Persistent neural activity in head direction cells.

Many neurons throughout the rat limbic system discharge in relation to the animal's directional heading with respect to its environment. These so-called head direction (HD) cells exhibit characteristics of persistent neural activity. This article summarizes where HD cells are found, their major properties, and some of the important experiments that have been conducted to elucidate how this signal is generated. The number of HD and angular head velocity cells was estimated for several brain areas involved in the generation of the HD signal, including the postsubiculum, anterior dorsal thalamus, lateral mammillary nuclei and dorsal tegmental nucleus. The HD cell signal has many features in common with what is known about how neural integration is accomplished in the oculomotor system. The nature of the HD cell signal makes it an attractive candidate for using neural network models to elucidate the signal's underlying mechanisms. The conditions that any network model must satisfy in order to accurately represent how the nervous system generates this signal are highlighted and areas where key information is missing are discussed.

[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]  M. T. Shipley The topographical and laminar organization of the presubiculum's projection to the ipsi‐ and contralateral entorhinal cortex in the guinea pig , 1975, The Journal of comparative neurology.

[3]  B. A. Flumerfelt,et al.  Afferent connections of the interpeduncular nucleus and the topographic organization of the habenulo‐interpeduncular pathway: An HRP study in the rat , 1981, The Journal of comparative neurology.

[4]  A. Berthoz,et al.  Neuronal activity in prepositus nucleus correlated with eye movement in the alert cat. , 1982, Journal of neurophysiology.

[5]  Michael W. Miller,et al.  Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices , 1983, The Journal of comparative neurology.

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

[7]  H. Groenewegen,et al.  Efferent connections of the dorsal tegmental region in the rat, studied by means of anterograde transport of the lectin Phaseolus vulgaris-leucoagglutinin (PHA-L) , 1984, Brain Research.

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

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

[10]  J. M. Wyss,et al.  Thalamic projections to retrosplenial cortex in the rat , 1986, The Journal of comparative neurology.

[11]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[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]  J. Michael Wyss,et al.  The laminar organization of efferent neuronal cell bodies in the retrosplenial granular cortex , 1987, Brain Research.

[14]  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.

[15]  H. Shibata Descending projections to the mammillary nuclei in the rat, as studied by retrograde and anterograde transport of wheat germ agglutinin–horseradish peroxidase , 1989, The Journal of comparative neurology.

[16]  K. Zyo,et al.  Retrograde double‐labeling study of the marnmillothalamic and the mammillotegmental projections in the rat , 1989, The Journal of comparative neurology.

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

[18]  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.

[19]  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.

[20]  T. van Groen,et al.  The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections , 1990, Brain Research.

[21]  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.

[22]  A. Fuchs,et al.  Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. , 1992, Journal of neurophysiology.

[23]  H. Shibata,et al.  Topographic organization of subcortical projections to the anterior thalamic nuclei in the rat , 1992, The Journal of comparative neurology.

[24]  J. Michael Wyass,et al.  Connections between the retrosplenial cortex and the hippocampal formation in the rat: A review , 1992, Hippocampus.

[25]  H. Shibata Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat , 1993, The Journal of comparative neurology.

[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]  H. Shibata,et al.  Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat , 1993, The Journal of comparative neurology.

[28]  S. Wiener Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  A. Gonzalo-Ruiz,et al.  Immunohistochemical localization of gaba in the mammillary complex of the rat , 1993, Neuroscience.

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

[31]  Hideshi Shibata,et al.  Terminal distribution of projections from the retrosplenial area to the retrohippocampal region in the rat, as studied by anterograde transport of biotinylated dextran amine , 1994, Neuroscience Research.

[32]  R. Baker,et al.  Eye position and eye velocity integrators reside in separate brainstem nuclei. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

[34]  H. T. Blair,et al.  Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  T. van Groen,et al.  Projections from the anterodorsal and anteroveniral nucleus of the thalamus to the limbic cortex in the rat , 1995, The Journal of comparative neurology.

[36]  Jeffrey S. Taube,et al.  Preferential use of the landmark navigational system by head direction cells in rats. , 1995 .

[37]  J. Taube,et al.  Head direction cell activity monitored in a novel environment and during a cue conflict situation. , 1995, Journal of neurophysiology.

[38]  J S Taube,et al.  Preferential use of the landmark navigational system by head direction cells in rats. , 1995, Behavioral neuroscience.

[39]  D L Robinson,et al.  Modified saccades evoked by stimulation of the macaque superior colliculus account for properties of the resettable integrator. , 1995, Journal of neurophysiology.

[40]  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.

[41]  H. T. Blair,et al.  Neural network modeling of the hippocampal formation spatial signals and their possible role in navigation: A modular approach , 1996, Hippocampus.

[42]  P E Sharp,et al.  Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat. , 1995, Behavioral neuroscience.

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

[44]  P. E. Sharp Multiple spatial/behavioral correlates for cells in the rat postsubiculum: multiple regression analysis and comparison to other hippocampal areas. , 1996, Cerebral cortex.

[45]  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.

[46]  J. Taube,et al.  Head direction cells and episodic spatial information in rats without a hippocampus. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[47]  B L McNaughton,et al.  Path Integration and Cognitive Mapping in a Continuous Attractor Neural Network Model , 1997, The Journal of Neuroscience.

[48]  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.

[49]  M J West,et al.  Neuron numbers in the presubiculum, parasubiculum, and entorhinal area of the rat , 1997, The Journal of comparative neurology.

[50]  J. Büttner-Ennever The Rat Brain in Stereotaxic Coordinates, 3rd edn. By George Paxinos and Charles Watson. (Pp. xxxiii+80; illustrated; £$69.95 paperback; ISBN 0 12 547623; comes with CD‐ROM.) San Diego: Academic Press. 1996. , 1997 .

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

[52]  E Godaux,et al.  Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. , 1998, Journal of neurophysiology.

[53]  Thomas J. Anastasio,et al.  Nonuniformity in the linear network model of the oculomotor integrator produces approximately fractional-order dynamics and more realistic neuron behavior , 1998, Biological Cybernetics.

[54]  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.

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

[56]  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.

[57]  J. Taube,et al.  Cue control and head direction cells. , 1998, Behavioral neuroscience.

[58]  Edward J Golob,et al.  Recordings of postsubiculum head direction cells following lesions of the laterodorsal thalamic nucleus , 1998, Brain Research.

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

[60]  A. Redish Beyond the Cognitive Map: From Place Cells to Episodic Memory , 1999 .

[61]  A M Bronstein,et al.  Vestibular perception of angular velocity in normal subjects and in patients with congenital nystagmus. , 1999, Brain : a journal of neurology.

[62]  G T Gdowski,et al.  Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. , 1999, Journal of neurophysiology.

[63]  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.

[64]  E. Rolls,et al.  Head direction cells in the primate pre‐subiculum , 1999, Hippocampus.

[65]  Sidney I. Wiener,et al.  Influence of conflicting visual, inertial and substratal cues on head direction cell activity , 2000, Experimental Brain Research.

[66]  Daniel D. Lee,et al.  Stability of the Memory of Eye Position in a Recurrent Network of Conductance-Based Model Neurons , 2000, Neuron.

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

[68]  S Leutgeb,et al.  Convergence of Head Direction and Place Information in the Ca1 Region of Hippocampus Subjects and Behavioral Testing , 2000 .

[69]  S. Mizumori,et al.  Location and head direction representation in the dorsal striatum of rats , 2000, Psychobiology.

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

[71]  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.

[72]  Jefferson E. Roy,et al.  Selective Processing of Vestibular Reafference during Self-Generated Head Motion , 2001, The Journal of Neuroscience.

[73]  A Berthoz,et al.  Active locomotion increases peak firing rates of anterodorsal thalamic head direction cells. , 2001, Journal of neurophysiology.

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

[75]  J. Bassett,et al.  Neural Correlates for Angular Head Velocity in the Rat Dorsal Tegmental Nucleus , 2001, The Journal of Neuroscience.

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

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

[78]  Jeffrey S Taube,et al.  The neural correlates of navigation: do head direction and place cells guide spatial behavior? , 2002, Behavioral and cognitive neuroscience reviews.

[79]  B. J. Yates,et al.  Does the vestibular system contribute to head direction cell activity in the rat? , 2002, Physiology & Behavior.

[80]  Richard H R Hahnloser,et al.  Double-ring network model of the head-direction system. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[81]  J. Bassett,et al.  Passive transport disrupts directional path integration by rat head direction cells. , 2003, Journal of neurophysiology.

[82]  A. Berthoz,et al.  Rapid Spatial Reorientation and Head Direction Cells , 2003, The Journal of Neuroscience.

[83]  H. Kornhuber,et al.  Natural and drug-induced variations of velocity and duration of human saccadic eye movements: Evidence for a control of the neural pulse generator by local feedback , 2004, Biological Cybernetics.

[84]  Carson C. Chow,et al.  Localized Bumps of Activity Sustained by Inhibition in a Two-Layer Thalamic Network , 2004, Journal of Computational Neuroscience.

[85]  E. J. Green,et al.  Head-direction cells in the rat posterior cortex , 1994, Experimental Brain Research.