Translaminar differentiation of visually guided behaviors revealed by restricted cerebral cooling deactivation.

The purpose of the present study was to test the hypothesis that superficial and deep layers within a single cerebral region influence cerebral functions and behaviors in different ways. For this test, we selected posterior middle suprasylvian (pMS) sulcal cortex of the cat, a suspected homolog of the area V5 complex of primates, because the region has been implicated in several visually guided behaviors. Cats were trained on three tasks: (1) discrimination of direction of motion; (2) discrimination of static patterns partially obscured by static or moving masks; and (3) visual detection and orienting. Cooling of cryoloops in contact with pMS sulcal cortex to 8+/-1 degrees C selectively and completely impaired performance on the two motion discrimination tasks (1 and 2), while leaving the detection and orienting task (task 3) unimpaired. Further cooling to 3 degrees C resulted in an additional complete impairment of task 3. The 8 degrees C temperature resulted in silencing of neuronal activity in the supragranular layers (I-III) and the 3 degrees C temperature silenced activity throughout the thickness of pMS sulcal cortex. The variation in behavioral performance with covariation of cryoloop temperature and vertical, but not lateral, spread of deactivation shows that deactivation of superficial cerebral layers alone was sufficient to completely impair performance on the two motion discrimination tasks, whereas additional deactivation of the deep layers was essential to block performance on the detection and orienting task. Thus, these results show a functional bipartite division of labor between upper and lower cortical layers that is supported by efferent connectional anatomy. Similar bipartite division into upper and lower layers may be a general feature of cerebral cortical architecture, signal processing and guidance of behavior.

[1]  B. Stein,et al.  The Merging of the Senses , 1993 .

[2]  M. Stryker,et al.  Physiological evidence that the 2-deoxyglucose method reveals orientation columns in cat visual cortex , 1981, Nature.

[3]  L. Sokoloff.  The F.O. Schmitt Lecture in Neuroscience 1980. The relationship between function and energy metabolism: its use in the localization of functional activity in the nervous system. , 1981, Neurosciences Research Program bulletin.

[4]  P. Somogyi,et al.  Synaptic organization of cortico‐cortical connections from the primary visual cortex to the posteromedial lateral suprasylvian visual area in the cat , 1991, The Journal of comparative neurology.

[5]  George L. Gerstein,et al.  Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex , 1994, Nature.

[6]  L. Optican,et al.  Cortical feedback increases visual information transmitted by monkey parvocellular lateral geniculate nucleus neurons , 1994, Visual Neuroscience.

[7]  L. Palmer,et al.  The retinotopic organization of lateral suprasylvian visual areas in the cat , 1978, The Journal of comparative neurology.

[8]  John H. R. Maunsell,et al.  Deficits in speed discrimination following lesions of the lateral suprasylvian cortex in the cat , 1989, Visual Neuroscience.

[9]  S G Lomber,et al.  Reversible inactivation of visual processing operations in middle suprasylvian cortex of the behaving cat. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[10]  S. Finger.  Origins of Neuroscience , 1994 .

[11]  L. Sokoloff,et al.  The deoxyglucose method for the measurement of local glucose utilization and the mapping of local functional activity in the central nervous system. , 1981, International review of neurobiology.

[12]  杉山 正章.  The projection of the visual cortex on the Clare-Bishop area in the cat : a degeneration study with the electron microscope , 1979 .

[13]  S G Lomber,et al.  Amplification of thalamic projections to middle suprasylvian cortex following ablation of immature primary visual cortex in the cat. , 1995, Cerebral cortex.

[14]  G A Orban,et al.  Functional impact of cerebral connections. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Role of corpus callosum in functional organization of cat striate cortex. , 1984, Journal of neurophysiology.

[16]  J. Malpeli,et al.  Cat area 17. I. Pattern of thalamic control of cortical layers. , 1986, Journal of neurophysiology.

[17]  B. Payne,et al.  Transgeniculate signal transmission to middle suprasylvian cortex in intact cats and following early removal of areas 17 and 18: a morphological study , 1997, Experimental Brain Research.

[18]  J. Malpeli.  Activity of cells in area 17 of the cat in absence of input from layer a of lateral geniculate nucleus. , 1983, Journal of neurophysiology.

[19]  B E Stein,et al.  Two visual corticotectal systems in cat. , 1984, Journal of neurophysiology.

[20]  W. James,et al.  The Principles of Psychology. , 1983 .

[21]  B. Payne,et al.  Survival and death of neurons in cortical area PMLS after removal of areas 17, 18, and 19 from cats and kittens. , 1991, Cerebral cortex.

[22]  R. Myers,et al.  Interocular transfer of pattern discrimination in cats following section of crossed optic fibers. , 1955, Journal of comparative and physiological psychology.

[23]  Lotfi B. Merabet,et al.  Motion integration in a thalamic visual nucleus , 1998, Nature.

[24]  S G Lomber,et al.  Removal of two halves restores the whole: Reversal of visual hemineglect during bilateral cortical or collicular inactivation in the cat , 1996, Visual Neuroscience.

[25]  Bertram R Payne,et al.  A method to assess the functional impact of cerebral connections on target populations of neurons , 1999, Journal of Neuroscience Methods.

[26]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[27]  G. Henry,et al.  Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey , 1979, The Journal of comparative neurology.

[28]  H. Sherk.  Visual response properties of cortical inputs to an extrastriate cortical area in the cat , 1989, Visual Neuroscience.

[29]  G. E. Alexander,et al.  Functional development of the dorsolateral prefrontal cortex: An analysis utilizing reversible cryogenic depression , 1978, Brain Research.

[30]  D. Ferster,et al.  Orientation selectivity of thalamic input to simple cells of cat visual cortex , 1996, Nature.

[31]  D. Whitteridge,et al.  Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. , 1984, The Journal of physiology.

[32]  B R Payne,et al.  Functional organization of neurons in cat striate cortex: variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in visual-field map. , 1983, Journal of Neurophysiology.

[33]  Jean Bullier,et al.  The Role of Area 17 in the Transfer of Information to Extrastriate Visual Cortex , 1994 .

[34]  W. Burke,et al.  Areas PMLS and 21a of cat visual cortex: two functionally distinct areas. , 1996, Cerebral cortex.

[35]  B E Stein,et al.  Small lateral suprasylvian cortex lesions produce visual neglect and decreased visual activity in the superior colliculus , 1988, The Journal of comparative neurology.

[36]  H. Sherk,et al.  A reassessment of the lower visual field map in striate-recipient lateral suprasylvian cortex , 1993, Visual Neuroscience.

[37]  S G Lomber,et al.  Perceptual and cognitive visual functions of parietal and temporal cortices in the cat. , 1996, Cerebral cortex.

[38]  C. Gross.  From Imhotep to Hubel and Wiesel , 1997 .

[39]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[40]  S Shipp,et al.  Visuotopic organization of the lateral suprasylvian area and of an adjacent area of the ectosylvian gyrus of cat cortex: A physioligical and connectional study , 1991, Visual Neuroscience.

[41]  H. Sherk.  Location and connections of visual cortical areas in the cat's suprasylvian sulcus , 1986, The Journal of comparative neurology.

[42]  K. Kawamura,et al.  Cells of origin of corticopontine and corticotectal fibers in the medial and lateral banks of the middle suprasylvian sulcus in the cat. An experimental study with the horseradish peroxidase method , 1978, Neuroscience Letters.

[43]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Stephen G Lomber,et al.  The advantages and limitations of permanent or reversible deactivation techniques in the assessment of neural function , 1999, Journal of Neuroscience Methods.

[45]  S G Lomber,et al.  Reversible visual hemineglect. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Michael W. von Grünau,et al.  Visual receptive field properties in the posterior suprasylvian cortex of the cat: A comparison between the areas PMLS and PLLS , 1987, Vision Research.

[47]  C. Gilbert,et al.  The projections of cells in different layers of the cat's visual cortex , 1975, The Journal of comparative neurology.

[48]  B. Payne,et al.  Thalamic and cortical projections to middle suprasylvian cortex of cats: constancy and variation , 1997, Experimental Brain Research.

[49]  L. Palmer,et al.  Projections of the pulvinar-lateral posterior complex to visual cortical areas in the cat , 1981, Neuroscience.

[50]  S G Lomber,et al.  Learning and recall of form discriminations during reversible cooling deactivation of ventral-posterior suprasylvian cortex in the cat. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Stephen G. Lomber,et al.  The cryoloop: an adaptable reversible cooling deactivation method for behavioral or electrophysiological assessment of neural function , 1999, Journal of Neuroscience Methods.

[52]  H. Condé,et al.  Effects of local cooling upon conduction and synaptic transmission. , 1972, Brain research.

[53]  J. Malpeli,et al.  Cat area 17. II. Response properties of infragranular layer neurons in the absence of supragranular layer activity. , 1986, Journal of neurophysiology.

[54]  Stephen G. Lomber,et al.  The spatial relationship between the cerebral cortex and fiber trajectory through the corpus callosum of the cat , 1994, Behavioural Brain Research.

[55]  C. Gilbert.  Laminar differences in receptive field properties of cells in cat primary visual cortex , 1977, The Journal of physiology.

[56]  H. Jasper,et al.  The effect of local cooling upon spontaneous and evoked electrical activity of cerebral cortex. , 1970, Canadian journal of physiology and pharmacology.

[57]  B. Payne,et al.  Functional organization of neurons in cat striate cortex: variations in ocular dominance and receptive-field type with cortical laminae and location in visual field. , 1982, Journal of neurophysiology.

[58]  B R Payne,et al.  Evidence for visual cortical area homologs in cat and macaque monkey. , 1993, Cerebral cortex.

[59]  S Shipp,et al.  Organization of reciprocal connections between area 17 and the lateral suprasylvian area of cat visual cortex , 1991, Visual Neuroscience.

[60]  J. G. Bjaalie,et al.  Distribution of corticopontine neurons in visual areas of the middle suprasylvian sulcus: Quantitative studies in the cat , 1986, Neuroscience.

[61]  June Kawano,et al.  Cortical projections of the parvocellular laminae C of the dorsal lateral geniculate nucleus in the cat: An anterograde wheat germ agglutinin conjugated to horseradish peroxidase study , 1998, The Journal of comparative neurology.