Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-23T04:45:08.128Z Has data issue: false hasContentIssue false
  • English
  • Français

Projections from cingulate cortex to the cat’s thalamic reticular nucleus

Published online by Cambridge University Press:  31 August 2011

THOMAS FITZGIBBON  and
NICK KIKUCHI
THOMAS FITZGIBBON*
Affiliation:
Discipline of Anatomy & Histology, School of Medical Sciences and Bosch Institute, The University of Sydney, Sydney, New South Wales, Australia
NICK KIKUCHI
Affiliation:
Discipline of Anatomy & Histology, School of Medical Sciences and Bosch Institute, The University of Sydney, Sydney, New South Wales, Australia
*
*Address correspondence and reprint requests to: Thomas FitzGibbon, Discipline of Anatomy & Histology (F13) and Bosch Institute for Biomedical Research, The University of Sydney, Sydney, NSW 2006, Australia. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The cingulate cortex (CG) and the adjacent region designated as the splenial visual area (SVA) project to areas of the extrageniculate thalamic system that are concerned with processing visual information. En route to the thalamus, they pass through the thalamic reticular nucleus (TRN), an important source of thalamic inhibition. We wished to determine whether SVA axon collaterals projected to the previously defined visual sector of the TRN or a separate projection zone and did this differ from the projection zone of CG. We iontophoretically injected different neuroanatomical tracers into several locations within CG/SVA and traced the labeled axons through the TRN. The CG and SVA have a projection zone that only partially overlaps the dorsorostral regions of the visuocortical projection zone; there was no evidence to suggest separate SVA and CG zones or tiers of label within the TRN. The projection formed only a weak topographic map in the TRN, which is largely defined in the rostrocaudal axis and is similar to that of the area 7 projection; both projections have a high degree of overlap in the dorsal TRN. We postulate that CG/SVA may be involved in the initiation of orientation behaviors via stimulation of thalamic nuclei and attentional mechanisms of the TRN.

Keywords

WGA-HRPBDANeuroanatomical tracingThalamusCorticoreticular maps
Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 5 , September 2011 , pp. 433 - 444
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asanuma, C. (1992). Noradrenergic innervation of the thalamic reticular nucleus: A light and electron microscope immunohistochemical study in rats. The Journal of Comparative Neurology 319, 299–311.CrossRefGoogle ScholarPubMed
Avanzini, G., Broggi, G., Franceschetti, S. & Spreafico, R. (1980). Multisensory convergence and interaction in the pulvinar-lateralis posterior complex of the cat’s thalamus. Neuroscience Letters 19, 27–32.CrossRefGoogle ScholarPubMed
Avanzini, G., Panzica, F. & de Curtis, M. (2000). The role of the thalamus in vigilance and epileptogenic mechanisms. Clinical Neurophysiology 111, s19–s26.CrossRefGoogle ScholarPubMed
Bajo, V.M., Rouiller, E.M., Welker, E., Clarke, S., Villa, A., Deribaupierre, Y. & Deribaupierre, F. (1995). Morphology and spatial-distribution of corticothalamic terminals originating from the cat auditory-cortex. Hearing Research 83, 161–174.CrossRefGoogle ScholarPubMed
Benedek, G., Perény, J., Kovács, G., Fischer-Szátmári, L. & Katoh, Y.Y. (1997). Visual, somatosensory, auditory and nociceptive modality properties in the feline suprageniculate nucleus. Neuroscience 78, 179–189.CrossRefGoogle ScholarPubMed
Berman, A.L. & Jones, E.G. (1982). The Thalamus and Basal Telencephalon of the Cat. A Cytoarchitectonic Atlas with Stereotaxic Coordinates. Madison, WI: University of Wisconsin Press.Google Scholar
Clascá, F., llamas, A. & Reinoso-Suárez, F. (1997). Insular cortex and neighboring fields in the cat: A redefinition based on cortical microarchitecture and connections with the thalamus. The Journal of Comparative Neurology 384, 456–482.3.0.CO;2-H>CrossRefGoogle Scholar
Coleman, K.A. & Mitrofanis, J. (1996). Organization of the visual reticular thalamic nucleus of the rat. The European Journal of Neuroscience 8, 388–404.CrossRefGoogle ScholarPubMed
Conley, M. & Diamond, I.T. (1990). Organization of the visual sector of the thalamic reticular nucleus in Galago—Evidence that the dorsal lateral geniculate and pulvinar nuclei occupy separate parallel tiers. The European Journal of Neuroscience 2, 211–226.CrossRefGoogle Scholar
Conley, M., Kupersmith, A.C. & Diamond, I.T. (1991). The organization of projections from subdivisions of the auditory cortex and thalamus to the auditory sector of the thalamic reticular nucleus in Galago . The European Journal of Neuroscience 3, 1089–1103.CrossRefGoogle Scholar
Cooper, B.G., Manka, T.F. & Mizumori, S.J.Y. (2001). Finding your way in the dark: The retrospinal cortex contributes to spatial memory and navigation without visual cues. Behavioral Neuroscience 115, 1012–1028.CrossRefGoogle Scholar
Crabtree, J.W. (1992 a). The somatotopic organization within the cat’s thalamic reticular nucleus. The European Journal of Neuroscience 4, 1352–1361.CrossRefGoogle ScholarPubMed
Crabtree, J.W. (1992 b). The somatotopic organization within the rabbit’s thalamic reticular nucleus. The European Journal of Neuroscience 4, 1343–1351.CrossRefGoogle ScholarPubMed
Crabtree, J.W. (1996). Organization in the somatosensory sector of the cat’s thalamic reticular nucleus. The Journal of Comparative Neurology 366, 207–222.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Crabtree, J.W. (1998). Organization in the auditory sector of the cat’s thalamic reticular nucleus. The Journal of Comparative Neurology 390, 167–182.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Crabtree, J.W., Collingridge, G.L. & Isaac, J.T.R. (1998). A new intrathalamic pathway linking modality-related nuclei in the dorsal thalamus. Nature Neuroscience 1, 389–394.CrossRefGoogle ScholarPubMed
Crabtree, J.W. & Isaac, J.T.R. (2002). New intrathalamic pathways allowing modality-related and cross modality switching in the dorsal thalamus. The Journal of Neuroscience 22, 8754–8761.CrossRefGoogle ScholarPubMed
Crabtree, J.W. & Killackey, H.P. (1989). The topographic organization and axis of projection within the visual sector of the rabbit’s thalamic reticular nucleus. The European Journal of Neuroscience 1, 94–109.CrossRefGoogle ScholarPubMed
Crick, F. & Koch, C. (1990). Some reflections on visual awareness. Cold Spring Harbor Symposia on Quantitative Biology 55, 953–962.CrossRefGoogle ScholarPubMed
Deleuze, C. & Huguenard, J.R. (2006). Distinct electrical and chemical connectivity maps in the thalamic reticular nucleus: Potential roles in synchronization and sensation. The Journal of Neuroscience 26, 8633–8645.CrossRefGoogle ScholarPubMed
Deschênes, M., Veinante, P. & Zhang, Z.-W. (1998). The organization of corticothalamic projections: Reciprocity versus parity. Brain Research Reviews 28, 286–308.CrossRefGoogle ScholarPubMed
FitzGibbon, T. (1994). Rostral reticular nucleus of the thalamus sends a patchy projection to the pulvinar lateralis-posterior complex of the cat. Experimental Neurology 129, 266–278.CrossRefGoogle Scholar
FitzGibbon, T. (2000). Cortical projections from the suprasylvian gyrus to the reticular thalamic nucleus in the cat. Neuroscience 97, 643–655.CrossRefGoogle Scholar
FitzGibbon, T., Bittar, R.G. & Dreher, B. (1999). Projections from striate and extrastriate visual cortices of the cat to the reticular thalamic nucleus. The Journal of Comparative Neurology 410, 467–488.3.0.CO;2-Y>CrossRefGoogle Scholar
FitzGibbon, T., Tevah, L.V. & Sefton, A.J. (1995). Connections between the reticular nucleus of the thalamus and pulvinar-lateralis posterior complex: A WGA-HRP study. The Journal of Comparative Neurology 363, 489–504.CrossRefGoogle ScholarPubMed
Funke, K. & Eysel, U.T. (1998). Inverse correlation of firing of single topographically matched perigeniculate neurons and cat dorsal lateral geniculate relay cells. Visual Neuroscience 15, 711–729.CrossRefGoogle ScholarPubMed
Gentet, L.J. & Ulrich, D. (2003). Strong, reliable and precise synaptic connections between thalamic relay cells and neurones of the nucleus reticularis in juvenile rats. The Journal of Physiology 546, 801–811.CrossRefGoogle ScholarPubMed
Gentet, L.J. & Ulrich, D. (2004). Electrophysiological characterization of synaptic connections between layer VI cortical cells and neurons of the nucleus reticularis thalami in juvenile rats. The European Journal of Neuroscience 19, 625–633.CrossRefGoogle ScholarPubMed
Graybiel, A.M. & Berson, D.M. (1980). Histochemical identification and afferent connections of subdivisions in the lateralis posterior-pulvinar complex and related thalamic nuclei in the cat. Neuroscience 5, 1175–1238.CrossRefGoogle ScholarPubMed
Guillery, R.W., Feig, S.L. & Lozsádi, D.A. (1998). Paying attention to the thalamic reticular nucleus. Trends in Neurosciences 21, 28–32.CrossRefGoogle Scholar
Guillery, R.W., Feig, S.L. & Van Lieshout, D.P. (2001). Connections of higher order visual relays in the thalamus: A study of corticothalamic pathways in cats. The Journal of Comparative Neurology 438, 66–85.CrossRefGoogle ScholarPubMed
Guillery, R.W. & Sherman, S.M. (2002). Thalamic relay functions and their role in corticocortical communication: Generalizations from the visual system. Neuron 33, 163–175.CrossRefGoogle ScholarPubMed
Heath, C.J. & Jones, E.G. (1971). An experimental study of ascending connections from the posterior group of thalamic nuclei in the cat. The Journal of Comparative Neurology 141, 397–426.CrossRefGoogle ScholarPubMed
Jones, E.G. (1975). Some aspects of the organization of the thalamic reticular complex. The Journal of Comparative Neurology 162, 258–308.CrossRefGoogle ScholarPubMed
Joseph, J.P. & Giroud, P. (1986). Visuomotor properties of neurons in the anterior suprasylvian gyrus in the awake cat. Experimental Brain Research 62, 355–362.CrossRefGoogle ScholarPubMed
Kaitz, S.S. & Robertson, R.T. (1981). Thalamic connections with limbic cortex. II Corticothalamic projections. The Journal of Comparative Neurology 195, 527–545.CrossRefGoogle ScholarPubMed
Kalia, M. & Whitteridge, D. (1973). The visual areas in the splenial sulcus of the cat. The Journal of Physiology 232, 275–283.CrossRefGoogle ScholarPubMed
Kimura, A., Donishi, T., Okamoto, K. & Tamai, Y. (2005). Topography of projections from the primary and non-primary auditory cortical area to the medial geniculate body and thalamic reticular nucleus in the rat. Neuroscience 135, 1325–1342.CrossRefGoogle Scholar
Kimura, A., Imbe, H., Donishi, T. & Tamai, Y. (2007). Axonal projections of single auditory neurons in the thalamic reticular nucleus: Implications for tonotopy-related gating function and cross modulation. The European Journal of Neuroscience 26, 3524–3535 CrossRefGoogle Scholar
Kolmac, C.I. & Mitrofanis, J. (1998). Patterns of brainstem projection to the thalamic reticular nucleus. The Journal of Comparative Neurology 396, 531–543.3.0.CO;2-2>CrossRefGoogle Scholar
Lam, Y.-W., Nelson, C.S. & Sherman, S.M. (2006). Mapping of the functional interconnections between thalamic reticular neurons using photostimulation. Journal of Neurophysiology 96, 2593–2600.CrossRefGoogle ScholarPubMed
Lam, Y.-W. & Sherman, S.M. (2005). Mapping by laser photostimulation of connections between the thalamic reticular and ventral posterior lateral nuclei in the rat. Journal of Neurophysiology 94, 2472–2483.CrossRefGoogle ScholarPubMed
Lam, Y.-W. & Sherman, S.M. (2007). Different topography of the reticular thalamic inputs to first- and higher-order somatosensory thalamic relays revealed using photostimulation. Journal of Neurophysiology 98, 2093–2909.CrossRefGoogle ScholarPubMed
Lozsádi, D.A. (1994). Organization of cortical afferents to the rostral, limbic sector of the rat thalamic reticular nucleus. The Journal of Comparative Neurology 341, 520–533.CrossRefGoogle Scholar
Lozsádi, D.A., Gonzalez-Soriano, J. & Guillery, R.W. (1996). The course and termination of corticothalamic fibres arising in the visual cortex of the rat. The European Journal of Neuroscience 8, 2416–2427.CrossRefGoogle ScholarPubMed
McAlonan, K., Cavanaugh, J. & Wurtz, R.H. (2006). Attentional modulation of thalamic reticular neurons. The Journal of Neuroscience 26, 4444–4450.CrossRefGoogle ScholarPubMed
McAlonan, K., Cavanaugh, J. & Wurtz, R.H. (2008). Guarding the gateway to cortex with attention in visual thalamus. Nature 456, 391–394.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Bal, T. (1997). Sleep and arousal. Annual Review of Neuroscience 20, 185–215.CrossRefGoogle ScholarPubMed
Montero, V.M. (1997). C-fos induction in sensory pathway of rats exploring a novel complex environment: Shifts of active thalamic reticular sectors by predominant sensory cues. Neuroscience 76, 1069–1081.CrossRefGoogle ScholarPubMed
Montero, V.M. (1999). Amblyopia decreases activation of the corticogeniculate pathway and visual thalamic reticularis in attentive rats: A ‘focal attention’ hypothesis. Neuroscience 91, 805–817.CrossRefGoogle ScholarPubMed
Motles, E., Ely, Y. & Elazar, Z. (1980). Role of the pulvinar-lateral posterior nucleus complex in turning behaviour. Physiology and Behavior 25, 921–929.CrossRefGoogle Scholar
Murray, E.A., Davidson, M., Gaffan, D., Olton, D.S. & Suomi, S. (1989). Effects of fornix transection and cingulate cortical ablation on spatial memory in rhesus monkeys. Experimental Brain Research 74, 173–186.CrossRefGoogle ScholarPubMed
Niimi, K., Niimi, M., Matsuoka, H., Yanagihara, M. & Katayama, T. (1983). The laminar arrangement of limbic thalamocortical neurons in the lateropulvinar nuclei of the cat thalamus. Neuroscience Letters 38, 215–219.CrossRefGoogle ScholarPubMed
Norita, M., Mucke, L., Benedek, G., Albowitz, B., Katoh, Y. & Creutzfeldt, O.D. (1986). Connections of the anterior ectosylvian visual area (AEV). Experimental Brain Research 62, 225–240.CrossRefGoogle ScholarPubMed
Olson, C.R. & Lawler, K. (1987). Cortical and subcortical afferent connections of a posterior division of feline area 7 (area 7p). The Journal of Comparative Neurology 259, 13–30.CrossRefGoogle ScholarPubMed
Olson, C.R. & Musil, S.Y. (1992). Topographic organization of cortical and subcortical projections to posterior cingulate cortex in the cat: Evidence for somatic, ocular, and complex subregions. The Journal of Comparative Neurology 324, 237–260.CrossRefGoogle ScholarPubMed
Paré, D. & Smith, Y. (1996). Thalamic collaterals of corticostriatal axons: Their termination field and synaptic targets in cats. The Journal of Comparative Neurology 372, 551–567.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Pinault, D. (2004). The thalamic reticular nucleus: Structure, function and concept. Brain Research Reviews 46, 1–31.CrossRefGoogle ScholarPubMed
Pinault, D. & Deschênes, M. (1998). Projection and innervation patterns of individual thalamic reticular axons in the thalamus of the adult rat: A three dimensional, graphic, and morphometric analysis. The Journal of Comparative Neurology 391, 180–203.3.0.CO;2-Z>CrossRefGoogle Scholar
Raczkowski, D. & Rosenquist, A.C. (1983). Connection of the multiple visual cortical areas with the lateral posterior-pulvinar complex and adjacent thalamic nuclei in the cat. The Journal of Neuroscience 3, 1912–1942.CrossRefGoogle ScholarPubMed
Raeva, S. & Lukashev, A. (1993). Unit activity in human thalamic reticularis neurons II. Activity evoked by significant and non-significant verbal or sensory stimuli. Electroencephalography and Clinical Neurophysiology 86, 110–122.CrossRefGoogle ScholarPubMed
Reichova, I. & Sherman, S.M. (2004). Somatosensory corticothalamic projections: Distinguishing drivers from modulators. Journal of Neurophysiology 92, 2185–2197.CrossRefGoogle ScholarPubMed
Robertson, R.T. & Cunningham, T.J. (1981). Organization of corticothalamic projections from parietal cortex in cat. The Journal of Comparative Neurology 199, 569–585.CrossRefGoogle ScholarPubMed
Robertson, R.T. & Kaitz, S.S. (1981). Thalamic connections with limbic cortex. I. Thalamocortical projections. The Journal of Comparative Neurology 195, 501–525.CrossRefGoogle ScholarPubMed
Robinson, D.L. & Petersen, S.E. (1992). The pulvinar and visual salience. Trends in Neurosciences 15, 127–132.CrossRefGoogle ScholarPubMed
Robson, J.A. (1983). The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat. The Journal of Comparative Neurology 216, 89–103.CrossRefGoogle Scholar
Rockland, K.S. (1996). Two types of corticopulvinar terminations: Round (type 2) and elongate (type 1). The Journal of Comparative Neurology 368, 57–87.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Rodrigo-Angulo, M.L. & Reinoso-Suárez, F. (1988). Connections to the lateral posterior-pulvinar complex from the reticular and ventral lateral geniculate thalamic nuclei: A topographical study in the cat. Neuroscience 26, 449–459.CrossRefGoogle Scholar
Rodrigo-Angulo, M.L. & Reinoso-Suarez, F. (1995). Afferent connections of the lateralis medialis thalamic nucleus in the cat. Brain Research Bulletin 38, 53–67.CrossRefGoogle ScholarPubMed
Room, P., Russchen, F.T., Groenewegen, H.J. & Lohmann, H. (1985). Efferent connections of the prelimbic (Area 32) and the infralimbic (Area 25) cortices: An anterograde tracing study in the cat. The Journal of Comparative Neurology 242, 40–55.CrossRefGoogle ScholarPubMed
Rosenquist, A.C. (1985). Connections of visual cortex in the cat. In Cerebral Cortex, ed. Peters, A. & Jones, E.G., pp. 81–117. Plenum Publishing Corporation, New York.Google Scholar
Sakoda, T., Kimura, A., Donishi, T., Kitano, H. & Tamai, Y. (2004). Presence and connections of auditory neurons in the rostrodorsal and rostrolateral parts of the thalamic reticular nucleus. Acta Oto-laryngologica. Supplementum 553, 36–42.CrossRefGoogle Scholar
Scannell, J.W., Burns, G.A.P.C., Hilgetag, C.C., O’Neil, M.A. & Young, M.P. (1999). The connectional organization of the cortico-thalamic system of the cat. Cerebral Cortex 9, 277–299.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Guillery, R.W. (1998). On the actions that one nerve cell can have on another: Distinguishing “drivers” from “modulators”. Proceedings of the National Academy of Sciences of the United States of America 95, 7121–7126.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Koch, C. (1986). The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Experimental Brain Research 63, 1–20.CrossRefGoogle ScholarPubMed
Shipp, S. (2004). The brain circuitry of attention. Trends in Cognitive Sciences 8, 223–230.CrossRefGoogle ScholarPubMed
Shosaku, A. & Sumitomo, I. (1983). Auditory neurons in the rat thalamic reticular nucleus. Experimental Brain Research 49, 432–442.CrossRefGoogle ScholarPubMed
Shumikhina, S.I. & Maiskii, V.A. (1991). Relationship between thalamic projections and different areas of the parietal association cortex in cats. Neurophysiology 23, 100–106.CrossRefGoogle Scholar
Steriade, M., Jones, E.G. & McCormick, D.A. (1997). Thalamus, Vol. 1. Amsterdam, The Netherlands: Elsevier.Google Scholar
Steriade, M. & Llinas, R.R. (1988). The functional states of the thalamus and the associated neuronal interplay. Physiological Reviews 68, 649–742.CrossRefGoogle ScholarPubMed
Steriade, M., Parent, A. & Hada, J. (1984). Thalamic projections of nucleus reticularis thalami of cat: A study using retrograde transport of horseradish peroxidase and fluorescent tracers. The Journal of Comparative Neurology 229, 531–547.CrossRefGoogle Scholar
Sugitani, M. (1979). Electrophysiological and sensory properties of the thalamic reticular neurones related to somatic sensation in rats. The Journal of Physiology 290, 79–95.CrossRefGoogle ScholarPubMed
Sutherland, R.J., Whishaw, I.Q. & Kolb, B. (1988). Contributions of cingulate cortex to two forms of spatial learning and memory. The Journal of Neuroscience 8, 1863–1872.CrossRefGoogle ScholarPubMed
Symonds, L.L. & Rosenquist, A.C. (1984). Corticocortical connections among visual areas in the cat. The Journal of Comparative Neurology 229, 1–38.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. The Journal of Comparative Neurology 177, 213–236.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1981). Multiple cortical visual areas. Visual field topography in the cat. In Cortical Sensory Organization, ed. Woolsey, C.N., pp. 1–31. New Jersey, NJ: Humana Press.Google Scholar
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 and 19 in the cat. The Journal of Comparative Neurology 185, 657–678.CrossRefGoogle Scholar
Ventre, J. (1985). Cortical control of oculomotor functions. I Optokinetic nystagmus. Behavioural Brain Research 15, 211–226.CrossRefGoogle ScholarPubMed
Yen, C.T., Conley, M., Hendry, S.H.C. & Jones, E.G. (1985). The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat. The Journal of Neuroscience 5, 2254–2268.CrossRefGoogle ScholarPubMed
Yingling, C.D. & Skinner, J.E. (1975). Regulation of unit activity in nucleus reticularis thalami by the mesencephalic reticular formation and the frontal granular cortex. Electroencephalography and Clinical Neurophysiology 39, 635–642.CrossRefGoogle ScholarPubMed
Zhang, L. & Jones, E.G. (2003). Corticothalamic inhibition in the thalamic reticular nucleus. Journal of Neurophysiology 91, 759–766.CrossRefGoogle ScholarPubMed
Zikopoulos, B. & Barbas, H. (2006). Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. The Journal of Neuroscience 26, 7348–7361.CrossRefGoogle Scholar