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Polysynaptic pathways from the vestibular nuclei to the lateral mammillary nucleus of the rat: substrates for vestibular input to head direction cells

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Abstract

The activity of some neurons in the lateral mammillary nucleus (LMN) of the rat corresponds with the animal’s current head direction (HD). HD cells have been studied extensively but the circuitry responsible for the generation and maintenance of the HD signal has not been established. The present study tested the hypothesis that a polysynaptic pathway connects the vestibular nuclei with the LMN via one or more relay nuclei. This circuitry could provide a substrate for the integration of sensory input necessary for HD cell activity. This hypothesis is based upon the prior demonstration that labyrinthectomy abolishes HD selectivity in thalamic neurons. Viral transneuronal tracing with pseudorabies virus (PRV) was used to test this hypothesis. We injected recombinants of PRV into the LMN and surrounding nuclei of adult male rats and defined the patterns of retrograde transneuronal infection at survival intervals of 60 and 72 h. Infected medial vestibular neurons (MVN) were only observed at the longest postinoculation interval in animals in which the injection site was localized largely to the LMN. Robust infection of the dorsal tegmental nucleus (DTN) and nucleus prepositus hypoglossi (PH) in these cases, but not in controls, at both survival intervals identified these nuclei as potential relays of vestibular input to the LMN. These data are consistent with the conclusion that vestibular information that contributes to the LMN HD cell activity is relayed to this caudal hypothalamic cell group via a polysynaptic brainstem circuit.

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References

  • Allen GV, Hopkins DA (1988) Mammillary body in the rat: a cytoarchitectonic, Golgi, and ultrastructural study. J Comp Neurol 275:39–64

    CAS  PubMed  Google Scholar 

  • Allen GV, Hopkins DA (1989) Mammillary body in the rat: topography and synaptology of projections from the subicular complex, prefrontal cortex and midbrain tegmentum. J Comp Neurol 286:311–336

    CAS  PubMed  Google Scholar 

  • Alonso A, Kohler C (1984) A study of reciprocal connections between the septum and entorhinal area using anterograde and retrograde axonal transport methods in the rat brain. J Comp Neurol 225:327–343

    CAS  PubMed  Google Scholar 

  • Baker R (1977) The nucleus prepositus hypoglossi. In: Brooks BA, Bajandas FJ (eds) Eye movements. Plenum, New York, pp 145–178

  • Balaban CD, McGee DM, Zhou J, Scudder CA (2002) Responses of primate caudal parabrachial nucleus and Kolliker-fuse nucleus neurons to whole body rotation. J Neurophysiol 88:3175–3193

    PubMed  Google Scholar 

  • Bassett JP, Taube JS (2001) Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J Neurosci 21:5740–5751

    CAS  PubMed  Google Scholar 

  • Beitz AJ, Clements HR, Mullett MA, Ecklund LJ (1986) Differential origin of brainstem serotonergic projections to the midbrain periaqueductal gray and superior colliculus of the rat. J Comp Neurol 250:498–509

    CAS  PubMed  Google Scholar 

  • Belknap DB, McCrea RA (1988) Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey. J Comp Neurol 268:12–38

    Google Scholar 

  • Billig I, Foris JM, Enquist LW, Card JP, Yates BJ (2000) Definition of neuronal circuitry controlling the activity of phrenic and abdominal motoneurons in the ferret using recombinant strains of pseudorabies virus. J Neurosci 20:7446–7454

    CAS  PubMed  Google Scholar 

  • Blair HT, Cho J, Sharp PE (1998) Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study. Neuron 21:1387–1397

    Article  CAS  PubMed  Google Scholar 

  • Blair HT, Cho J, Sharp PE (1999) The anterior thalamic head-direction signal is abolished by bilateral but not unilateral lesions of the lateral mammillary nucleus. J Neurosci 19:6673–3383

    CAS  PubMed  Google Scholar 

  • Brodal A (1983) The perihypoglossal nuclei in the macaque monkey and the chimpanzee. J Comp Neurol 218:257–269

    CAS  PubMed  Google Scholar 

  • Brown JE, Yates BJ, Taube JS (2002) Does the vestibular system contribute to head direction cell activity in the rat? Physiol Behav 77:743–748

    Article  CAS  PubMed  Google Scholar 

  • Cannon SC, Robinson DA (1987) Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol 57:1383–1409

    CAS  PubMed  Google Scholar 

  • Card JP (2001) Pseudorabies virus neuroinvasiveness: a window into the functional organization of the brain. Adv Virus Res 56:39–71

    Article  CAS  PubMed  Google Scholar 

  • Card JP, Enquist LW, Moore RY (1999) Neuroinvasiveness of pseudorabies virus injected intracerebrally is dependent on viral concentration and terminal field density. J Comp Neurol 407:438–452

    Article  CAS  PubMed  Google Scholar 

  • Card JP, Rinaman L, Schwaber JS, Miselis RR, Whealy ME, Robbins AK, Enquist LW (1990) Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J Neurosci 10:1974–1994

    CAS  PubMed  Google Scholar 

  • Chen LL, Lin LH, Barnes CA, McNaughton BL (1994) Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp Brain Res 101:24–34

    CAS  PubMed  Google Scholar 

  • Cornwall J, Cooper JD, Phillipson OT (1990) Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat. Brain Res Bull 25:271–284

    Article  CAS  PubMed  Google Scholar 

  • Ennis M, Aston-Jones G (1989) Potent inhibitory input to locus coeruleus from the nucleus prepositus hypoglossi. Brain Res Bull 22:793–803

    Article  CAS  PubMed  Google Scholar 

  • Gonzalo-Ruiz A, Sanz-Anquela JM, Spencer RF (1993) Immunohistochemical localization of GABA in the mammillary complex of the rat. Neuroscience 54:143–156

    Google Scholar 

  • Gonzalo-Ruiz A, Morte L, Flecha JM, Sanz JM (1999) Neurotransmitter characteristic of neurons projecting to the supramammillary nucleus of the rat. Anat Embryol 200:377–392

    Article  CAS  PubMed  Google Scholar 

  • Goto Y, Swanson LW, Canteras NS (2001) Connections of the nucleus incertus. J Comp Neurol 438:86–122

    Article  CAS  PubMed  Google Scholar 

  • Groenewegen HJ, Van Dijk CA (1984) Efferent connections of the dorsal tegmental region in the rat, studied by means of anterograde transport of the lectin Phaseolus vulgaris-leucoagglutinin (PHA-L). Brain Res 304:367–371

    Article  CAS  PubMed  Google Scholar 

  • Hayakawa T, Ito H, Zyo K (1993) Neuroanatomical study of afferent projections to the supramammillary nucleus of the rat. Anat Embryol (Berl) 188:139–148

    Google Scholar 

  • Hayakawa T, Ito H, Zyo K (1994) Fine structure of the supramammillary nucleus of the rat: analysis of the ultrastructural character of dopaminergic neurons. J Comp Neurol 346:127–136

    CAS  PubMed  Google Scholar 

  • Hayakawa T, Zyo K (1985) Afferent connections of Gudden’s tegmental nuclei in the rabbit. J Comp Neurol 235:169–181

    CAS  PubMed  Google Scholar 

  • Hayakawa T, Zyo K (1990) Fine structure of the lateral mammillary projection of the dorsal tegmental nucleus of Gudden in the rat. J Comp Neurol 298:224–236

    CAS  PubMed  Google Scholar 

  • Hayakawa T, Zyo K (1991) Quantitative and ultrastructural study of ascending projections to the medial mammillary nucleus in the rat. Anat Embryol (Berl) 184:611–622

    Google Scholar 

  • Hayakawa T, Zyo K (1992) Ultrastructural study of ascending projections to the lateral mammillary nucleus of the rat. Anat Embryol (Berl) 185:547–557

    Google Scholar 

  • Henn V, Young LR, Finley C (1974) Vestibular nucleus units in alert monkeys are also influenced by moving visual fields. Brain Res 71:144–149

    Article  CAS  PubMed  Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase techniques. Am J Clin Pathol 75:816–821

    CAS  PubMed  Google Scholar 

  • Iwasaki H, Kani K, Maeda T (1999) Neural connections of the pontine reticular formation, which connects reciprocally with the nucleus prepositus hypoglossi in the rat. Neuroscience 93:195–208

    Google Scholar 

  • Jasmin L, Burkey AR, Card JP, Basbaum A (1997) Transneuronal labeling of a nociceptive pathway, the spinal-(trigemino-)parabrachio-amygdalaoid, in the rat. J Neurosci 17:3751–3765

    CAS  PubMed  Google Scholar 

  • Kim SY, Frohardt RJ, Taube JS (2003) Head direction cells shift reference frames in the vertical plane. Program No. 519.19, 2003 Abstract viewer/itinerary planner. Society for Neuroscience, Washington, DC

  • Korp BG, Blanks RHI, Torigoe Y (1989) Projections of the nucleus of the optic tract to the nucleus reticularis tegmenti pontis and the prepositus hypoglossi nucleus in the pigmented rat as demonstrated by anterograde and retrograde transport methods. Vis Neurosci 2:275–286

    CAS  PubMed  Google Scholar 

  • Lannou J, Cazin L, Precht W, Le Taillanter M (1984) Responses of prepositus hypoglossi neurons to optokinetic and vestibular stimulations in the rat. Brain Res 301:39–45

    Article  CAS  PubMed  Google Scholar 

  • Liu R, Chang L, Wickern G (1984) The dorsal tegmental nucleus: an axoplasmic transport study. Brains Res 310:123–132

    Article  CAS  Google Scholar 

  • Luppi PH, Aston-Jones G, Akaoka H, Chouvet G, Jouvet M (1995) Afferent projections to the rat locus coeruleus demonstrated by retrograde and anterograde tracing with cholera-toxin b subunit and phaseolus vulgaris leucoagglutinin. Neuroscience 65:119–160

    Google Scholar 

  • Marchand ER, Riley JN, Moore RY (1980) Interpeduncular nucleus afferents in the rat. Brain Res 193:339–352

    Article  CAS  PubMed  Google Scholar 

  • Marchand JE, Hagino (1983) Afferents to the periaqueductal gray in the rat. A horseradish peroxidase study. Neuroscience 9:95–106

    Google Scholar 

  • Marchand CF, Schwab ME (1986) Binding, uptake and retrograde axonal transport of herpes virus suis in sympathetic neurons. Brain Res 383:262–270

    Article  CAS  PubMed  Google Scholar 

  • Matesz C, Bacskai T, Nagy E, Halasi G, Kulik A (2002) Efferent connections of the vestibular nuclei in the rat: a neuromorphological study using PHA-L. Brain Res Bull 57:313–315

    Article  PubMed  Google Scholar 

  • McCrea RA (1988) Neuroanatomy of the oculomotor system. The nucleus prepositus. Rev Oculomot Res 2:203–223.

    CAS  PubMed  Google Scholar 

  • McCrea RA, Baker R (1985) Anatomical connections of the nucleus prepositus in the cat. J Comp Neurol 237:377–407

    CAS  PubMed  Google Scholar 

  • McLean IW, Nakane PK (1974) Periodate-lysine-paraformaldehyde fixative. A new fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077–1083

    CAS  PubMed  Google Scholar 

  • Mizumori SJY, Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal thalamic nucleus of rats. J Neurosci 13:4015–4028

    CAS  PubMed  Google Scholar 

  • Muller RU, Ranck JB, Taube JS (1996) Head direction cells: properties and functional significance. Curr Opin Neurobiol 6:196–206

    Google Scholar 

  • Olucha-Bordonau FE, Teruel V, Barcia-Gonzalez J, Ruiz-Torner A, Valverde-Navarro AA, Martinez-Soriano F (2003) Cytoarchitecture and efferent projections of the nucleus incertus of the rat. J Comp Neurol 464:62–97

    Article  PubMed  Google Scholar 

  • Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, San Diego

  • Pickard GE, Smeraski CA, Tomlinson CC, Banfield BW, Kaufman J, Wilcox CL, Enquist LW, Sollars PJ (2002) Intravitreal injection of the attenuated pseudorabies virus PRV Bartha results in infection of the hamster suprachiasmatic nucleus only by retrograde transsynaptic transport via autonomic circuits. J Neurosci 22:2701–2710

    CAS  PubMed  Google Scholar 

  • Risold PY, Swanson LW (1996) Structural evidence for functional domains in the rat hippocampus. Science 272:1484–1486

    CAS  PubMed  Google Scholar 

  • Risold PY, Swanson LW (1997) Connections of the rat lateral septal complex. Brain Res Brain Res Rev 24:91–113

    Article  CAS  PubMed  Google Scholar 

  • Ruggiero DA, Giuliano R, Anwar M, Stornetta R, Reis DJ (1990) Anatomical substrates of cholinergic-autonomic regulation in the rat. J Comp Neurol 292:1–53

    CAS  PubMed  Google Scholar 

  • Schor RH, Steinbacher BC, Yates BJ (1998). Horizontal linear and angular responses of neurons in the medial vestibular nucleus of the decerebrate cat. J Vestib Res 8:107–116

    Article  CAS  PubMed  Google Scholar 

  • Sharp PE, Blair HT, Cho J (2001a) The anatomical and computational basis of the rat head-direction signal. Trends Neurosci 24:289–294

    Article  CAS  PubMed  Google Scholar 

  • Sharp PE, Tinkelman A, Cho J (2001b) Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of Gudden in the rat: implications for path integration in the head direction cell circuit. Behav Neurosci 115:571–588

    Article  CAS  PubMed  Google Scholar 

  • Shibata H (1987) Ascending projections to the mammillary nuclei in the rat: a study using retrograde and anterograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. J Comp Neurol 264:205–215

    CAS  PubMed  Google Scholar 

  • Shibata H, Suzuki T, Matsushita M (1986) Afferent projections to the interpeduncular nucleus in the rat, as studied by retrograde and anterograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. J Comp Neurol 248:272–284

    CAS  PubMed  Google Scholar 

  • Stackman RW, Taube JS (1997) Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17:4349–4358

    CAS  PubMed  Google Scholar 

  • Stackman RW, Taube JS (1998) Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J Neurosci 18:9020–9037

    CAS  PubMed  Google Scholar 

  • Stackman RW, Tullman ML, Taube JS (2000) Maintenance of rat head direction cell firing during locomotion in the vertical plane. J Neurophysiol 83:393–405

    CAS  PubMed  Google Scholar 

  • Swanson LW (1998) Brain maps: structure of the rat brain. Elsevier, Amsterdam

    Google Scholar 

  • Takeuchi Y, Allen GV, Hopkins DA (1985) Transnuclear transport and axon collateral projections of the mamillary nuclei in the rat. Brain Res Bull 14:453–468

    Article  CAS  PubMed  Google Scholar 

  • Taube JS (1995) Head-direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86

    Google Scholar 

  • Taube JS (1998) Head direction cells and the neurophysiological basis for a sense of direction. Prog Neurobiol 55:225–256

    Article  CAS  PubMed  Google Scholar 

  • Taube JS, Muller RU, Ranck JB (1990) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10:420–435

    Google Scholar 

  • Vahlne A, Svennerholm B, Sandber M, Hamberger A, Lycke E (1980) Differences in attachment between herpes simplex type 1 and type 2 viruses to neurons and glial cells. Infect Immun 28:675–680

    CAS  PubMed  Google Scholar 

  • Watson RE, Wiegand ST, Clough RW, Hoffman GE (1986) Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7:155–159

    Article  CAS  Google Scholar 

  • Weiner SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigational task. J Neurosci 13:3802–3817

    Google Scholar 

  • Wirtshafter D, Stratford TR (1993) Evidence for GABAergic projections from the tegmental nuclei of Gudden to the mammillary body in the rat. Brain Res 630:188–194

    Article  CAS  PubMed  Google Scholar 

  • Zelman FP, Behbehani MM, Beckstead RM (1984) Ascending and descending projections from nucleus reticularis magnocellularis and nucleus reticularis gigantocellularis: an autoradiographic and horseradish peroxidase study in the rat. Brain Res 292:207–220

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Lucy Cotter, Jen-Shew Yen, Rebecca Edelmeyer, Katie Wilkinson, Andrew Maurer and Brian Sadacca for valuable technical assistance. This work was supported by grant R21-DC006049 from the National Institutes of Health.

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Correspondence to B. J. Yates.

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Brown, J.E., Card, J.P. & Yates, B.J. Polysynaptic pathways from the vestibular nuclei to the lateral mammillary nucleus of the rat: substrates for vestibular input to head direction cells. Exp Brain Res 161, 47–61 (2005). https://doi.org/10.1007/s00221-004-2045-4

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  • DOI: https://doi.org/10.1007/s00221-004-2045-4

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