Abstract
Many neurons in the deeper layers of the superior colliculus (SC) respond to multiple sensory inputs — visual, auditory, and somatic — as well as provide signals essential for saccadic eye movements to targets in different modalities. When the eyes and pinnae are in primary position, the neural map of auditory space is in rough topographic alignment with the map of visual space, and if the auditory map is based solely on head-pinna coordinates, any changes in eye position in the orbit will cause misalignment of the maps. We investigated the effects of eye position on the response of sound-sensitive neurons in the SC of cats because previous work on cats and on monkeys had suggested the possibility of species differences in the representation of auditory signals in the SC. We also investigated the effects of eye position on the accuracy of saccades to auditory, visual, and bimodal stimuli. All studies were conducted in alert, trained cats with the head restrained in a fixed position. Neuronal and behavioral responses were studied during periods when the eyes were steadily directed to different positions relative to the position of the sound. Cats showed partial compensation for eye position in making saccades, regardless of the modality of the target, and they showed similar patterns of error in saccades to auditory and visual targets. These behavioral data are consistent with coding the location of visual and auditory targets in the same coordinate system. In the vast majority of intermediate-layer neurons, eye position significantly affected the number of spikes evoked by sound stimuli. For most of these neurons, changes in eye position produced significant shifts in the speaker location producing maximal response. In some neurons, eye position significantly facilitated the magnitude of neuronal response evoked by sounds from a variety of speaker locations. Because few pinna movements could be detected, it is unlikely that these changes in neuronal response could be due to changes in the position of the pinnae. Our results indicate that the deep layers of the SC contain an eye-centered representation of sound location. Because eye position did not affect the percentage of neurons exhibiting multimodal integration, visual and auditory maps appear to remain integrated in the SC even when the eyes are directed eccentrically. Examination of the effects of eye position on neuronal responses to visual stimuli revealed that a substantial minority of neurons showed quantitative changes in the magnitude of response to visual stimuli when the retinal locus of stimulation was held constant.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Aitkin LM, Pettigrew JD, Calford MB, Phillips SC, Wise LZ (1985) Representation of stimulus azimuth by low-frequency neurons in inferior colliculus of the cat. J Neurophysiol 53: 43–59
Andersen RA, Bracewell RM, Barash S, Gnadt JW, Fogassi L (1990) Eye position effects on visual, memory, and saccaderelated activity in areas LIP and 7a of macaque. J Neurosci 10: 1176–1196
Calford MB, Moore DR, Hutchings ME (1986) Central and peripheral contributions to coding of acoustic space by neurons in inferior colliculus of cat. J Neurophysiol 55: 587–603
Duhamel J-R, Colby CL, Goldberg ME (1992) The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255: 90–92
Funahashi S, Bruce CJ, Goldman-Rakic PS (1990) Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. J Neurophysiol 63: 814–831
Gentilucci M, Scandolara C, Pigarev IN, Rizzolatti G (1983) Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position. Exp Brain Res 50: 464–468
Grasse KL, Dougles RM, Mendelson JR (1993) Alterations in visual receptive fields in the superior colliculus induced by amphetamine. Exp Brain Res 92: 453–466
Groh JM, Sparks DL (1992) Two models for transforming auditory signals from head-centered to eye-centered coordinates. Biol Cybern 67: 291–302
Guitton D, Munoz D (1991) Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. I. Identification, localization, and effects of behavior on sensory responses. J Neurophysiol 66: 1605–1623
Harris LR, Blakemore C, Donaghy M (1980) Integration of visual and auditory space in the mammalian superior colliculus. Nature 288: 56–59
Hartline PH, King AJ, Kurylo DD, Northmore DPM (1989) Effects of eye position on auditory localization and auditory spatial representation in cat superior colliculus. Invest Ophthalmol Vis Sci [Suppl] 30: 181
Hirsch JA, Chan JCK, Yin TCT (1985) Responses of neurons in the cat's superior colliculus to acoustic stimuli. I. Monaural and binaural response properties. J Neurophysiol 53: 726–745
Jay MF, Sparks DL (1987) Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals. J Neurophysiol 57: 35–55
Jay MF, Sparks DL (1989) Localization of auditory and visual targets for the initiation of saccadic eye movements. In: Berkley MA, Stebbins WC (eds) Comparative perception, vol 1. Wiley, New York, pp 351–374
King AJ, Moore DR (1991) Plasticity of auditory maps in the brain. Trends Neurosci 14: 31–37
Knudsen EI, Knudsen PF (1990) Sensitive and critical periods for visual calibration of sound localization by barn owls. J Neurosci 10: 222–232
Knudsen E, Lac SD, Esterly S (1987) Computational maps in the brain. Annu Rev Neurosci 10: 41–65
Korte M, Rauschecker JP (1993) Auditory spatial tuning of cortical neurons is sharpened in cats with early blindness. J Neurophysiol 70: 1717–1721
Kurylo DD, Vimal RLP, Hartline PH (1992) Effects of multiple stimuli on ocular orientation by cats. J Cogn Neurosci 4: 165–174
Kuwada S, Stanford TR, Batra R (1987) Interaural phase-sensitive units in the inferior colliculus of the unanesthetized rabbit: effects of changing frequency. J Neurophysiol 57: 1338–1360
Lal R, Friedlander MJ (1990) Effect of passive eye position changes on retinogeniculate transmission in the cat. J Neurophysiol 63: 502–522
Mays LE, Sparks DL (1980) Dissociation of visual and saccade-related responses in superior colliculus neurons. J Neurophysiol 43: 207–232
McIlwain JT (1983) Representation of the visual streak in visuotopic maps of the cat's superior colliculus: influence of the mapping variable. Vision Res 23: 507–516
Meredith MA, Nemitz JW, Stein BE (1987) Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors. J Neurosci 7: 3215–3229
Middlebrooks JC, Knudsen EI (1987) Changes in external ear position modify the spatial tuning of auditory units in the cat's superior colliculus. J Neurophysiol 57: 672–687
Middlebrooks JC, Clock AE, Xu L, Green DM (1994) A panoramic code for sound location by cortical neurons. Science 264: 842–844
Nelson JS, Meredith MA, Stein BE (1986) The influence of passive eye rotation on cat superior colliculus neurons. Soc Neurosci Abstr 12: 1538
Peck CK (1987) Visual-auditory interactions in cat superior colliculus: their role in the control of gaze. Brain Res 420: 162–166
Peck CK (1989) Visual responses of neurones in cat superior colliculus in relation to fixation of targets. J Physiol (Lond) 414: 301–315
Peck CK (1990) Neuronal activity related to head and eye movements in cat superior colliculus. J Physiol (Lond) 421: 79–104
Peck CK, Wartman FS (1989) Effects of eye position on auditory responses in cat superior colliculus. Invest Ophthalmol Vis Sci [Suppl] 30: 181
Peck CK, Schlag-Rey M, Schlag J (1980) Visuo-oculomotor properties of cells in the superior colliculus of the alert cat. J Comp Neurol 194: 97–116
Peck CK, Baro JA, Warder SM (1993) Sensory integration in the deep layers of the superior colliculus. In: Hicks TP, Molotchnikoff S, Ono T (eds) The visually responsive neuron: from basic physiology to behavior. Elsevier, Amsterdam, pp 91–102
Reuter-Lorenz PA, Nozawa G, Hughes HC (1992) Intersensory facilitation and express saccades. Invest Ophthalmol Vis Sci [Suppl] 33: 1357
Robinson DL, McClurkin JW, Kertzman C (1990) Orbital position and eye movement influences on visual responses in th pulvinar nuclei of the behaving macaque. Exp Brain Res 82: 235–246
Schlag J, Schlag-Rey M, Peck C, Joseph J-P (1980) Visual responses of thalamic neurons depending on the direction of gaze and the position of targets in space. Exp Brain Res 40: 170–184
Semple M, Aitkin L, Calford M, Pettigrew J, Phillips D (1983) Spatial receptive fields in the cat inferior colliculus. Hearing Res 10: 203–215
Sparks D (1986) Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol Rev 66: 118–171
Stein BE, Meredith MA (1993) The merging of the senses. MIT Press, Cambridge, Mass
Stein B, Meredith M, Huneycutt W, McDade L (1988) Behavioral indices of multisensory integration: orientation to visual cues is affected by auditory stimuli. J Cogn Neurosci 1: 12–24
Walker MF, Goldberg ME (1992) Soc Neurosci Abstr 18: 699
Weyand TG, Malpeli JG (1993) Responses of neurons in primary visual cortex are modulated by eye position. J Neurophysiol 69: 2258–2260
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Peck, C.K., Baro, J.A. & Warder, S.M. Effects of eye position on saccadic eye movements and on the neuronal responses to auditory and visual stimuli in cat superior colliculus. Exp Brain Res 103, 227–242 (1995). https://doi.org/10.1007/BF00231709
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00231709