Sound-localization performance in the cat: the effect of restraining the head.

In oculomotor research, there are two common methods by which the apparent location of visual and/or auditory targets are measured, saccadic eye movements with the head restrained and gaze shifts (combined saccades and head movements) with the head unrestrained. Because cats have a small oculomotor range (approximately +/-25 degrees), head movements are necessary when orienting to targets at the extremes of or outside this range. Here we tested the hypothesis that the accuracy of localizing auditory and visual targets using more ethologically natural head-unrestrained gaze shifts would be superior to head-restrained eye saccades. The effect of stimulus duration on localization accuracy was also investigated. Three cats were trained using operant conditioning with their heads initially restrained to indicate the location of auditory and visual targets via eye position. Long-duration visual targets were localized accurately with little error, but the locations of short-duration visual and both long- and short-duration auditory targets were markedly underestimated. With the head unrestrained, localization accuracy improved substantially for all stimuli and all durations. While the improvement for long-duration stimuli with the head unrestrained might be expected given that dynamic sensory cues were available during the gaze shifts and the lack of a memory component, surprisingly, the improvement was greatest for the auditory and visual stimuli with the shortest durations, where the stimuli were extinguished prior to the onset of the eye or head movement. The underestimation of auditory targets with the head restrained is explained in terms of the unnatural sensorimotor conditions that likely result during head restraint.

[1]  Marco Schieppati,et al.  Neck muscle vibration and spatial orientation during stepping in place in humans. , 2002, Journal of neurophysiology.

[2]  C. Prablanc,et al.  Saccadic responses evoked by presentation of visual and auditory targets , 2004, Experimental Brain Research.

[3]  J. Roll,et al.  Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study , 2004, Experimental Brain Research.

[4]  R. McCrea,et al.  Neck proprioceptive inputs to primate vestibular nucleus neurons , 2000, Experimental Brain Research.

[5]  Scott L. Delp,et al.  Three-dimensional spatial tuning of neck muscle activation in humans , 2002, Experimental Brain Research.

[6]  E D Young,et al.  Responses of squirrel monkey vestibular neurons to audio-frequency sound and head vibration. , 1977, Acta oto-laryngologica.

[7]  T. Kitama,et al.  Integration of vestibular and neck afferent signals in the central cervical nucleus. , 1988, Progress in brain research.

[8]  D. Kurylo,et al.  Effects of eye position on auditory localization and neural representation of space in superior colliculus of cats , 2004, Experimental Brain Research.

[9]  G. Blasdel,et al.  Sound localization by the barn owl (Tyto alba) measured with the search coil technique , 1979, Journal of comparative physiology.

[10]  D. McCloskey,et al.  Proprioceptive Illusions Induced by Muscle Vibration: Contribution by Muscle Spindles to Perception? , 1972, Science.

[11]  Tom C T Yin,et al.  Bimodal Interactions in the Superior Colliculus of the Behaving Cat , 2002, The Journal of Neuroscience.

[12]  Daniel J Tollin,et al.  Spectral cues explain illusory elevation effects with stereo sounds in cats. , 2003, Journal of neurophysiology.

[13]  J. Lackner Some proprioceptive influences on the perceptual representation of body shape and orientation. , 1988, Brain : a journal of neurology.

[14]  C. K. Peck,et al.  Saccadic eye movements to visual and auditory targets , 1997, Experimental Brain Research.

[15]  V C Abrahams,et al.  Projections of extraocular, neck muscle, and retinal afferents to superior colliculus in the cat: their connections to cells of origin of tectospinal tract. , 1975, Journal of neurophysiology.

[16]  B Craske,et al.  Perception of impossible limb positions induced by tendon vibration. , 1977, Science.

[17]  B D Corneil,et al.  Neck muscles in the rhesus monkey. I. Muscle morphometry and histochemistry. , 2001, Journal of neurophysiology.

[18]  Igal Savion,et al.  Bone conduction experiments in humans – a fluid pathway from bone to ear , 2000, Hearing Research.

[19]  A. Fuchs,et al.  A method for measuring horizontal and vertical eye movement chronically in the monkey. , 1966, Journal of applied physiology.

[20]  T. Yin,et al.  Behavioral Studies of Sound Localization in the Cat , 1998, The Journal of Neuroscience.

[21]  T Mergner,et al.  Vestibular-neck interaction and transformation of sensory coordinates. , 1997, Journal of vestibular research : equilibrium & orientation.

[22]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[23]  K. E. Popov,et al.  Visual and oculomotor responses induced by neck vibration in normal subjects and labyrinthine-defective patients , 1999, Experimental Brain Research.

[24]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[25]  David L. Sparks,et al.  Auditory receptive fields in primate superior colliculus shift with changes in eye position , 1984, Nature.

[26]  T C Yin,et al.  Pinna Movements of the Cat during Sound Localization , 1998, The Journal of Neuroscience.

[27]  J. Lackner,et al.  Aspects of body self-calibration , 2000, Trends in Cognitive Sciences.

[28]  B. May,et al.  Sound orientation behavior in cats. I. Localization of broadband noise. , 1996, The Journal of the Acoustical Society of America.

[29]  H. Barbas,et al.  Excitatory and inhibitory interactions of extraocular and dorsal neck muscle afferents in the cat frontal cortex , 1981, Experimental Neurology.

[30]  H. Voss [Tabulation of the absolute and relative muscular spindle numbers in human skeletal musculature]. , 1971, Anatomischer Anzeiger.

[31]  G. Goldenberg,et al.  Neck muscle vibration induces lasting recovery in spatial neglect , 2002, Journal of neurology, neurosurgery, and psychiatry.

[32]  P. Daniel,et al.  MUSCLE SPINDLES IN MAN; THEIR MORPHOLOGY IN THE LUMBRICALS AND THE DEEP MUSCLES OF THE NECK. , 1963, Brain : a journal of neurology.

[33]  A. Hudspeth Mechanoelectrical transduction by hair cells of the bullfrog's sacculus. , 1989, Progress in brain research.

[34]  H. Karnath,et al.  Decrease of contralateral neglect by neck muscle vibration and spatial orientation of trunk midline. , 1993, Brain : a journal of neurology.

[35]  H. MacDougall,et al.  Vibration-induced ocular torsion and nystagmus after unilateral vestibular deafferentation. , 2003, Brain : a journal of neurology.

[36]  F L Wightman,et al.  Resolution of front-back ambiguity in spatial hearing by listener and source movement. , 1999, The Journal of the Acoustical Society of America.

[37]  David L. Sparks,et al.  Saccades to remembered target locations: an analysis of systematic and variable errors , 1994, Vision Research.

[38]  E D Young,et al.  Effects of pinna position on head-related transfer functions in the cat. , 1996, The Journal of the Acoustical Society of America.

[39]  Richard R. Fay,et al.  Integrative Functions in the Mammalian Auditory Pathway , 2002, Springer Handbook of Auditory Research.

[40]  D. Sparks,et al.  Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. , 1996, Journal of neurophysiology.

[41]  John A. Baro,et al.  Effects of eye position on saccadic eye movements and on the neuronal responses to auditory and visual stimuli in cat superior colliculus , 2004, Experimental Brain Research.

[42]  Régine Roll,et al.  From balance regulation to body orientation: two goals for muscle proprioceptive information processing? , 1999, Experimental Brain Research.

[43]  P. Narins,et al.  Sound and vibration sensitivity of VIIIth nerve fibers in the frogs Leptodactylus albilabris and Rana pipiens pipiens , 2004, Journal of Comparative Physiology A.

[44]  Michael Fetter,et al.  The interactive contribution of neck muscle proprioception and vestibular stimulation to subjective “straight ahead” orientation in man , 2004, Experimental Brain Research.

[45]  W. Ehrenstein,et al.  Influence of head-to-trunk position on sound lateralization , 1998, Experimental Brain Research.

[46]  R H Schor,et al.  Response of vestibular neurons to head rotations in vertical planes. II. Response to neck stimulation and vestibular-neck interaction. , 1988, Journal of neurophysiology.

[47]  Simon Carlile,et al.  Methods for spherical data analysis and visualization , 1998, Journal of Neuroscience Methods.

[48]  Robert Tibshirani,et al.  Bootstrap Methods for Standard Errors, Confidence Intervals, and Other Measures of Statistical Accuracy , 1986 .

[49]  J R Lackner,et al.  Elicitation of vestibular side effects by regional vibration of the head. , 1974, Aerospace medicine.

[50]  I. Curthoys,et al.  Neck muscle vibration alters visually‐perceived roll after unilateral vestibular loss , 2000, Neuroreport.

[51]  J. Roll,et al.  Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography , 2004, Experimental Brain Research.

[52]  E. Knudsen The Hearing of the Barn Owl , 1981 .

[53]  K. Popov,et al.  Postural responses to vibration of neck muscles in patients with unilateral vestibular lesions , 1996, Neuroscience Letters.

[54]  J. Lackner,et al.  Changes in apparent body orientation and sensory localization induced by vibration of postural muscles: vibratory myesthetic illusions. , 1979, Aviation, space, and environmental medicine.

[55]  F. Richmond,et al.  Marked non-uniformity of fiber-type composition in the primate suboccipital muscle obliquus capitis inferior , 1999, Experimental Brain Research.

[56]  William H. Press,et al.  Numerical Recipes in C, 2nd Edition , 1992 .

[57]  G. Lennerstrand,et al.  Eye movements in normal subjects induced by vibratory activation of neck muscle proprioceptors. , 2009, Acta ophthalmologica Scandinavica.

[58]  F Lacquaniti,et al.  Effect of gaze on postural responses to neck proprioceptive and vestibular stimulation in humans , 1999, The Journal of physiology.

[59]  Daniel J Tollin,et al.  Psychophysical investigation of an auditory spatial illusion in cats: the precedence effect. , 2003, Journal of neurophysiology.

[60]  D. Sparks,et al.  Saccades to remembered targets exhibit enhanced orbital position effects in monkeys , 2001, Vision Research.

[61]  F L Wightman,et al.  Headphone simulation of free-field listening. II: Psychophysical validation. , 1989, The Journal of the Acoustical Society of America.

[62]  P. Matthews Where does Sherrington's "muscular sense" originate? Muscles, joints, corollary discharges? , 1982, Annual review of neuroscience.

[63]  M. Crommelinck,et al.  Stimulation of the superior colliculus in the alert cat , 1980, Experimental Brain Research.

[64]  A. Hein,et al.  Neck muscle vibration modifies the representation of visual motion and direction in man. , 1988, Brain : a journal of neurology.

[65]  T. Mergner,et al.  Visual object localisation in space , 2001, Experimental Brain Research.

[66]  J. M. de Jong,et al.  On cervical nystagmus and related disorders. , 1969, Brain : a journal of neurology.

[67]  T. Mergner,et al.  Human perception of horizontal trunk and head rotation in space during vestibular and neck stimulation , 2004, Experimental Brain Research.

[68]  H H Goossens,et al.  Influence of head position on the spatial representation of acoustic targets. , 1999, Journal of neurophysiology.

[69]  T. Brandt,et al.  Perceptual and oculomotor effects of neck muscle vibration in vestibular neuritis. Ipsilateral somatosensory substitution of vestibular function. , 1998, Brain : a journal of neurology.

[70]  O. Grüsser,et al.  Vestibular neurones in the parieto‐insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses. , 1990, The Journal of physiology.

[71]  E. B. Newman,et al.  The localization of actual sources of sound. , 1936 .

[72]  F. Richmond,et al.  Animal models of motor systems: cautionary tales from studies of head movement. , 1999, Progress in brain research.

[73]  J. C. Middlebrooks,et al.  Two-dimensional sound localization by human listeners. , 1990, The Journal of the Acoustical Society of America.

[74]  F. Richmond,et al.  Morphology and distribution of muscle spindles in dorsal muscles of the cat neck. , 1975, Journal of neurophysiology.

[75]  L F Dell'Osso,et al.  Audio-ocular response characteristics. , 1978, Sensory processes.

[76]  Graeme D. Jackson,et al.  Head Position Modulates Activity in the Human Parietal Eye Fields , 2003, NeuroImage.

[77]  D L Sparks,et al.  Activity of cells in the deeper layers of the superior colliculus of the rhesus monkey: evidence for a gaze displacement command. , 1997, Journal of neurophysiology.

[78]  P. Matthews,et al.  Mammalian muscle receptors and their central actions , 1974 .

[79]  M. A. Frens,et al.  A quantitative study of auditory-evoked saccadic eye movements in two dimensions , 2004, Experimental Brain Research.

[80]  S. Lund Postural effects of neck muscle vibration in man , 1980, Experientia.

[81]  L. Cohen Role of eye and neck proprioceptive mechanisms in body orientation and motor coordination. , 1961, Journal of neurophysiology.

[82]  H. Heffner,et al.  Visual factors in sound localization in mammals , 1992, The Journal of comparative neurology.

[83]  J. Dichgans,et al.  Effect of prolonged neck muscle vibration on lateral head tilt in severe spasmodic torticollis , 2000, Journal of neurology, neurosurgery, and psychiatry.

[84]  D R Perrott,et al.  Changes in head position as a measure of auditory localization performance: auditory psychomotor coordination under monaural and binaural listening conditions. , 1987, The Journal of the Acoustical Society of America.

[85]  Zahn,et al.  The audioocular response: intersensory delay. , 1979, Sensory processes.

[86]  P T de Jong,et al.  Ataxia and nystagmus induced by injection of local anesthetics in the neck , 1977, Annals of neurology.

[87]  R. Andersen,et al.  Head position signals used by parietal neurons to encode locations of visual stimuli , 1995, Nature.

[88]  Richard A. Andersen,et al.  Sensorimotor transformation during eye movements to remembered visual targets , 1991, Vision Research.

[89]  J. L. Taylor,et al.  Illusions of head and visual target displacement induced by vibration of neck muscles. , 1991, Brain : a journal of neurology.

[90]  U. Windhorst,et al.  Interactions between motor units in modulating discharge patterns of primary muscle spindle endings , 2005, Experimental Brain Research.

[91]  M. Hepp-Reymond,et al.  Eye and head movements to auditory targets , 2004, Experimental Brain Research.

[92]  T. Yagi,et al.  Three-dimensional analysis of nystagmus induced by neck vibration. , 1996, Acta oto-laryngologica.

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

[94]  F. Richmond,et al.  Anatomical organization and sensory receptor content of soft tissues surrounding upper cervical vertebrae in the cat. , 1982, Journal of neurophysiology.

[95]  R. Andersen,et al.  Dorsal neck muscle vibration induces upward shifts in the endpoints of memory-guided saccades in monkeys. , 2004, Journal of neurophysiology.

[96]  Haim Sohmer,et al.  Bone conduction experiments in animals – evidence for a non-osseous mechanism , 2000, Hearing Research.

[97]  J. Roll,et al.  Eye and neck proprioceptive messages contribute to the spatial coding of retinal input in visually oriented activities , 2004, Experimental Brain Research.

[98]  A M Bronstein,et al.  The perception of head and neck angular displacement in normal and labyrinthine-defective subjects. A quantitative study using a 'remembered saccade' technique. , 1995, Brain : a journal of neurology.

[99]  S. Gandevia Kinesthesia : roles for afferent signals and motor commands , 1996 .

[100]  G E Loeb,et al.  Neck muscles in the rhesus monkey. II. Electromyographic patterns of activation underlying postures and movements. , 2001, Journal of neurophysiology.

[101]  S. Aw,et al.  Vibration-induced shift of the subjective visual horizontal: a sign of unilateral vestibular deficit. , 2002, Archives of otolaryngology--head & neck surgery.

[102]  R. Douglas,et al.  Eye-head coordination in cats. , 1984, Journal of neurophysiology.

[103]  T. Mergner,et al.  The role of canal-neck interaction for the perception of horizontal trunk and head rotation , 2004, Experimental Brain Research.

[104]  Daniel J Tollin,et al.  Effect of eye position on saccades and neuronal responses to acoustic stimuli in the superior colliculus of the behaving cat. , 2004, Journal of neurophysiology.

[105]  A. Berthoz,et al.  Horizontal eye position-related activity in neck muscles of the alert cat , 2004, Experimental Brain Research.

[106]  Eliana M. Klier,et al.  The superior colliculus encodes gaze commands in retinal coordinates , 2001, Nature Neuroscience.

[107]  Richard A. Andersen,et al.  Separate body- and world-referenced representations of visual space in parietal cortex , 1998, Nature.

[108]  A John Van Opstal,et al.  The influence of duration and level on human sound localization. , 2004, The Journal of the Acoustical Society of America.

[109]  H. Karnath,et al.  The perception of body orientation after neck-proprioceptive stimulation , 2002, Experimental Brain Research.

[110]  A. D. Van Beuzekom,et al.  Interaction between visual and vestibular signals for the control of rapid eye movements , 2002 .

[111]  J. Lackner,et al.  Fingertip contact suppresses the destabilizing influence of leg muscle vibration. , 2000, Journal of neurophysiology.

[112]  Mark A. Ericson,et al.  A pointing technique for rapidly collecting localization responses in auditory research , 1995 .

[113]  W. Ehrenstein,et al.  Neck-proprioceptive influence on auditory lateralization , 1999, Experimental Brain Research.