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Two different types of thalamic fibers innervate the rat striatum
BRAIN RESEARCH ELSEVIER
Brain Research 701 (1995) 288-292
Short communication
Two different types of thalamic fibers innervate the rat striatum Martin Desch~nes *, Jacques Bourassa, Andr6 Parent Centre de Recherche en Neurobiologie, H6pital de l'Enfant-JEsus, UniuersitE Lat,al, 1401 lSkme rue, QuEbec G1J lZ4, Canada
Accepted 22 August 1995
Abstract
Thalamostriatal projections were studied in rats by tracing the axons of small pools of thalamic neurons labeled anterogradely with biocytin. Single-cell mapping of these projections revealed two types of thalamostriatal fibers. The first type arises from the bushy relay cells of the central lateral and associative thalamic nuclei which arborize sparsely in the striatum by means of long varicose axon collaterals. The second type of fiber arises from large, reticular-like, relay cells located in the parafascicular and ethmoid nuclei. These latter fibers form dense clusters of terminations within the striatum and they also send branches to other components of the basal ganglia. These different morphological features suggest that the two types of fibers subserve different functions. Kevwords: Thalamostriatal fiber; CM/Pf complex; Central lateral nucleus; Posterior thalamic group; Striatal matrix; Ethmoid nucleus
Axonal transport studies have shown that the thalamostriatal projection arises predominantly from the intralaminat and midline nuclei with a minor contribution from certain nuclei of the lateral thalamus (see reviews in [14,15]). Anterograde transport of tritiated amino acids and bulk labeling of fibers with Phaseolus eulgaris leucoagglutinin were previously used to determine the topographical organization of the thalamostriatal projection in different species [1-3,7,8,13,16]. These techniques, however, do not allow the determination of the single-fiber composition of this projection. It was recently demonstrated that the extracellular injection of biocytin with fine micropipettes and low intensity currents can be used to label in a Golgi-like manner the axonal arborizations of small pools of cells in the central nervous system [12]. In the present study we employed this technique to determine the singlecell features of thalamic neurons that project to the rat striatum. The present report derives from a broader experimental series (n = 70 rats) that aimed at determining the axonal projections of thalamic neurons. Experiments were made in adult rats (Sprague-Dawley) under ketamine (75 m g / k g ) plus xylazine (5 m g / k g ) anesthesia. Housing and treatment conditions adhered to federally prescribed and
Corresponding author. Fax: (1) (418) 649-5910. 0006-8993/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSD1 0006-8993(95)011 24-2
University animal care and use guidelines. Biocytin injections were made with glass micropipettes (tip diameter: 2 - 4 /zm) filled with a solution of NaC1 (0.5 M) plus 2% biocytin (Sigma). A high compliance iontophoresis device (Neuro Data) was used to eject the tracer with positive current pulses of 150-400 nA (1 s o n / 1 s off) for 40 min. The stereotaxic coordinates of the atlas of Paxinos and Watson [11] were used to target various thalamic nuclei. After a survival period of 2 4 - 4 8 h animals were perfused with a saline solution followed by a fixative containing 4% paraformaldehyde and 0.5% glutaraldehyde in phosphate buffer (0.1M, pH 7.4). Brains were cut at 50 /zm on a freezing microtome and sections were processed for biocytin histochemistry using nickel-diaminobenzidine as the enzymatic substrate. In about half of the cases sections were also processed for cytochrome oxidase histochemistry [19] or calbindin D-28k immunohistochemistry [4]. Sections were mounted on gelatin-coated slides and covered with Permount. Cells and their axonal processes were drawn with a camera lucida using 40 x or 100 x objectives. Injection sites were also mapped at low magnification to refer their position to corresponding nuclei in the atlas of Paxinos and Watson [11]. When the nuclear location of labeled cells remained uncertain, coverslips were removed and sections were counterstained with thionin. The extracellular protocol of biocytin application produced Golgi-like labeling of 2 - 2 0 neurons at the injection
M. Desch~,nes et al. / Brain Research 701 ( lq(,~5) 288-2~,J2
sites. In the striatum 1 to 15 well-stained fibers were usually found. Axonal projections arising from forty-three injection sites served as data base for the present report
2S<,~
(see Fig. IA). Twelve sites were located in the parafascicular nucleus (Pf), eleven in the ethmoid nucleus (Eth), eight in different sectors of the posterior thalamic group (Po),
A
•
Po
!
B
1O0 gm
D
~,
50 gm
E
Fig. 1. Charts ~f biocytin injection sites in the rat thalamus and morphological features of type 1 thalamostriatal cells. Drawings in A show the location of 42 injection sites on frontal sections of the rat thalamus. Grey circles and black squares indicate respectively the injection sites where type I and type [I cells were located. One injection site situated in the A V nucleus is not depicted. Camera lucida drawing and photomicrograph of a bushy cell from the Po nucleus are sh~wn respectively in B and D. Drawing in C illustrates the loosely organized collaterals within a striatal terminal field. Varicose endings emitted 'en pa~,san~" by type 1 axons are shown in E. Scale bars: 200 /am in D; 50 /am in E.
290
M. DeschOnes et al. / Brain Research 701 (1995) 288-292
six in the central lateral nucleus (CL), two in the lateral posterior nucleus (LP), two in the ventrobasal complex (VB), one in the mediodorsal nucleus (MD), and one in the anterior ventral nucleus (AV). Tracing single axons from these injection sites revealed that all the above mentioned thalamic nuclei, except the ventrobasal complex, distribute branches to the striatum.
A
Thalamostriatal projections arise from two types of neurons whose axons form different types of terminal fields. The first type of neuron, which is found in CL, Po, LP, MD and AV nuclei, has the typical bushy appearance that characterizes the morphology of relay cells of most thalamic nuclei (Fig. 1B,D). They display many short radiating dendrites studded with protrusions and grapelike
B
1 O0 I~m
(
Fig. 2. Morphological features of type II thalamostriatal cells. Camera lucida drawing and photomicrograph of a large Pf cell are shown respectively in A and B. Drawing in C illustrates the lace-like appearance of the terminal field in the striatum. Thc grape-like terminations arising from type II axons is shown in D. Scale bars: 200 /zm in B; 50 /zm in D.
M. DeschOnes et al. / Brain Research 701 (1995) 28?4-292
appendages. The total extent of their dendritic fields is about 250 /am. All CL neurons and about 50% of cells in the above mentioned nuclei project to the striatum. Axons of bushy cells distribute branches in the thalamic reticular nucleus, arborize sparsely in the striatum and more heavily in the cerebral cortex. The striatal projection is made of long varicose axonal branches aligned rostrocaudally which appear to contact en passant a large number of neurons (Fig. 1C,E). The second type of neuron consists of a distinct population of large relay cells tbal are found in the Pf and Eth nuclei. These neurons resemble those of the thalamic reticular nucleus. Pf and Eth cells have polygonal or ovoid somata of about 2(I-25 /am from which emerge 4 - 5 thick, long and poorly branched dendrites bearing spines and filamentous appendages (Fig. 2A,B). These dendrites extend over considerable distances generating domains of up to 1.5 ram. Axons arising from these large neurons branch heavily in the striatum but very sparsely in the cortex. In the striatum they form well-spaced and dense clusters of terminations producing the typical lace-like plexuses shown in Fig. 2C,D). As a rule the axon of these large thalamostriatal cells also distribute branches to the thalamic reticular nucleus as well as to olher components of the basal ganglia (globus pallidus, entopeduncular nucleus, subthalamic nucleus [5]). Bushy relay neurons represent the commonest cell type in the dorsal thalamus [10]. Their dendritic trees are either bitufted (as in VB) or radialing (as in Po) and their high degree of branching offers a large surface area for synaptic contacts in a relatively small volume of tissue. These cells share similar electrophysiological characteristics [9] and their axons, after branching in the thalamic reticular nucleus, project principally to the cerebral cortex. A subpopulation of bushy cells, comprising cells of the central lateral nucleus and about half of the neuronal population of the other thalamic nuclei inw,'stigated also branch upon the striatum. Although we did not make biocytin injections in every thalamic nuclei, our data suggest that, except the sensory-specific nuclei, all the other thalamic nuclei might project to the striatum. Albeit sparse, this thalamostriatal projection from the bushy cells form well-defined rostrocaudally oriented bands of varicose collaterals in specific regions of the striatum. These fibers may exert a significant excitatory drive on their targets when a large number of relay ceils fire in synchrony. A second class of thalamic cells is represented by the large relay cells of the Pf and Eth nuclei. These neurons, which were previously evidenced in the centromedianparafascicular complex of rats, cats and monkeys [5,6,17,18,20] possess very long and poorly ramified dendrites offering a receptive surface upon which heterogeneous afferents can make contact. Indeed, Pf and Eth neurons lie in a region rich in various excitatory and inhibitory inputs (spinothalamic, reticular thalamic, collicular, incertal, pretectal, parabrachial, entopeduncular,
2t~ I
tegmental; see [15]). Poorly branched and extensive dendrites contacted by a variety of synaptic inputs represent an ideal architectonic design for integrative a n d / o r associative functions. The axons of these cells also distribute collaterals to the thalamic reticular nucleus, but in marked contrast with those of the bushy neurons, they generate very dense clusters of terminals in the striatum. This clustering suggests that each axon establishes mutiple contacts with the dendrites of a single striatal cell and, consequently, the firing of a single large neuron may significantly affect the excitability of the postsynaptic elements. Previous studies have mostly emphasized the topographical and compartmental distribution of thalamostriatal fibers within the striatum. The two types of fibers described in the present study arise from thalamic nuclei that project to the striatal matrix [14]. This dual thalamostriatal innervation of the matrix compartment offers a new anatomical background for the interpretation of physiological and clinical data concerning the role of the striatum in normal and disease states.
Acknowledgements This research was supported by the Medical Research Council of Canada
References [1] Beckstead, R.M., The thalamostriatal projection in the cat, J. Comp. Neurol., 223 (1984)313-346. [2] Beckstead, R.M., A projection to the striatum from the medial subdivision of the posterior group of the thalamus in the cat, Brain Res., 3(10 ( 19841 351-356. [3] Berendse, H.W. and Groenewegen, H.J., Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum, J. Comp. Neurol., 299 (1990) 187-228. [4] Cello. M.R., Calbindin D-28k and parvalbumin in the rat nervous system, Neuroseience, 35 (19901 375 475. [5] Desch,Snes, M, Bourassa, J., Van Diep. D. and Parent, A., A single-cell study of the axonal projections arising fi-orn the parafascicular and ethmoid nuclei in the rat, Eur. ,I. Neuro.sci., in press. [6] Hazlctt, J.C., Dutta, C.R. and Fox, ('.A., The neurons in the centromcdian-parafascicular complex of the monkcv (Maeaca malatta): a Golgi study, J. Comp. Neurol., 168 (1976) 41-74. [7] Hcrkenham, M., lntralaminar and parafascicular cffercnts to the striatum and cortex in the rat: tin auloradiographie study, 4nat. Ree., 190 (1978) 4211. [8] Hcrkenham, M., New perspectives on the organization and evolution of non-specific thalamocortical projections. In E.G. Jones and A. Peters (Eds.), Cerebral Cortex. Vol. 5. Plenum Press, New York, 1986, pp. 4(13 445. [9] Jahnsen, H. and Llinas, R., Electrophysiological properties of guinea pig thalamic neurones: an in vitro study, ,I. l'hysioL. 349 (19841 2/15-226. [10] Jones, E.G., The Thalamus, New York, Plenum Pres,~, 1~85. [11] Paxinos, G. and Watson, C., The Rat Brain in Stereotaxie ('oordlhates, 2nd edn., Academic Press, Sydney, 198¢~. [12] Pinault, D. and Desch,~nes, M., A method for the complete staining of identified neurons at wilt, Soc. Neuros'ei. Ab~tr., 19 ( 1t~93l 1320.
292
M. DeschOnes et al. /Brain Research 701 (19951 288-292
[13] Ragsdale, C.W. and Graybiel, A.M., Compartmental organization of the thalamostriatal connection in the cat, J. Comp. Neurol., 311 (1991) 134-167. [I4] Ragsda[e, C.W. and Graybiel, A.M., Multiple patterns of thalamostriatal innervation in the cat. In M. Bentivoglio and R. Spreafico (Eds.), Cellular Thalamic Mechanisms, Elsevier, Amsterdam, 1988, pp. 261-267. [15] Royce, G.J., Recent research on the centromedian and parafascicular nuclei. In M.B. Carpenter and A. Jayaraman (Eds.), The Basal Ganglia I1: Structure and Functions - - - Current Concepts, Vol. 32,
Plenum Press, New York, 1987, pp. 293-319. [16] Sadikot, A.F., Parent, A. and Francois, C., Efferent connections of the ccntromedian and parafascicular thalamic nuclei in the aquirrel monkey: a PHA-L study of subcortical projections, ,I. Comp. NeuroL, 315 (1992) 137-159.
[17] Scheibcl, M.E. and Scheibel, A.B., Structural organization of nonspecific thalamic nuclei and their projection toward cortex, Brain Res., 6 (19671 6(I-94. [18] Tseng, G. and Royce, G.J., A Golgi and ultrastructural analysis of the centromedian nucleus of the cat, J. Comp. Neurol., 245 (19861 359-378. [19] Wong-Riley, M.T.T., Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochromc oxidase histochemistry, Brain Res., 171 (19791 11-28. [20] Yamamoto, T., Noda, T., Samejima, A. and Oka, H., Electrophysiological and morphological features of thalamic neurons with special refcrence to the cercbellar and pallidal inputs. In M. Bentiw)glio and R. Spreafico (Eds.), Cellular Thalamic Mechanisms, Elsevicr, Amsterdam, 198g, pp. 239-260.
Brain Research 701 (1995) 288-292
Short communication
Two different types of thalamic fibers innervate the rat striatum Martin Desch~nes *, Jacques Bourassa, Andr6 Parent Centre de Recherche en Neurobiologie, H6pital de l'Enfant-JEsus, UniuersitE Lat,al, 1401 lSkme rue, QuEbec G1J lZ4, Canada
Accepted 22 August 1995
Abstract
Thalamostriatal projections were studied in rats by tracing the axons of small pools of thalamic neurons labeled anterogradely with biocytin. Single-cell mapping of these projections revealed two types of thalamostriatal fibers. The first type arises from the bushy relay cells of the central lateral and associative thalamic nuclei which arborize sparsely in the striatum by means of long varicose axon collaterals. The second type of fiber arises from large, reticular-like, relay cells located in the parafascicular and ethmoid nuclei. These latter fibers form dense clusters of terminations within the striatum and they also send branches to other components of the basal ganglia. These different morphological features suggest that the two types of fibers subserve different functions. Kevwords: Thalamostriatal fiber; CM/Pf complex; Central lateral nucleus; Posterior thalamic group; Striatal matrix; Ethmoid nucleus
Axonal transport studies have shown that the thalamostriatal projection arises predominantly from the intralaminat and midline nuclei with a minor contribution from certain nuclei of the lateral thalamus (see reviews in [14,15]). Anterograde transport of tritiated amino acids and bulk labeling of fibers with Phaseolus eulgaris leucoagglutinin were previously used to determine the topographical organization of the thalamostriatal projection in different species [1-3,7,8,13,16]. These techniques, however, do not allow the determination of the single-fiber composition of this projection. It was recently demonstrated that the extracellular injection of biocytin with fine micropipettes and low intensity currents can be used to label in a Golgi-like manner the axonal arborizations of small pools of cells in the central nervous system [12]. In the present study we employed this technique to determine the singlecell features of thalamic neurons that project to the rat striatum. The present report derives from a broader experimental series (n = 70 rats) that aimed at determining the axonal projections of thalamic neurons. Experiments were made in adult rats (Sprague-Dawley) under ketamine (75 m g / k g ) plus xylazine (5 m g / k g ) anesthesia. Housing and treatment conditions adhered to federally prescribed and
Corresponding author. Fax: (1) (418) 649-5910. 0006-8993/95/$09.50 © 1995 Elsevier Science B.V. All rights reserved SSD1 0006-8993(95)011 24-2
University animal care and use guidelines. Biocytin injections were made with glass micropipettes (tip diameter: 2 - 4 /zm) filled with a solution of NaC1 (0.5 M) plus 2% biocytin (Sigma). A high compliance iontophoresis device (Neuro Data) was used to eject the tracer with positive current pulses of 150-400 nA (1 s o n / 1 s off) for 40 min. The stereotaxic coordinates of the atlas of Paxinos and Watson [11] were used to target various thalamic nuclei. After a survival period of 2 4 - 4 8 h animals were perfused with a saline solution followed by a fixative containing 4% paraformaldehyde and 0.5% glutaraldehyde in phosphate buffer (0.1M, pH 7.4). Brains were cut at 50 /zm on a freezing microtome and sections were processed for biocytin histochemistry using nickel-diaminobenzidine as the enzymatic substrate. In about half of the cases sections were also processed for cytochrome oxidase histochemistry [19] or calbindin D-28k immunohistochemistry [4]. Sections were mounted on gelatin-coated slides and covered with Permount. Cells and their axonal processes were drawn with a camera lucida using 40 x or 100 x objectives. Injection sites were also mapped at low magnification to refer their position to corresponding nuclei in the atlas of Paxinos and Watson [11]. When the nuclear location of labeled cells remained uncertain, coverslips were removed and sections were counterstained with thionin. The extracellular protocol of biocytin application produced Golgi-like labeling of 2 - 2 0 neurons at the injection
M. Desch~,nes et al. / Brain Research 701 ( lq(,~5) 288-2~,J2
sites. In the striatum 1 to 15 well-stained fibers were usually found. Axonal projections arising from forty-three injection sites served as data base for the present report
2S<,~
(see Fig. IA). Twelve sites were located in the parafascicular nucleus (Pf), eleven in the ethmoid nucleus (Eth), eight in different sectors of the posterior thalamic group (Po),
A
•
Po
!
B
1O0 gm
D
~,
50 gm
E
Fig. 1. Charts ~f biocytin injection sites in the rat thalamus and morphological features of type 1 thalamostriatal cells. Drawings in A show the location of 42 injection sites on frontal sections of the rat thalamus. Grey circles and black squares indicate respectively the injection sites where type I and type [I cells were located. One injection site situated in the A V nucleus is not depicted. Camera lucida drawing and photomicrograph of a bushy cell from the Po nucleus are sh~wn respectively in B and D. Drawing in C illustrates the loosely organized collaterals within a striatal terminal field. Varicose endings emitted 'en pa~,san~" by type 1 axons are shown in E. Scale bars: 200 /am in D; 50 /am in E.
290
M. DeschOnes et al. / Brain Research 701 (1995) 288-292
six in the central lateral nucleus (CL), two in the lateral posterior nucleus (LP), two in the ventrobasal complex (VB), one in the mediodorsal nucleus (MD), and one in the anterior ventral nucleus (AV). Tracing single axons from these injection sites revealed that all the above mentioned thalamic nuclei, except the ventrobasal complex, distribute branches to the striatum.
A
Thalamostriatal projections arise from two types of neurons whose axons form different types of terminal fields. The first type of neuron, which is found in CL, Po, LP, MD and AV nuclei, has the typical bushy appearance that characterizes the morphology of relay cells of most thalamic nuclei (Fig. 1B,D). They display many short radiating dendrites studded with protrusions and grapelike
B
1 O0 I~m
(
Fig. 2. Morphological features of type II thalamostriatal cells. Camera lucida drawing and photomicrograph of a large Pf cell are shown respectively in A and B. Drawing in C illustrates the lace-like appearance of the terminal field in the striatum. Thc grape-like terminations arising from type II axons is shown in D. Scale bars: 200 /zm in B; 50 /zm in D.
M. DeschOnes et al. / Brain Research 701 (1995) 28?4-292
appendages. The total extent of their dendritic fields is about 250 /am. All CL neurons and about 50% of cells in the above mentioned nuclei project to the striatum. Axons of bushy cells distribute branches in the thalamic reticular nucleus, arborize sparsely in the striatum and more heavily in the cerebral cortex. The striatal projection is made of long varicose axonal branches aligned rostrocaudally which appear to contact en passant a large number of neurons (Fig. 1C,E). The second type of neuron consists of a distinct population of large relay cells tbal are found in the Pf and Eth nuclei. These neurons resemble those of the thalamic reticular nucleus. Pf and Eth cells have polygonal or ovoid somata of about 2(I-25 /am from which emerge 4 - 5 thick, long and poorly branched dendrites bearing spines and filamentous appendages (Fig. 2A,B). These dendrites extend over considerable distances generating domains of up to 1.5 ram. Axons arising from these large neurons branch heavily in the striatum but very sparsely in the cortex. In the striatum they form well-spaced and dense clusters of terminations producing the typical lace-like plexuses shown in Fig. 2C,D). As a rule the axon of these large thalamostriatal cells also distribute branches to the thalamic reticular nucleus as well as to olher components of the basal ganglia (globus pallidus, entopeduncular nucleus, subthalamic nucleus [5]). Bushy relay neurons represent the commonest cell type in the dorsal thalamus [10]. Their dendritic trees are either bitufted (as in VB) or radialing (as in Po) and their high degree of branching offers a large surface area for synaptic contacts in a relatively small volume of tissue. These cells share similar electrophysiological characteristics [9] and their axons, after branching in the thalamic reticular nucleus, project principally to the cerebral cortex. A subpopulation of bushy cells, comprising cells of the central lateral nucleus and about half of the neuronal population of the other thalamic nuclei inw,'stigated also branch upon the striatum. Although we did not make biocytin injections in every thalamic nuclei, our data suggest that, except the sensory-specific nuclei, all the other thalamic nuclei might project to the striatum. Albeit sparse, this thalamostriatal projection from the bushy cells form well-defined rostrocaudally oriented bands of varicose collaterals in specific regions of the striatum. These fibers may exert a significant excitatory drive on their targets when a large number of relay ceils fire in synchrony. A second class of thalamic cells is represented by the large relay cells of the Pf and Eth nuclei. These neurons, which were previously evidenced in the centromedianparafascicular complex of rats, cats and monkeys [5,6,17,18,20] possess very long and poorly ramified dendrites offering a receptive surface upon which heterogeneous afferents can make contact. Indeed, Pf and Eth neurons lie in a region rich in various excitatory and inhibitory inputs (spinothalamic, reticular thalamic, collicular, incertal, pretectal, parabrachial, entopeduncular,
2t~ I
tegmental; see [15]). Poorly branched and extensive dendrites contacted by a variety of synaptic inputs represent an ideal architectonic design for integrative a n d / o r associative functions. The axons of these cells also distribute collaterals to the thalamic reticular nucleus, but in marked contrast with those of the bushy neurons, they generate very dense clusters of terminals in the striatum. This clustering suggests that each axon establishes mutiple contacts with the dendrites of a single striatal cell and, consequently, the firing of a single large neuron may significantly affect the excitability of the postsynaptic elements. Previous studies have mostly emphasized the topographical and compartmental distribution of thalamostriatal fibers within the striatum. The two types of fibers described in the present study arise from thalamic nuclei that project to the striatal matrix [14]. This dual thalamostriatal innervation of the matrix compartment offers a new anatomical background for the interpretation of physiological and clinical data concerning the role of the striatum in normal and disease states.
Acknowledgements This research was supported by the Medical Research Council of Canada
References [1] Beckstead, R.M., The thalamostriatal projection in the cat, J. Comp. Neurol., 223 (1984)313-346. [2] Beckstead, R.M., A projection to the striatum from the medial subdivision of the posterior group of the thalamus in the cat, Brain Res., 3(10 ( 19841 351-356. [3] Berendse, H.W. and Groenewegen, H.J., Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum, J. Comp. Neurol., 299 (1990) 187-228. [4] Cello. M.R., Calbindin D-28k and parvalbumin in the rat nervous system, Neuroseience, 35 (19901 375 475. [5] Desch,Snes, M, Bourassa, J., Van Diep. D. and Parent, A., A single-cell study of the axonal projections arising fi-orn the parafascicular and ethmoid nuclei in the rat, Eur. ,I. Neuro.sci., in press. [6] Hazlctt, J.C., Dutta, C.R. and Fox, ('.A., The neurons in the centromcdian-parafascicular complex of the monkcv (Maeaca malatta): a Golgi study, J. Comp. Neurol., 168 (1976) 41-74. [7] Hcrkenham, M., lntralaminar and parafascicular cffercnts to the striatum and cortex in the rat: tin auloradiographie study, 4nat. Ree., 190 (1978) 4211. [8] Hcrkenham, M., New perspectives on the organization and evolution of non-specific thalamocortical projections. In E.G. Jones and A. Peters (Eds.), Cerebral Cortex. Vol. 5. Plenum Press, New York, 1986, pp. 4(13 445. [9] Jahnsen, H. and Llinas, R., Electrophysiological properties of guinea pig thalamic neurones: an in vitro study, ,I. l'hysioL. 349 (19841 2/15-226. [10] Jones, E.G., The Thalamus, New York, Plenum Pres,~, 1~85. [11] Paxinos, G. and Watson, C., The Rat Brain in Stereotaxie ('oordlhates, 2nd edn., Academic Press, Sydney, 198¢~. [12] Pinault, D. and Desch,~nes, M., A method for the complete staining of identified neurons at wilt, Soc. Neuros'ei. Ab~tr., 19 ( 1t~93l 1320.
292
M. DeschOnes et al. /Brain Research 701 (19951 288-292
[13] Ragsdale, C.W. and Graybiel, A.M., Compartmental organization of the thalamostriatal connection in the cat, J. Comp. Neurol., 311 (1991) 134-167. [I4] Ragsda[e, C.W. and Graybiel, A.M., Multiple patterns of thalamostriatal innervation in the cat. In M. Bentivoglio and R. Spreafico (Eds.), Cellular Thalamic Mechanisms, Elsevier, Amsterdam, 1988, pp. 261-267. [15] Royce, G.J., Recent research on the centromedian and parafascicular nuclei. In M.B. Carpenter and A. Jayaraman (Eds.), The Basal Ganglia I1: Structure and Functions - - - Current Concepts, Vol. 32,
Plenum Press, New York, 1987, pp. 293-319. [16] Sadikot, A.F., Parent, A. and Francois, C., Efferent connections of the ccntromedian and parafascicular thalamic nuclei in the aquirrel monkey: a PHA-L study of subcortical projections, ,I. Comp. NeuroL, 315 (1992) 137-159.
[17] Scheibcl, M.E. and Scheibel, A.B., Structural organization of nonspecific thalamic nuclei and their projection toward cortex, Brain Res., 6 (19671 6(I-94. [18] Tseng, G. and Royce, G.J., A Golgi and ultrastructural analysis of the centromedian nucleus of the cat, J. Comp. Neurol., 245 (19861 359-378. [19] Wong-Riley, M.T.T., Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochromc oxidase histochemistry, Brain Res., 171 (19791 11-28. [20] Yamamoto, T., Noda, T., Samejima, A. and Oka, H., Electrophysiological and morphological features of thalamic neurons with special refcrence to the cercbellar and pallidal inputs. In M. Bentiw)glio and R. Spreafico (Eds.), Cellular Thalamic Mechanisms, Elsevicr, Amsterdam, 198g, pp. 239-260.