from serial horizontal sections immunostained for calbindin-D28k to delineate striatal patch/matrix compartments. Reconstruction of > 40 axons shows that all Cg3 corticofugal fibers, including corticothalamic axons from layer VI, course through the patch network in the rostromedial sector of the striatum. Corticostriatal projections arise from two types of layer V cells: (i) long-range corticofugal neurons, whose main axons reach the brainstem and/or spinal cord, and (ii) neurons arborizing into both striatum and claustrum, either ipsi-, contra- or bilaterally. The axons of these two types of neurons arborize profusely in striatal patches and only sparsely in the matrix. Layer VI neurons do not arborize in the striatum but target principally the thalamus. The same corticothalamic axon can innervate the anterior, rostral intralaminar and mediodorsal thalamic nuclei. These findings support the concept that no corticofugal fiber system exists that is solely devoted to the striatum. They also shed new light on how neural information from prelimbic cortex is conveyed to various subcortical limbic structures in the rat.

Corticostriatal connections of the superior temporal region in rhesus monkeys

Corticostriatal connections of auditory areas within the supratemporal plane and in rostral and caudal portions of the superior temporal gyrus were studied by the autoradiographic anterograde tracing technique. The results show that the primary auditory cortex has limited projections to the caudoventral putamen and to the tail of the caudate nucleus. In contrast, the second auditory area within the circular sulcus has connections to the rostral and the caudal putamen and to the body of the caudate nucleus and the tail. The association areas of the superior temporal gyrus collectively have widespread corticostriatal projections characterized by differential topographic distributions. The rostral part of the gyrus projects to ventral portions of the head of the caudate nucleus and of the body and to the tail. In addition, there are connections to rostroventral and caudoventral portions of the putamen. The mid-portion of the gyrus projects to similar striatal regions, but the connections to the head of the caudate nucleus are less extensive. Compared with the rostral and middle parts of the superior temporal gyrus, the caudal portion has little connectivity to the tail of the caudate nucleus. It projects more dorsally within the head and the body and also more dorsally within the caudal putamen. These differential patterns of corticostriatal connectivity are consistent with functional specialization at the cortical level.

Corticostriatal connections of the superior temporal region in rhesus monkeys

Corticostriatal connections of auditory areas within the supratemporal plane and in rostral and caudal portions of the superior temporal gyrus were studied by the autoradiographic anterograde tracing technique. The results show that the primary auditory cortex has limited projections to the caudoventral putamen and to the tail of the caudate nucleus. In contrast, the second auditory area within the circular sulcus has connections to the rostral and the caudal putamen and to the body of the caudate nucleus and the tail. The association areas of the superior temporal gyrus collectively have widespread corticostriatal projections characterized by differential topographic distributions. The rostral part of the gyrus projects to ventral portions of the head of the caudate nucleus and of the body and to the tail. In addition, there are connections to rostroventral and caudoventral portions of the putamen. The mid-portion of the gyrus projects to similar striatal regions, but the connections to the head of the caudate nucleus are less extensive. Compared with the rostral and middle parts of the superior temporal gyrus, the caudal portion has little connectivity to the tail of the caudate nucleus. It projects more dorsally within the head and the body and also more dorsally within the caudal putamen. These differential patterns of corticostriatal connectivity are consistent with functional specialization at the cortical level. J. Comp. Neurol. 399:384–402, 1998. © 1998 Wiley-Liss, Inc.

Excitatory amino acids as neurotransmitters of corticostriatal projections: immunocytochemical evidence in the rat.

The retrograde transport of a tracer has been combined with peroxidase immunocytochemistry to verify whether corticostriatal (CS) neurons contain in their cell bodies high levels of glutamate (Glu) and aspartate (Asp). Injections of WGAapoHRP-Au in the caudate/putamen of adult rats produced retrograde labeling of a large number of layer V neurons of wide regions of the ipsilateral cerebral cortex; fewer labeled neurons were also found on the contralateral side. In all experiments, most CS neurons were seen in the agranular frontal cortex, in both the medial and the lateral subdivisions. Moreover, numerous retrogradely labeled neurons were observed in the cingulate cortex and in the granular parietal cortex, depending on the location of the injection site in the various experiments. The majority of CS neurons examined were immunostained using antibodies against glutaraldehyde-conjugates of Glu or Asp. Glu immunopositive neurons resulted 52-61% of CS neurons. Asp immunopositive neurons ranged between 53% and 62%. In the cortical tissue where Glu and Asp antisera were visualized simultaneously, up to 96% of the CS neurons were immunostained. The latter finding indicates that the populations of Glu and Asp immunopositive neurons are largely segregated and that virtually all cortical neurons projecting to the striatum contain high concentrations of Glu and/or Asp, thus corroborating the hypothesis that CS projections use excitatory amino acids as neurotransmitters.

The Basal Ganglia and Chunking of Action Repertoires

The basal ganglia have been shown to contribute to habit and stimulus–response (S–R) learning. These forms of learning have the property of slow acquisition and, in humans, can occur without conscious awareness. This paper proposes that one aspect of basal ganglia-based learning is the recoding of cortically derived information within the striatum. Modular corticostriatal projection patterns, demonstrated experimentally, are viewed as producing recoded templates suitable for the gradual selection of new input–output relations in cortico-basal ganglia loops. Recordings from striatal projection neurons and interneurons show that activity patterns in the striatum are modified gradually during the course of S–R learning. It is proposed that this recoding within the striatum can chunk the representations of motor and cognitive action sequences so that they can be implemented as performance units. This scheme generalizes Miller's notion of information chunking to action control. The formation and the efficient implementation of action chunks are viewed as being based on predictive signals. It is suggested that information chunking provides a mechanism for the acquisition and the expression of action repertoires that, without such information compression would be biologically unwieldy or difficult to implement. The learning and memory functions of the basal ganglia are thus seen as core features of the basal ganglia's influence on motor and cognitive pattern generators.

Model of Cortical-Basal Ganglionic Processing: Encoding the Serial Order of Sensory Events

Several lines of evidence suggest that the prefrontal (PF) cortex and basal ganglia are important in cognitive aspects of serial order in behavior. We present a modular neural network model of these areas that encodes the serial order of events into spatial patterns of PF activity. The model is based on the topographically specific circuits linking the PF with the basal ganglia. Each module traces a pathway from the PF, through the basal ganglia and thalamus, and back to the PF. The complete model consists of an array of modules interacting through recurrent corticostriatal projections and collateral inhibition between striatal spiny units. The model's architecture positions spiny units for the classification of cortical contexts and events and provides bistable cortical-thalamic loops for sustaining a representation of these contextual events in working memory activations. The model was tested with a simulated version of a delayed-sequencing task. In single-unit studies, the task begins with the presentation of a sequence of target lights. After a short delay, the monkey must touch the targets in the order in which they were presented. When instantiated with randomly distributed corticostriatal weights, the model produces different patterns of PF activation in response to different target sequences. These patterns represent an unambiguous and spatially distributed encoding of the sequence. Parameter studies of these random networks were used to compare the computational consequences of collateral and feed-forward inhibition within the striatum. In addition, we studied the receptive fields of 20,640 model units and uncovered an interesting set of cue-, rank- and sequence-related responses that qualitatively resemble responses reported in single unit studies of the PF. The majority of units respond to more than one sequence of stimuli. A method for analyzing serial receptive fields is presented and utilized for comparing the model units to single-unit data.