Spatial separation of visual and vestibular processing in the human hippocampal formation

The hippocampal formation, that is, the hippocampus proper and the parahippocampal region, is essential for various aspects of memory and plays an important role in human navigation. Navigational cues can be provided by both the visual system (e.g., landmarks, optic flow) and the vestibular system (e.g., estimation of direction during path integration). This study reviews anatomical, electrophysiological, and imaging data that support the view that vestibular input is primarily processed in the anterior part of the hippocampal formation, whereas visual cues are primarily integrated in the posterior part. In cases of reduced vestibular or visual input or excessive sensory stimulation, this hippocampal navigational network is reorganized. The separation of vestibular and visual information in the hippocampal formation has a twofold functional consequence: missing input from either system may be partially substituted for, and the task‐dependent sensorial weight can be shifted to, the more reliable modality for navigation.

[1]  M. Witter,et al.  Anatomical Organization of the Parahippocampal‐Hippocampal Network , 2000, Annals of the New York Academy of Sciences.

[2]  Martin Wiesmann,et al.  Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies , 2005, NeuroImage.

[3]  O. Grüsser,et al.  Responses of Single Neurons in the Parietoinsular Vestibular Cortex of Primates a , 1988, Annals of the New York Academy of Sciences.

[4]  P. Stoeter,et al.  Voxel‐based morphometry depicts central compensation after vestibular neuritis , 2010, Annals of neurology.

[5]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[6]  M P Witter,et al.  Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat , 1984, The Journal of comparative neurology.

[7]  Martin Wiesmann,et al.  Asymmetric modulation of human visual cortex activity during 10° lateral gaze (fMRI study) , 2005, NeuroImage.

[8]  N Burgess,et al.  Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. , 2001, Brain : a journal of neurology.

[9]  P. Liu,et al.  Long-term changes in hippocampal n-methyl-d-aspartate receptor subunits following unilateral vestibular damage in rat , 2003, Neuroscience.

[10]  A Berthoz,et al.  Discharge correlates of hippocampal complex spike neurons in behaving rats passively displaced on a mobile robot , 1998, Hippocampus.

[11]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[12]  M. Wilson,et al.  Trajectory Encoding in the Hippocampus and Entorhinal Cortex , 2000, Neuron.

[13]  R. Burwell The Parahippocampal Region: Corticocortical Connectivity , 2000, Annals of the New York Academy of Sciences.

[14]  R. Vertes,et al.  Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. , 1997, Neuroscience.

[15]  E. D. Haan,et al.  Varieties of human spatial memory: a meta-analysis on the effects of hippocampal lesions , 2001, Brain Research Reviews.

[16]  Hidenao Fukuyama,et al.  Cortical correlates of vestibulo-ocular reflex modulation: a PET study. , 2003, Brain : a journal of neurology.

[17]  R. Ito,et al.  Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging. , 2001, Brain research. Cognitive brain research.

[18]  Arne D. Ekstrom,et al.  Human Hippocampal CA1 Involvement during Allocentric Encoding of Spatial Information , 2009, The Journal of Neuroscience.

[19]  Richard S. J. Frackowiak,et al.  Recalling Routes around London: Activation of the Right Hippocampus in Taxi Drivers , 1997, The Journal of Neuroscience.

[20]  C. Gross,et al.  Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. , 1998, Journal of neurophysiology.

[21]  E. Gould,et al.  Learning enhances adult neurogenesis in the hippocampal formation , 1999, Nature Neuroscience.

[22]  J. Gabrieli,et al.  Neural Correlates of Encoding Space from Route and Survey Perspectives , 2002, The Journal of Neuroscience.

[23]  I S Curthoys,et al.  Electrophysiological evidence for vestibular activation of the guinea pig hippocampus , 2000, Neuroreport.

[24]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[25]  T. Brandt,et al.  Sensory system interactions during simultaneous vestibular and visual stimulation in PET , 2002, Human brain mapping.

[26]  P. Schlindwein,et al.  Neural correlates of hemispheric dominance and ipsilaterality within the vestibularsystem , 2008, NeuroImage.

[27]  J. Taube The head direction signal: origins and sensory-motor integration. , 2007, Annual review of neuroscience.

[28]  C. Darlington,et al.  Damage to the vestibular inner ear causes long-term changes in neuronal nitric oxide synthase expression in the rat hippocampus , 2001, Neuroscience.

[29]  M. Lemire,et al.  [Demonstration of a retino-thalamo-hippocampal pathway in the rat]. , 1987, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[30]  J B Poline,et al.  Human cortical networks for new and familiar sequences of saccades. , 2001, Cerebral cortex.

[31]  Robert Freedman,et al.  Neurobiology of smooth pursuit eye movement deficits in schizophrenia: an fMRI study. , 2004, The American journal of psychiatry.

[32]  T. Ohnishi,et al.  Navigation ability dependent neural activation in the human brain: An fMRI study , 2006, Neuroscience Research.

[33]  R. Muller,et al.  The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  T. Brandt,et al.  Structural and functional plasticity of the hippocampal formation in professional dancers and slackliners , 2010, Hippocampus.

[35]  Jeffrey S. Taube,et al.  Head direction cells and the neural mechanisms of spatial orientation , 2005 .

[36]  A. Wunderlich,et al.  Brain activation during human navigation: gender-different neural networks as substrate of performance , 2000, Nature Neuroscience.

[37]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[38]  W. Becker,et al.  Deriving angular displacement from optic flow: a fMRI study , 2009, Experimental Brain Research.

[39]  Tarek A. Yousry,et al.  fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation , 2002, Experimental Brain Research.

[40]  D. Manahan‐Vaughan,et al.  Synaptic Plasticity from Visual Cortex to Hippocampus: Systems Integration in Spatial Information Processing , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[41]  P. Andersen,et al.  Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  S. Bricogne,et al.  Neural Correlates of Topographic Mental Exploration: The Impact of Route versus Survey Perspective Learning , 2000, NeuroImage.

[43]  Ericka Stricklin-Parker,et al.  Ann , 2005 .

[44]  P. Schlindwein,et al.  Cortical representation of saccular vestibular stimulation: VEMPs in fMRI , 2008, NeuroImage.

[45]  K Cheng,et al.  Human cortical regions activated by wide-field visual motion: an H2(15)O PET study. , 1995, Journal of neurophysiology.

[46]  D. Amaral,et al.  Topographical organization of the entorhinal projection to the dentate gyrus of the monkey , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  T. Brandt,et al.  Reciprocal inhibitory visual-vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex. , 1998, Brain : a journal of neurology.

[48]  Thomas Brandt,et al.  Metabolic changes in vestibular and visual cortices in acute vestibular neuritis , 2004, Annals of neurology.

[49]  E. Maguire,et al.  Topographical disorientation following unilateral temporal lobe lesions in humans , 1996, Neuropsychologia.

[50]  H. Son,et al.  Adult hippocampal neurogenesis and related neurotrophic factors. , 2009, BMB reports.

[51]  Anatomical evidence of a retino-thalamo-hippocampal pathway in the pigeon (Columba livia). , 1995, Journal fur Hirnforschung.

[52]  F. Gage,et al.  Neurogenesis in the adult human hippocampus , 1998, Nature Medicine.

[53]  Derek K. Jones,et al.  Occipito-temporal connections in the human brain. , 2003, Brain : a journal of neurology.

[54]  T. Brandt,et al.  Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation , 2007, Hippocampus.

[55]  B. McNaughton,et al.  Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  Frontiers in Integrative Neuroscience Integrative Neuroscience , 2022 .

[57]  J. Krebs,et al.  Spatial learning induces neurogenesis in the avian brain , 1997, Behavioural Brain Research.

[58]  Robert S. Astur,et al.  Factors affecting the hippocampal BOLD response during spatial memory , 2008, Behavioural Brain Research.

[59]  T. Brandt,et al.  Gray‐Matter Atrophy after Chronic Complete Unilateral Vestibular Deafferentation , 2009, Annals of the New York Academy of Sciences.

[60]  Richard S. J. Frackowiak,et al.  Cerebral representations for egocentric space: functional-anatomical evidence from caloric vestibular stimulation and neck vibration , 2001, NeuroImage.

[61]  Thomas Stephan,et al.  Rollvection versus linearvection: Comparison of brain activations in PET , 2004, Human brain mapping.

[62]  Neil Burgess,et al.  Navigation expertise and the human hippocampus: A structural brain imaging analysis , 2003, Hippocampus.

[63]  Martin Wiesmann,et al.  Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging , 2004, NeuroImage.

[64]  M. Salami,et al.  Light deprivation improves melatonin related suppression of hippocampal plasticity , 2009, Hippocampus.

[65]  Jeffrey S Taube,et al.  Differentiating ascending vestibular pathways to the cortex involved in spatial cognition. , 2010, Journal of vestibular research : equilibrium & orientation.

[66]  Unilateral inner ear damage results in lasting changes in hippocampal CA1 field potentials in vitro , 2003, Hippocampus.

[67]  L. Domenici,et al.  Reduction of GFAP induced by long dark rearing is not restricted to visual cortex , 2006, Brain Research.

[68]  C. Frith,et al.  Cerebral representations for egocentric space: functional-anatomical evidence from caloric vestibular stimulation and neck vibration , 2001, NeuroImage.

[69]  Franco Lepore,et al.  Wayfinding in the blind: larger hippocampal volume and supranormal spatial navigation. , 2008, Brain : a journal of neurology.

[70]  Paul M. Thompson,et al.  Pattern of hippocampal shape and volume differences in blind subjects , 2009, NeuroImage.

[71]  T L Babb,et al.  Visual receptive fields and response properties of neurons in human temporal lobe and visual pathways. , 1983, Brain : a journal of neurology.

[72]  C. Gross,et al.  Neurogenesis in the neocortex of adult primates. , 1999, Science.

[73]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[74]  C. Büchel,et al.  Differential Recruitment of the Hippocampus, Medial Prefrontal Cortex, and the Human Motion Complex during Path Integration in Humans , 2007, The Journal of Neuroscience.

[75]  M. Petrides,et al.  Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice , 2003, The Journal of Neuroscience.

[76]  W. Milberg,et al.  Galvanic vestibular stimulation speeds visual memory recall , 2008, Experimental Brain Research.

[77]  D. Amaral,et al.  Topographical and laminar distribution of cortical input to the monkey entorhinal cortex , 2007, Journal of anatomy.

[78]  P. E. Sharp,et al.  Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  A. Berthoz,et al.  Mental navigation along memorized routes activates the hippocampus, precuneus, and insula , 1997, Neuroreport.

[80]  C. Büchel,et al.  Dissociable Retrosplenial and Hippocampal Contributions to Successful Formation of Survey Representations , 2005, The Journal of Neuroscience.

[81]  Thomas Brandt,et al.  Spatial Memory Deficits in Patients with Chronic Bilateral Vestibular Failure , 2003, Annals of the New York Academy of Sciences.

[82]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[83]  Gabriele Janzen,et al.  Memory consolidation of landmarks in good navigators , 2008, Hippocampus.

[84]  Arthur W. Toga,et al.  Genomic–anatomic evidence for distinct functional domains in hippocampal field CA1 , 2009, Proceedings of the National Academy of Sciences.

[85]  M. Wiesmann,et al.  Asymmetric modulation of human visual cortex activity during 10 degrees lateral gaze (fMRI study). , 2005, NeuroImage.

[86]  Thomas Stephan,et al.  Human Hippocampal Activation during Stance and Locomotion , 2009, Annals of the New York Academy of Sciences.

[87]  J. Feldon,et al.  Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: a within‐subject, within‐task comparison of reference and working spatial memory , 2004, The European journal of neuroscience.

[88]  Paul F. Smith,et al.  Vestibular–hippocampal interactions , 1997, Hippocampus.

[89]  T. Brandt,et al.  Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. , 2005, Brain : a journal of neurology.

[90]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[91]  A. Berthoz,et al.  Neurons responding to whole-body motion in the primate hippocampus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[92]  A. Berthoz,et al.  Activation of the hippocampal formation by vestibular stimulation: a functional magnetic resonance imaging study , 1996, Experimental Brain Research.

[93]  P. Brugger,et al.  Spatial- and verbal-memory improvement by cold-water caloric stimulation in healthy subjects , 2000, Experimental Brain Research.

[94]  J. Rawlins,et al.  Dissociation of function within the hippocampus: effects of dorsal, ventral and complete excitotoxic hippocampal lesions on spatial navigation , 2004, Neuroscience.

[95]  E. Maguire,et al.  The Well-Worn Route and the Path Less Traveled Distinct Neural Bases of Route Following and Wayfinding in Humans , 2003, Neuron.

[96]  Bruno Poucet,et al.  Properties of place cell firing after damage to the visual cortex , 2002, The European journal of neuroscience.

[97]  C. Wilson,et al.  Asymmetry and ventral course of the human geniculostriate pathway as determined by hippocampal visual evoked potentials and subsequent visual field defects after temporal lobectomy , 2004, Experimental Brain Research.

[98]  Adam N Mamelak,et al.  Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task , 2002, Behavioural Brain Research.

[99]  T. Brandt,et al.  Dominance for vestibular cortical function in the non-dominant hemisphere. , 2003, Cerebral cortex.

[100]  David K Bilkey,et al.  Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. , 2006, Journal of neurophysiology.

[101]  Alain Ptito,et al.  Alterations in right posterior hippocampus in early blind individuals , 2007, Neuroreport.

[102]  Hans-Jochen Heinze,et al.  Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task , 2004, Neuroreport.

[103]  Eren Gultepe,et al.  MRI diffusion tensor tracking of a new amygdalo‐fusiform and hippocampo‐fusiform pathway system in humans , 2009, Journal of Magnetic Resonance Imaging.

[104]  Cynthia L. Darlington,et al.  Vestibular influences on CA1 neurons in the rat hippocampus: an electrophysiological study in vivo , 2004, Experimental Brain Research.

[105]  T. Brandt,et al.  Thalamic infarctions cause side-specific suppression of vestibular cortex activations. , 2005, Brain : a journal of neurology.