Skip to main content
Log in

Organization of feedback and feedforward projections of the barrel cortex: a PHA-L study in the mouse

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

In order to analyze the organization of the efferent projections of single barrel columns (BC, i.e. a barrel in layer IV of parietal cortex plus the cortical tissue above and below it), we made small iontophoretic injections of the anterograde tracer Phaseolus vulgaris leucoagglutinin in the barrel cortex of 20 adult mice. On the basis of reconstructions of the sites of terminal labelling, the brain regions receiving projections from the barrel cortex could be identified and classified in five groups. Each group is characterized by the topography of the distribution of efferents arising from a single BC. The projections to the trigeminal sensory complex are point to point: i.e. one BC projects only to the site of termination of the primary sensory neurons innervating the corresponding whisker follicle. In the ventrobasal thalamic nucleus BC projections are not restricted to the corresponding barreloid; instead they contact parts of barreloids belonging to one arc. In the reticular and posterior thalamic nuclei the projections from a row of BC's converge to a collective termination site, whereas in the superior colliculus the projections from an arc of BC's converge to a common termination site. There is a complete overlap of BC projections in restricted zones within SII, motor cortex, perirhinal cortex, contralateral barrelfield, caudoputamen and pons. The organization of the efferents from the barrel cortex demonstrates a contrast between feedback and feedforward projections from this important area of neocortex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akers RM, Killackey HP (1978) Organization, of corticocortical connections in the parietal cortex of the rat. J Comp Neurol 181: 513–538

    Google Scholar 

  • Arvidsson J (1982) Somatotopic organization of vibrissae afferents in the trigeminal sensory nuclei of the rat studied by transganglionic transport of HRP. J Comp Neurol 211: 84–92

    Google Scholar 

  • Bates CA, Killackey HP (1985) The organization of the neonatal rat's brainstem trigeminal complex and its role in the formation of central trigeminal patterns. J Comp Neurol 240: 265–287

    Google Scholar 

  • Belford GR, Killackey HP (1979) Vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 183: 305–322

    Google Scholar 

  • Bruce LL, McHaffie JG, Stein BE (1987) The organization of trigeminotectal and trigeminothalamic neurons in rodents: a double-labelling study with fluorescent dyes. J Comp Neurol 262: 315–330

    Google Scholar 

  • Cajal SR (1909) Histologie du système nerveux de l'homme et des vertébrés, Tome 1. Maloine, Paris

    Google Scholar 

  • Cajal SR (1911) Histologie du système nerveux de l'homme et des vertébrés, Tome II. Maloine, Paris

    Google Scholar 

  • Carvell GE, Simons DJ (1986) Somatotopic organization of the second somatosensory area (SII) in the cerebral cortex of the mouse. Somatosens Res 3: 213–237

    Google Scholar 

  • Caviness VS Jr (1975) Architectonic map of neocortex of the normal mouse. J Comp Neurol 164: 247–264

    Google Scholar 

  • Cechetto DF, Saper CB (1987) Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J Comp Neurol 262: 27–45

    Google Scholar 

  • Danforth CH (1925) Hair in its relation to questions of homology and phylogeny. Am J Anat 36: 47–68

    Google Scholar 

  • Deacon TW, Eichenbaum H, Rosenberg P, Eckmann KW (1983) Afferent connections of the perirhinal cortex in the rat. J Comp Neurol 220: 168–190

    Google Scholar 

  • Dörfl J (1985) The innervation of the mystacial region of the white mouse. A topographical study. J Anat (Lond) 142: 173–184

    Google Scholar 

  • Donoghue JP, Kitai ST (1981) A collateral pathway to the neostriatum from corticofugal neurons of the rat sensorymotor-cortex: an intracellular HRP study. J Comp Neurol 201: 1–13

    Google Scholar 

  • Dräger UC, Hubel DH (1976) Topography of visual and somatosensory projections to mouse superior colliculus. J Neurophysiol 39: 91–101

    Google Scholar 

  • Durham D, Woolsey TA (1984) Effects of neonatal whisker lesions on mouse central trigeminal pathways. J Comp Neurol 223: 424–447

    Google Scholar 

  • Erzurumlu RS, Killackey HP (1980) Diencephalic projections of the subnucleus interpolaris of the brainstem trigeminal complex in the rat. Neuroscience 5: 1891–1901

    Google Scholar 

  • Faull RLM, Nauta WJH, Domesick VB (1986) The visual corticostriato-nigral pathway in the rat. Neuroscience 19: 1119–1132

    Google Scholar 

  • Fekete DM, Rouiller EM, Liberman MC, Ryogo DK (1984) The central projections of intracellularly labeled auditory nerve fibers in cats. J Comp Neurol 229: 432–450

    Google Scholar 

  • Forel A (1887) Einige hirnanatomische Betrachtungen und Ergebnisse. Arch Psychiat Nervenkr 18: 162–198

    Google Scholar 

  • Gerfen CR (1984) The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311: 461–464

    CAS  PubMed  Google Scholar 

  • Gerfen CR, Sawchenko PE (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 290: 219–238

    Google Scholar 

  • Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66: 23–28

    Google Scholar 

  • Hayashi H (1980) Distributions of vibrissae afferent fiber collaterals in the trigeminal nuclei as revealed by intra-axonal injection of horseradish peroxidase. Brain Res 183: 442–446

    Google Scholar 

  • Herkenham M, Pert CB (1981) Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 291: 415–418

    Google Scholar 

  • Hoogland PV, Welker E, Van der Loos H (1987) Organization of the projections from barrel cortex to thalamus in mice studied with Phaseolus vulgaris-leucoagglutinin and HRP. Exp Brain Res 68: 73–87

    Google Scholar 

  • Hoogland PV, Welker E, Van der Loos H, Wouterlood FG (1988) The organization and structure of the thalamic afferents from the barrel cortex in the mouse: a PHA-L study. In: Bentivoglio M, Spreafico R (eds) Cellular thalamic mechanisms. Elsevier, Amsterdam 151–162

    Google Scholar 

  • Jacquin MF, Barcia M, Golden J, Rhoades RW (1987) Functionally identified local circuit neurons in rat trigeminal subnucleus interpolaris. Soc Neurosci Abstr 13: 523

    Google Scholar 

  • Jacquin MF, Renehan WE, Mooney RD, Rhoades RW (1986a) Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents. J Neurophysiol 55: 1153–1186

    Google Scholar 

  • Jacquin MF, Woerner D, Szczepanik M, Riecker V, Mooney RD, Rhoades RW (1986b) Structure-function relationships in rat brainstem subnucleus interpolaris. I. Vibrissa primary afferents. J Comp Neurol 243: 266–279

    Google Scholar 

  • Jones EG, Coulter JD, Burton H, Porter R (1977) Cells of origin and terminal distribution of corticostriatal fibers arising in the sensory-motor cortex of monkeys. J Comp Neurol 173: 53–80

    Google Scholar 

  • Kelley AE, Domesick VB, Nauta WJH (1982) The amygdalostriatal projection in the rat — an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7: 615–630

    Google Scholar 

  • Killackey HP, Erzurumlu RS (1981) Trigeminal projections to the superior colliculus of the rat. J Comp Neurol 201: 221–242

    Google Scholar 

  • Knudsen EI, Du Lac S, Esterly SD (1987) Computational maps in the brain. Ann Rev Neurosci 10: 41–65

    Google Scholar 

  • Kosinski R, Neafsey EJ, Castro AJ (1986) A comparative topographical analysis of dorsal column nuclear and cerebral cortical projections to the basilar pontine gray in rats. J Comp Neurol 244: 163–173

    Google Scholar 

  • Ledoux MS, Whitworth RH Jr, Gould HJ III (1987) Interhemispheric connections of the somatosensory cortex in the rabbit. J Comp Neurol 258: 145–157

    Google Scholar 

  • Lin C-S, Lu SM, Yamawaki RM (1987) Laminar and synaptic organization of terminals from the ventrobasal and posterior thalamic nuclei in rat barrel cortex. Soc Neurosci Abstr 13: 248

    Google Scholar 

  • Malach R, Graybiel AM (1986) Mosaic architecture of the somatic sensory-recipient sector of the cat's striatum. J Neurosci 6: 3436–3458

    Google Scholar 

  • McGeorge AJ, Faull RLM (1987) The organization and collateralization of corticostriate neurones in the motor and sensory cortex of the rat brain. Brain Res 423: 318–324

    Google Scholar 

  • Melzer P, Van der Loos H, Dörfl J, Welker E, Robert P, Emery D, Berrini J-C (1985) A magnetic device to stimulate whiskers of freely moving or restrained small rodents: its application in a deoxyglucose study. Brain Res 348: 229–240

    Google Scholar 

  • Melzer P, Welker E, Dörfl J, Van der Loos H (1986) Development of order in the whisker-to-barrel pathway of the mouse: neuronal metabolic responses to whisker stimulation. Soc Neurosci Abstr 12: 953

    Google Scholar 

  • Mihailoff GA, Watt CB, Burne RA (1981) Evidence suggesting that both the corticopontine and cerebellopontine systems are each composed of two separate neuronal populations: an electron microscopic and horseradish peroxidase study in rat. J Comp Neurol 195: 221–242

    Google Scholar 

  • Mihailoff GA, Lee H, Watt CB, Yates R (1985) Projections to the basilar pontine nuclei from face sensory and motor regions of the cerebral cortex in the rat. J Comp Neurol 237: 251–263

    Google Scholar 

  • Nussbaumer J-C, Van der Loos H (1985) An electrophysiological and anatomical study of projections to the mouse cortical barrelfield and its surroundings. J Neurophysiol 53: 686–698

    Google Scholar 

  • Olavarria J, Van Sluyters RC, Killackey HP (1984) Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex. Brain Res 291: 364–368

    Google Scholar 

  • Perentes E (1979) Analyse du cortex somatosensoriel (PMBSF) de la souris: ultrastructure des bords des tonneaux et des septa. Thesis. Université de Lausanne, Faculté de Médecine.

  • Pidoux B, Verley R (1979) Projection on the cortical somatic I barrel subfield from ipsilateral vibrissae in adult rodents. Electroenceph Clin Neurophysiol 46: 715–726

    Google Scholar 

  • Rhoades RW, Belford GR, Killackey HP (1987) Receptive-field properties of rat ventral posterior medial neurons before and after selective kainic acid lesions of the trigeminal brain stem complex. J Neurophysiol 57: 1577–1600

    Google Scholar 

  • Rossner KL, Jacquin MF (1982) Receptive field synthesis in trigeminal subnucleus interpolaris. I. Cortical inputs. Soc Neurosci Abstr 13: 523

    Google Scholar 

  • Slotnick BM, Leonard CM (1975) A stereotaxic atlas of the albino mouse forebrain. U.S. Department of Health, Education, and Welfare, Rockville, Maryland

    Google Scholar 

  • Smith RL (1973) The ascending fiber projections from the principal sensory trigeminal nucleus in the rat. J Comp Neurol 148: 423–446

    Google Scholar 

  • Steindler DA (1985) Trigeminocerebellar, trigeminotectal, and trigeminothalamic projections: a double retrograde axonal tracing study in the mouse. J Comp Neurol 237: 155–175

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry. John Wiley and Sons, New York

    Google Scholar 

  • Swenson RS, Kosinski RJ, Castro AJ (1984) Topography of spinal, dorsal column nuclear, and spinal trigeminal projections to the pontine gray in rats. J Comp Neurol 222: 301–311

    Google Scholar 

  • Triller A, Korn H (1981) Morphologically distinct classes of inhibitory synapses arise from the same neurons: ultrastructural identification from crossed vestibular interneurons intracellularly stained with HRP. J Comp Neurol 203: 131–155

    Google Scholar 

  • Tolberg DL, Dunn RC Jr, Vogler GA (1984) The postnatal development of corticotrigeminal projections in the cat. J Comp Neurol 228: 478–490

    Google Scholar 

  • Valverde F (1966) The pyramidal tract in rodents. A study of its relations with the posterior column nuclei, dorsolateral reticular formation of the medulla oblongata and cervical spinal cord. Z Zellforsch 71: 297–363

    Google Scholar 

  • Van der Loos H (1976) Neuronal circuitry and its development. Progr Brain Res 45: 259–278

    Google Scholar 

  • Van der Loos H, Welker E, Dörfl J, Rumo G (1986) Selective breeding for variations in patterns of mystacial vibrissae of mice; bilaterally symmetrical strains derived from ICR-stock. J Hered 77: 66–82

    Google Scholar 

  • Waite PME, Cragg BG (1982) The peripheral and central changes resulting from cutting of crushing the afferent nerve supply to the whiskers. Proc R Soc Lond 214: 191–211

    Google Scholar 

  • Walker AE (1934) The thalamic projection to the central gyri in Macacus rhesus. J Comp Neurol 60: 161–184

    Google Scholar 

  • Walker AE (1938) The thalamus of the chimpanzee. IV. Thalamic projections to the cerebral cortex. J Anat (Lond) 73: 37–93

    Google Scholar 

  • Wallace MN, Welker E (1985) Spatial relationship of histochemically demonstrable patches in the intermediate layers of the superior colliculus. Neurosci Lett Suppl 22: S314

    Google Scholar 

  • Wallace MN (1986) Spatial relationship of histochemically demonstrable patches in the mouse superior colliculus. Exp Brain Res 62: 241–249

    Google Scholar 

  • Wallace MN (1987) Histochemical demonstration of sensory maps in the rat and mouse cerebral cortex. Brain Res 418: 178–182

    Google Scholar 

  • Welker C (1976) Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol 166: 173–189

    Google Scholar 

  • Welker E, Hoogland PV, Van der Loos H (1987) The fine grained organization of the projections from the barrel cortex of the mouse: a Phaseolus vulgaris leucoagglutinin (PHA-L) study. Soc Neurosci Abstr 13: 247

    Google Scholar 

  • White EL, DeAmicis RA (1977) Afferent and efferent projections of the region in mouse SmI cortex which contains the posteromedial barrel subfield. J Comp Neurol 175: 455–482

    Google Scholar 

  • Wiesendanger R, Wiesendanger M (1982) The corticopontine system in the rat. II. The projection pattern. J Comp Neurol 208: 227–238

    Google Scholar 

  • Wilson CJ (1987) Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J Comp Neurol 263: 567–580

    Google Scholar 

  • Wise SP, Jones EG (1976) The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. J Comp Neurol 168: 313–344

    Google Scholar 

  • Wise SP, Jones EG (1977a) Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J Comp Neurol 175: 129–158

    Google Scholar 

  • Wise SP, Jones EG (1977b) Somatic and columnar organization in the cortico-tectal projection of the rat somatic sensory cortex. Brain Res 133: 223–235

    Google Scholar 

  • Wise SP, Murray EA, Coulter JD (1979) Somatotopic organization of corticospinal and corticotrigeminal neurons in the rat. Neuroscience 4: 65–78

    Google Scholar 

  • Wong-Riley M (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171: 11–28

    Google Scholar 

  • Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex: the description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17: 205–242

    Google Scholar 

  • Woolston DC, La Londe JR, Gibson JM (1983) Corticofugal influences in the rat on responses of neurons in the trigeminal nucleus interpolaris to mechanical stimulation. Neurosci Lett 36: 43–48

    Google Scholar 

  • Yorke CH Jr, Caviness VS Jr (1975) Interhemispheric neocortical connections of the corpus callosum in the normal mouse: a study based on anterograde methods. J Comp Neurol 164: 233–246

    Google Scholar 

  • Zilles K (1985) The cortex of the rat: a stereotaxic atlas. Springer, Berlin

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Welker, E., Hoogland, P.V. & Van der Loos, H. Organization of feedback and feedforward projections of the barrel cortex: a PHA-L study in the mouse. Exp Brain Res 73, 411–435 (1988). https://doi.org/10.1007/BF00248234

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00248234

Key words

Navigation