Termination of cortical afferents on identified neurons in the caudate nucleus of the cat

Frotscher, Michael; Rinne, Ulrich; Häßler, R.; Wagner, A.

doi:10.1007/bf00238890

Cited by 62 publications

(35 citation statements)

References 26 publications

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“…The same dendrite receives symmetric synaptic contact (arrow) from another bouton, which in A seems to contain the BDHC reaction product indicating TH sory cortices in monkey terminate almost exclusively on the heads of dendritic spines. Previous ultrastructural data obtained in rat (Somogyi et al, 1981;Dube et al, 1988;Wictorin et al, 1989;Xu et al, 1989;Lapper and Bolam, 19921, cat (Kemp and Powell, 1971;Hassler et al, 1978;Frotscher et al, 1981) and monkey are consistent with the fact that the major postsynaptic targets of cortical afferents in the striatum are dendritic spines. Furthermore, the ultrastructural features and synaptic specializations of the anterogradely labelled cortical terminals observed in the present study are in keeping with those described in other species by means of anterograde labelling or anterograde degeneration methods (Kemp and Powell, 1971;Somogyi et al, 1981;Bouyer et al, 1984;Wictorin et al, 1989;.…”

Section: Corticostriatai and Thaiamostriatai Afferentssupporting

confidence: 72%

Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey

Smith

Bennett

Bolam

et al. 1994

J of Comparative Neurology

277

223

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The cerebral cortex and the intralaminar thalamic nuclei are the major sources of excitatory glutamatergic afferents to the striatum, whereas the midbrain catecholaminergic neurones provide a dense intrastriatal plexus of dopamine-containing terminals. Evidence from various sources suggests that there is a functional interaction between the glutamate- and dopamine-containing terminals in the striatum. The aim of the present study was to determine the synaptic relationships between cortical or thalamic inputs and the dopaminergic afferents in the sensorimotor territory of the monkey striatum. To address this issue, anterograde tracing in combination with immunocytochemistry for tyrosine hydroxylase (TH) was carried out by light and electron microscopy. Squirrel monkeys received injections of biocytin in the primary motor and somatosensory cortical areas or injections of either Phaseolus vulgaris-leucoagglutinin (PHA-L) or biocytin in the centromedian nucleus (CM) of the thalamus. Sections that included the striatum were processed to visualize the anterograde tracers alone or in combination with TH immunoreactivity. The anterogradely labelled fibres from the cerebral cortex and CM display a band-like pattern and are exclusively confined to the postcommissural region of the putamen, whereas TH-immunoreactive axon terminals are homogeneously distributed throughout the entire extent of the striatum. Electron microscopic analysis revealed that the anterogradely labelled terminals from the cerebral cortex form asymmetric synapses almost exclusively with the heads of dendritic spines. The thalamic terminals also form asymmetric synapses, but in contrast to cortical fibres, predominantly with dendrites (67.4%) and less frequently with spines (32.6%). The TH-immunoreactive boutons are heterogeneous in morphology. The most common type (84% of the total population) forms symmetric synapses; of these the majority is in contact with dendritic shafts (72.1%), less with spines (22.5%) and few with perikarya (5.4%). In sections processed to reveal anterogradely labelled cortical fibres and TH-immunoreactive structures, individual spines of striatal neurones were found to receive convergent synaptic inputs from both cortical and TH-immunoreactive boutons. In contrast, anterogradely labelled thalamic terminals and TH-immunoreactive boutons were never seen to form convergent synaptic contacts on the same postsynaptic structure. These findings suggest that the dopaminergic afferents are located to subserve a more specific modulation of afferent cortical input than afferent thalamic input in the sensorimotor territory of the striatum in primates.

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Section: Corticostriatai and Thaiamostriatai Afferentssupporting

confidence: 72%

Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey

Smith

Bennett

Bolam

et al. 1994

J of Comparative Neurology

277

223

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“…However, most synaptic contacts of thalamic origin occur on the dendritic shaft while those from the cortex are largely found on the head of dendritic spines of medium spiny neurons (Somogyi et al, 1981;Frotscher et al, 1981;Sadikot et al, 1992a;Smith et al, 1994). This ultrastructural arrangement suggests that thalamostriatal synapses can modulate, in a highly precise manner, the activity of medium spiny neurons that receive cortical input.…”

Section: Thalamostriatal Projectionsmentioning

confidence: 95%

Single-axon tracing and three-dimensional reconstruction of centre médian-parafascicular thalamic neurons in primates

Parent

2004

J. Comp. Neurol.

117

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The axonal projections from the centre median (CM)/parafascicular (Pf) thalamic complex in squirrel monkeys were studied after microiontophoretic injections of biotinylated dextran amine under electrophysiological guidance. A total of 29 axons connected to their parent cell body were entirely reconstructed from serial sections with a camera lucida. Our investigation shows that the CM and Pf nuclei in primates comprise three types of projection neurons: (1) neurons that innervate densely and focally the striatum; (2) neurons that arborize diffusely in the cerebral cortex; and (3) neurons that innervate both striatum and cerebral cortex. Striatal innervation of CM origin consists of dense clusters of axon terminals exhibiting pedunculated varicosities and forming oblique bands in the dorsolateral sector of putamen (sensorimotor striatal territory). The same type of striatal innervation occurs in the head of caudate nucleus (associative striatal territory) in cases of Pf-labeled neurons. The CM neurons that target cerebral cortex arborize principally in motor and premotor areas, whereas Pf neurons innervate chiefly prefrontal areas. Cortical innervation from both nuclei is much more profuse in layers V and VI than in layer I. Our three-dimensional reconstruction studies show that dendritic and axonal arborizations of CM neurons extend essentially along the sagittal plane. These results revealed that, in contrast to rodents where virtually all Pf neurons project to both striatum and cortex, the primate CM/Pf complex harbors several types of highly patterned projection neurons. As such, this complex might be considered as an integral part of the widely distributed basal ganglia neuronal system.

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“…Central to our understanding of basal ganglia function is the relationship between the glutamatergic projection from the cortex to the principal division of the basal ganglia, the striatum, and the dopaminergic innervation of the same region, derived from the substantia nigra pars compacta (Kemp and Powell, 1971;Wilson et al, 1983;Bouyer et al, 1984;Freund et al, 1984). Excitatory corticostriatal afferents mainly innervate the spines of medium-sized spiny projection neurons (Frotscher et al, 1981;Somogyi et al, 1981;Smith et al, 1998) and the response of the postsynaptic structure is modulated by synaptically released dopamine (Kerr and Wickens, 2001;Reynolds et al, 2001;Surmeier et al, 2007;Shen et al, 2008). Furthermore, the modulatory effect of dopamine on cortical transmission may also occur by synaptic spill-over and/or nonsynaptic release (Gonon, 1997;Cragg and Rice, 2004;Rice and Cragg, 2008) acting presynaptically and/or postsynaptically.…”

Section: Introductionmentioning

confidence: 99%

A Dopaminergic Axon Lattice in the Striatum and Its Relationship with Cortical and Thalamic Terminals

Moss

Bolam²

2008

J. Neurosci.

163

160

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Interactions between glutamatergic corticostriatal afferents and dopaminergic nigrostriatal afferents are central to basal ganglia function. The thalamostriatal projection provides a glutamatergic innervation of similar magnitude to the corticostriatal projection. We tested the hypotheses that (1) thalamostriatal synapses have similar spatial relationships with dopaminergic axons as corticostriatal synapses do and (2) the spatial relationships between excitatory synapses and dopaminergic axons are selective associations. We examined at the electron microscopic level rat striatum immunolabeled to reveal vesicular glutamate transporters (VGluTs) 1 and 2, markers of corticostriatal and thalamostriatal terminals, respectively, together with tyrosine hydroxylase (TH) to reveal dopaminergic axons. Over 80% of VGluT-positive synapses were within 1 m of a TH-positive axon and Ͼ40% were within 1 m of a TH-positive synapse. Of structures postsynaptic to VGluT1-or VGluT2-positive terminals, 21 and 27%, respectively, were apposed by a TH-positive axon and about half of these made synaptic contact. When structures postsynaptic to VGluT-positive terminals and VGluT-positive terminals themselves were normalized for length of plasma membrane, the probability of them being apposed by, or in synaptic contact with, a TH-positive axon was similar to that of randomly selected structures. Extrapolation of the experimental data to more closely reflect the distribution in 3D reveals that all structures in the striatum are within ϳ1 m of a TH-positive synapse. We conclude that (1) thalamostriatal synapses are in a position to be influenced by released dopamine to a similar degree as corticostriatal synapses are and (2) these associations arise from a nonselective dopaminergic axon lattice.

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Termination of cortical afferents on identified neurons in the caudate nucleus of the cat

Cited by 62 publications

References 26 publications

Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey

Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey

Single-axon tracing and three-dimensional reconstruction of centre médian-parafascicular thalamic neurons in primates

A Dopaminergic Axon Lattice in the Striatum and Its Relationship with Cortical and Thalamic Terminals

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