Neural Correlates for Angular Head Velocity in the Rat Dorsal Tegmental Nucleus

Many neurons in the rat lateral mammillary nuclei (LMN) fire selectively in relation to the animal's head direction (HD) in the horizontal plane independent of the rat's location or behavior. One hypothesis of how this representation is generated and updated is via subcortical projections from the dorsal tegmental nucleus (DTN). Here we report the type of activity in DTN neurons. The majority of cells (75%) fired as a function of the rat's angular head velocity (AHV). Cells exhibited one of two types of firing patterns: (1) symmetric, in which the firing rate was positively correlated with AHV during head turns in both directions, and (2) asymmetric, in which the firing rate was positively correlated with head turns in one direction and correlated either negatively or not at all in the opposite direction. In addition to modulation by AHV, some of the AHV cells (40.1%) were weakly modulated by the rat's linear velocity, and a smaller number were modulated by HD (11%) or head pitch (15.9%). Autocorrelation analyses indicated that with the head stationary, AHV cells displayed irregular discharge patterns. Because afferents from the DTN are the major source of information projecting to the LMN, these results suggest that AHV information from the DTN plays a significant role in generating the HD signal in LMN. A model is proposed showing how DTN AHV cells can generate and update the LMN HD cell signal.

[1]  J. Goldberg,et al.  Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. 3. Variations among units in their discharge properties. , 1971, Journal of neurophysiology.

[2]  A. A. Skavenski,et al.  Role of abducens neurons in vestibuloocular reflex. , 1973, Journal of neurophysiology.

[3]  R. Baker.  The Nucleus Prepositus Hypoglossi , 1977 .

[4]  R. Skinner,et al.  Monosynaptic vestibular nerve input to vestibular and adjacent reticular neurons projecting into the ascending medial longitudinal fasciculus , 1979, Experimental Neurology.

[5]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[6]  J. Kubie.  A driveable bundle of microwires for collecting single-unit data from freely-moving rats , 1984, Physiology & Behavior.

[7]  Lisa Chang,et al.  The dorsal tegmental nucleus: an axoplasmic transport study , 1984, Brain Research.

[8]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[9]  W. Precht,et al.  Responses of prepositus hypoglossi neurons to optokinetic and vestibular stimulations in the rat , 1984, Brain Research.

[10]  W. Nauta,et al.  Cytoarchitecture, fiber connections, and some histochemical aspects of the interpeduncular nucleus in the rat , 1986, The Journal of comparative neurology.

[11]  N. Hirai.  Input-output relations of lobules I and II of the cerebellar anterior lobe vermis in connexion with neck and vestibulospinal reflexes in the cat , 1987, Neurosciences research.

[12]  Hideshi Shibata,et al.  Ascending projections to the mammillary nuclei in the rat: A study using retrograde and anterograde transport of wheat germ agglutinin conjugated to horseradish peroxidase , 1987, The Journal of comparative neurology.

[13]  A K Moschovakis,et al.  Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey. II. Correlation with output pathways of secondary neurons. , 1987, Journal of neurophysiology.

[14]  D. Pfaff,et al.  Electrical stimulation of the midbrain central gray facilitates lateral vestibulospinal activation of back muscle EMG in the rat , 1987, Brain Research.

[15]  R. McCrea,et al.  Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey , 1988, The Journal of comparative neurology.

[16]  H. Groenewegen,et al.  Basal forebrain inputs to the interpeduncular nucleus in the rat studied with the Phaseolus vulgaris-leucoagglutinin tracing method , 1988, Brain Research Bulletin.

[17]  G. Aston-Jones,et al.  Potent inhibitory input to locus coeruleus from the nucleus prepositus hypoglossi , 1989, Brain Research Bulletin.

[18]  D. Hopkins,et al.  Mamillary body in the rat: Topography and synaptology of projections from the subicular complex, prefrontal cortex, and midbrain tegmentum , 1989, The Journal of comparative neurology.

[19]  D. Robinson,et al.  Integrating with neurons. , 1989, Annual review of neuroscience.

[20]  K. Zyo,et al.  Fine structure of the lateral mammillary projection to the dorsal tegmental nucleus of gudden in the rat , 1990, The Journal of comparative neurology.

[21]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  J. Goldberg,et al.  Vestibular-nerve inputs to the vestibulo-ocular reflex: a functional- ablation study in the squirrel monkey , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  永福 智志.  The Organization of Learning , 2005, Journal of Cognitive Neuroscience.

[25]  B. McNaughton,et al.  Dead Reckoning, Landmark Learning, and the Sense of Direction: A Neurophysiological and Computational Hypothesis , 1991, Journal of Cognitive Neuroscience.

[26]  S. Mizumori,et al.  Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  David Wirtshafter,et al.  Evidence for GABAergic projections from the tegmental nuclei of Gudden to the mammillary body in the rat , 1993, Brain Research.

[28]  Bruce L. McNaughton,et al.  A Model of the Neural Basis of the Rat's Sense of Direction , 1994, NIPS.

[29]  Hugh T. Blair,et al.  Simualtion of a Thalamocortical Circuit for Computing Directional Heading in the Rat , 1995, NIPS.

[30]  J. Taube.  Head direction cells recorded in the anterior thalamic nuclei of freely moving rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  A David Redishyx,et al.  A coupled attractor model of the rodent head direction system , 1996 .

[32]  K. Zhang,et al.  Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  J. Taube,et al.  Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input , 1997, The Journal of Neuroscience.

[34]  J. Taube,et al.  Interaction between the Postsubiculum and Anterior Thalamus in the Generation of Head Direction Cell Activity , 1997, The Journal of Neuroscience.

[35]  J. Taube,et al.  Firing Properties of Rat Lateral Mammillary Single Units: Head Direction, Head Pitch, and Angular Head Velocity , 1998, The Journal of Neuroscience.

[36]  R U Muller,et al.  Comparisons of head direction cell activity in the postsubiculum and anterior thalamus of freely moving rats , 1998, Hippocampus.

[37]  H. Aldskogius,et al.  Central neuron–glial and glial–glial interactions following axon injury , 1998, Progress in Neurobiology.

[38]  H. T. Blair,et al.  Role of the Lateral Mammillary Nucleus in the Rat Head Direction Circuit A Combined Single Unit Recording and Lesion Study , 1998, Neuron.

[39]  J. Taube.  Head direction cells and the neurophysiological basis for a sense of direction , 1998, Progress in Neurobiology.

[40]  P E Sharp,et al.  The Anterior Thalamic Head-Direction Signal Is Abolished by Bilateral But Not Unilateral Lesions of the Lateral Mammillary Nucleus , 1999, The Journal of Neuroscience.

[41]  D. Touretzky,et al.  Modeling attractor deformation in the rodent head-direction system. , 2000, Journal of neurophysiology.

[42]  N. Shimizu.  [Neurology of eye movements]. , 2000, Rinsho shinkeigaku = Clinical neurology.

[43]  P. E. Sharp,et al.  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. , 2001, Behavioral neuroscience.

[44]  H. T. Blair,et al.  The anatomical and computational basis of the rat head-direction cell signal , 2001, Trends in Neurosciences.

[45]  P. E. Sharp,et al.  Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. , 2001, Behavioral neuroscience.

[46]  J. Taube,et al.  Hippocampal spatial representations require vestibular input , 2002, Hippocampus.