Visual, somatosensory, auditory and nociceptive modality properties in the feline suprageniculate nucleus

Response properties of 252 single-units to visual, auditory, somatosensory and noxious stimulation were recorded by means of extracellular microelectrodes in the suprageniculate nucleus of anaesthetized, immobilized cats. Of the 141 units tested for modality properties the majority (n=113, 80.1%) was found unimodal in the sense that stimuli of exclusively one sensory modality were able to elicit an activation of the unit. Twenty-four (17.0%) cells were bimodal and four (2.8%) were trimodal (visual, somatosensory and auditory). The visual modality dominated the unimodal cells (n=74, 65.5%), while cells responsive to somatic stimulation (n=20, 17.6%), auditory stimulation (n=16, 14.1%) or noxious stimulation of the tooth pulp (n=3, 2.6%) were less frequently encountered. Visual sensitivity dominated the multisensory cells, too. The visually responsive units were characterized by having a sensitivity to stimuli moving in a rather large, uniform receptive field that covered the contralateral lower quadrant, and encompassed a flanking area of about 20 degree width in both the upper contralateral and lower ipsilateral visual fields. Many cells (n=52, 47%) were sensitive to the direction of the stimulation and reacted to stimuli moving at a high velocity (20-200 deg/s). Most cells responded differently to stimuli of a variety of sizes. Somatosensory units reacted to stimuli presented over a wide area on the contralateral side of the body, thus showing no sign of somatotopic organization. The auditory sensitivity fell within a wide range of acoustic stimuli in extremely large auditory receptive fields. The physiological properties of suprageniculate nucleus cells strongly resemble the sensory properties of cells found along the ventral bank of the anterior ectosylvian sulcus and the deeper layers of the superior colliculus. Our results provide further support for the notion of a separate tecto-suprageniculate-anterior ectosylvian sulcus/insular pathway that takes part in the processing of multimodal signals important for various types of sensory related behaviours.

[1]  T C Yin,et al.  Responses of neurons in the cat's superior colliculus to acoustic stimuli. I. Monaural and binaural response properties. , 1985, Journal of neurophysiology.

[2]  J. Wepsic,et al.  Multimodal sensory activation of cells in the magnocellular medial geniculate nucleus. , 1966, Experimental neurology.

[3]  B E Stein,et al.  Relationship between visual and tactile representations in cat superior colliculus. , 1976, Journal of neurophysiology.

[4]  B. Stein,et al.  Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. , 1986, Journal of neurophysiology.

[5]  B. V. Updyke,et al.  Retinotopic organization within the lateral posterior complex of the cat , 1989, The Journal of comparative neurology.

[6]  D. Irvine,et al.  Auditory response properties of neurons in the anterior ectosylvian sulcus of the cat , 1986, Brain Research.

[7]  D B Lindsley,et al.  Polysensory responses and sensory interaction in pulvinar and related postero-lateral thalamic nuclei in cat. , 1973, Electroencephalography and clinical neurophysiology.

[8]  M. Armstrong‐James,et al.  Carbon fibre microelectrodes , 1979, Journal of Neuroscience Methods.

[9]  Visual properties of neurons in the suprageniculate nucleus of the cat , 1984, Neuroscience Letters.

[10]  P. O. Bishop,et al.  Some quantitative aspects of the cat's eye: axis and plane of reference, visual field co‐ordinates and optics , 1962, The Journal of physiology.

[11]  W. R. Webster,et al.  Medial geniculate body of the cat: organization and responses to tonal stimuli of neurons in ventral division. , 1972, Journal of neurophysiology.

[12]  L. Aitkin,et al.  Medial geniculate body of the cat: responses to tonal stimuli of neurons in medial division. , 1973, Journal of neurophysiology.

[13]  C. Olson,et al.  Ectosylvian visual area of the cat: Location, retinotopic organization, and connections , 1987, The Journal of comparative neurology.

[14]  L. Chalupa,et al.  Multiple pathways from the superior colliculus to the extrageniculate visual thalamus of the cat , 1988, The Journal of comparative neurology.

[15]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[16]  Lennart Heimer,et al.  Simultaneous demonstration of horseradish peroxidase and acetylcholinesterase , 1976, Neuroscience Letters.

[17]  J. C. Middlebrooks,et al.  A neural code for auditory space in the cat's superior colliculus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  N. Matsumoto,et al.  Characteristics of tooth pulp-driven neurons in the posterior group of the cat thalamus , 1988, Neuroscience Letters.

[19]  Yasuhiko Tamai,et al.  Sensory response of cortical neurons in the anterior ectosylvian sulcus, including the area evoking eye movement , 1992, Brain Research.

[20]  H. Vanegas,et al.  Comparative neurology of the optic tectum , 1984 .

[21]  T. Hicks,et al.  Modality specificity of neuronal responses within the cat's insula. , 1988, Journal of neurophysiology.

[22]  Mountcastle Vb,et al.  A study of the functional contributions of the lemniscal and spinothalamic systems to somatic sensibility. Central nervous mechanisms in pain. , 1960 .

[23]  H. Harlow,et al.  The History and Philosophy of Knowledge of the Brain and its Functions , 1960, Neurology.

[24]  M. Meulders,et al.  Visual properties of neurons in pulvinar, nucleus lateralis posterior and nucleus suprageniculatus thalami in the cat. I. Qualitative investigation. , 1972, Brain research.

[25]  Steiner Be Development and organization of multimodal representation in cat superior colliculus. , 1978 .

[26]  O D Creutzfeldt,et al.  Anterior ectosylvian visual area (AEV) of the cat: physiological properties. , 1988, Progress in brain research.

[27]  C. J. Heath,et al.  An experimental study of ascending connections from the posterior group of thalamic nuclei in the cat , 1971, The Journal of comparative neurology.

[28]  C. Trevarthen,et al.  Two mechanisms of vision in primates , 1968, Psychologische Forschung.

[29]  G. Benedek,et al.  Physiological properties of visually responsive neurones in the insular cortex of the cat , 1986, Neuroscience Letters.

[30]  D. Irvine,et al.  Auditory response properties of neurons in deep layers of cat superior colliculus. , 1983, Journal of neurophysiology.

[31]  T. Hicks,et al.  Origins of afferents to visual suprageniculate nucleus of the cat , 1986, The Journal of comparative neurology.

[32]  E. Miyashita,et al.  Subcortical connections of an ‘oculomotor’ region in the ventral bank of the anterior ectosylvian sulcus in the cat , 1989, Neuroscience Research.

[33]  G. Benedek,et al.  Organization of the colliculo‐suprageniculate pathway in the cat: A wheat germ agglutinin‐horseradish peroxidase study , 1995, The Journal of comparative neurology.

[34]  B. Gordon,et al.  Receptive fields in deep layers of cat superior colliculus. , 1973, Journal of neurophysiology.

[35]  Yasuhiko Tamai,et al.  Eye movements following cortical stimulation in the ventral bank of the anterior ectosylvian sulcus of the cat , 1989, Neuroscience Research.

[36]  Giancarlo Tassinari,et al.  Visual and somatosensory integration in the anterior ectosylvian cortex of the cat , 1987, Brain Research.

[37]  W Singer,et al.  Metabolic mapping of visual areas in the behaving cat: A[14C]2‐deoxyglucose study , 1995, The Journal of comparative neurology.

[38]  C R Olson,et al.  An outlying visual area in the cerebral cortex of the cat. , 1983, Progress in brain research.

[39]  Y. Katoh,et al.  Bilateral projections from the superior colliculus to the suprageniculate nucleus in the cat: A WGA-HRP/double fluorescent tracing study , 1995, Brain Research.

[40]  K. Berkley Response properties of cells in ventrobasal and posterior group nuclei of the cat. , 1973, Journal of neurophysiology.

[41]  Barbara G. Wickelgren,et al.  Superior Colliculus: Some Receptive Field Properties of Bimodally Responsive Cells , 1971, Science.

[42]  T. Hicks,et al.  Organization and properties of neurons in a visual area within the insular cortex of the cat. , 1988, Journal of neurophysiology.

[43]  K. Sanderson,et al.  The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat , 1971, The Journal of comparative neurology.

[44]  J. K. Harting,et al.  The Mammalian Superior Colliculus: Studies of Its Morphology and Connections , 1984 .

[45]  T. Hicks,et al.  The visual insular cortex of the cat: organization, properties and modality specificity. , 1988, Progress in brain research.