- Email: [email protected]
Chapter 16 Afferent and developmentally inherent mechanisms of form and motion processing in cat extrastriate cortex
M. Norita, T. Bando and B. Stein (Eds.)
Pmgress in Bmin Research. Vol 112 Q 1996
Elsevier Science BV. All rights reserved.
CHAPTER 16
Afferent and developmentally inherent mechanisms of form and motion processing in cat extrastriate cortex Peter D. Spear* Department of PJrchologyand Centerfor Neuroscience, Universi~ of Wiiconsin-Madhn, 1202 West Johnson St., Madison, WI 53706, USA
Introduction Every mammalian species that has been studied has been shown to have multiple extrastriate cortical areas devoted to vision (see Spear, 1991, for a review). Each of these extrastriate areas receives multiple sources of afferent information, including inputs from other visual cortical areas and from several thalamic nuclei. The recipient neurons somehow process and integrate these multiple sources of input to produce their own output visual receptive-field properties. How is this done? That is, how do the recipient neurons use the multiple sources of afferent information? Do they combine specific input receptive-field properties from each afferent source to produce the output receptive-field? Or do some inputs have only modulatory functions that are not reflected in specific output receptive-field properties? During development, do the extrastriate neurons have their receptive-field properties imposed on them by their inputs, or do the neurons themselves have inherent properties that determine their output receptive-field characteristics? For example, if the inputs to extrastriate 'Corresponding author. Tel.: + 1 303 492 7294; fax: 4944, email: [email protected]
+ 303 492
neurons are changed during development, will the output receptive fields also change, or will the neurons use the different inputs to produce the same output receptive-field properties that they normally would have? My laboratory has addressed many of these questions in the course of our studies of the mechanisms of compensation for visual cortex damage in adult cats and newborn kittens. As part of these studies, we have investigated the effects of both acute and long-term removal of inputs from areas 17, 18, and 19 (referred to collectively as visual cortex, or VC) on the receptive-field properties of neurons in the posteromedial lateral suprasylvian (PMLS) extrastriate visual area of cortex. This has allowed us to determine the role of various inputs in the elaboration of PMLS receptive fields in normal adult animals. In addition, it has provided evidence that the development of certain receptivefield properties depends upon intrinsic characteristics of the PMLS neurons, not simply upon the particular inputs to the neurons. Normal motion and form processing in PMLS cortex
It has long been known that PMLS cortex is involved in processing information about stimulus
224
motion. Thus, the vast majority of the neurons are motion sensitive and direction selective. They respond better to moving than to stationary flashing stimuli, and their responses depend upon the direction of stimulus movement (e.g., Hubel and Wiesel, 1969; Wright, 1969; Spear and Baumann, 1975; Turlejski, 1975; Camarda and Rizzolatti, 1976). This direction-selective motion processing can be quite complex. For example, many cells have opponent direction-selectivity between the receptive-field center and surround regions (von Grunau and Frost, 1983). In addition, the direction selectivity extends beyond simple sensitivity to the direction of motion in the frontoparallel plane, and many cells respond differentially to stimuli moving toward or away from the animal (Toyama et al., 1985). PMLS neurons also are sensitive to various aspects of stimulus form. For example, many of the receptive fields have inhibitory surrounds (e.g., Spear and Baumann, 1975; Camarda and Rizzolatti, 19761, which makes the cells sensitive to the size of a stimulus. Tests with sine-wave grating stimuli also demonstrate that PMLS cells are sensitive to the spatial-frequency content of visual stimuli (e.g., Morrone et al., 1986; Zumbroich and Blakemore, 1987; Gizzi et al., 1990; Guido et al., 199ob). However, both the optimal spatial frequencies and the spatial resolutions of PMLS neurons tend to be quite low. Thus, the spatial-frequency sensitivity is very crude compared to that in striate cortex. Recent studies also have shown that PMLS neurons are sensitive to stimulus orientation (Blakemore and Zumbroich, 1987; Hamada, 1987; Gizzi et al., 1990; Danilov et al., 1995a), another aspect of form processing. Like spatial-frequency sensitivity, however, the orientation sensitivity is very crude compared to that of neurons in striate cortex. For example, PMLS cells respond to a much wider range of stimulus orientations than do striate cortex neurons. Thus, normal PMLS neurons are sensitive to stimulus form as well as to stimulus motion and direction. However, the form processing is fairly crude, and the neurons do not appear to be
providing information for detail vision. Correspondingly, the receptive fields tend to be quite large, and the topographic organization of PMLS cortex is quite course (e.g., Spear and Baumann, 1975; Palmer et al., 1978; Zumbroich et al., 1986). These and other properties of PMLS neurons have led to suggestions that PMLS cortex is involved in the processing of image motion, to specialized aspects of attention and orientation, or to the near response (lens accommodation, pupillary constriction, and convergent eye movements) that occurs when an object moves closer to the eyes (see Spear, 1991, for a review). Influence of afferents to PMLS cortex in adults The PMLS cortex receives convergent inputs from several pathways (for reviews see Rosenquist, 1985; Spear, 1985; Bullier, 1986; Dreher, 1986). The main visual inputs are summarized in Fig. 1. There is a direct retinogeniculate pathway to PMLS cortex via the geniculate wing (GW), medial interlaminar nucleus (MINI, and C layers of the dorsal lateral geniculate nucleus (LGN). This pathway includes inputs from LGN Y-cells and W-cells, but not X-cells.A second visual pathway comes from the tectothalamic system. The upper layers of the superior colliculus (SC) project to portions of the LGN, the lateral posterior nucleus (Lp), and the posterior nucleus (PN) of the thalamus that project to PMLS cortex. A third pathway consists of a projection from the pretectal nucleus of the optic tract (PRE-TECD to portions of the LGN and pulvinar (PUL) that project to PMLS cortex. PMLS cortex also receives direct corticocortical inputs from areas 17, 18, and 19 of both hemispheres and from a variety of other extrastriate cortical areas. Unlike areas 17 and 18 (Fig. 1, right), PMLS cortex does not receive projections from layers A and A1 of the E N . If one surgically removes the inputs from ipsilateral visual cortex (areas 17, 18, and 19). the receptive-field properties of PMLS cells change dramatically. As shown in Fig. 2 (cf. A and B), the percentage of direction-selective cells decreases
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Fig. 1. Diagrams showing the 'primary' retino-geniculo-cortical pathways to areas 17,18, and 19 (right) and the projections to the posteromedial lateral suprasylvian (LS) extrastriate visual area of cortex (left). A and A1 refer to the corresponding layers of the dorsal lateral geniculate nucleus (LGN). C refers to the C complex of the LGN, which includes four hidden layers (C, C1, C2,and C3).MIN, medial interlaminar nucleus. GW, geniculate wing. LP, lateral posterior nucleus. PUL, pulvinar nucleus. PN, posterior nucleus. SC, superior colliculus. PRE-TECT, pretectal nuclei.
from about 80% of the responsive cells in normal cats to about 20% in cats with ipsilateral VC inputs removed. This decrease is accompanied by an increase in the percentage of cells that respond best to moving stimuli but lack direction selectivity (cells in the movement-sensitive class). However, the increase in movement-sensitive cells corresponds to only about half of the decrease in direction-selective cells. There also is an increase in the percentage of cells that respond as well to stationary flashed stimuli as to stimulus movement (stationary class). Thus, the VC removal appears to produce a reduction in both direction selectivity and movement sensitivity. These effects occur within hours of removing inputs from ipsilateral VC, and no further changes occur during a period of more than a year after the lesion. Thus, the effects are due to removal of inputs from VC and not to secondary consequences of the lesion, such as retrograde degeneration in the thalamus or in PMLS cortex itself (which projects back to areas 17, 18, and 19).
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Fig. 2. Summary of acute and long-term effects of adult VC removal on the receptive-field properties of PMLS neurons. Panels show the percentages of PMLS cells with different receptive-field properties in normal cats (A) and cats with or bilateral (D) removal of ipsilateral (B), contralateral (0, areas 17, 18, and 19. Cross-hatched portions of each bar are results from cats studied within a day of the cortical lesion (acute lesion). Open portions of each bar are results from cats studied 2 weeks to more than a year after the lesion (long-term lesion). N is the number of cells in each condition. Receptive-field classes are: D, direction selective; M, movement sensitive; s, stationary; I, indefinite. Data in A are combined from Spear and Baumann (1979, Smith and Spear (1979). Spear et al. (19851, and McCall et al. (1988). Data in B are combined from Spear and Baumann (1979a1, Spear et al. (1980,19881, and Tong et al. (1984). Data in C are from Spear and Baumann (1979a). Data in D are combined from Spear and Baumann (1979a,b) and Spear et al. (1988). Figure from Spear (1988).
Fig. 2C shows that unilateral VC removal has little or no effect on the receptive-field properties of the PMLS neurons in the contralateral hemisphere. In addition, bilateral removal of VC produces effects that are very similar to ipsilateral
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removal (Fig. 2D). Other studies have shown that similar effects are produced by removal of inputs from areas 17 and 18, and that removal of inputs from area 19 has little or no effect on the properties that have been studied (Spear and Baumann, 1979a; Spear, 1988). Removing inputs from ipsilateral VC also affects the orientation sensitivity of PMLS neurons (Danilov et al., 1995a,b). In normal cats, approximately 70% of responsive PMLS cells are orientation sensitive to a grating stimulus independent of the spatial phase of the grating. Following removal of ipsilateral VC inputs, only about 15% of the cells are orientation sensitive. Thus, orientation sensitivity also depends upon inputs from ipsilateral VC. In contrast, the spatial-frequency tuning properties of PMLS neurons do not depend upon cortico-cortical inputs. Removal of ipsilateral VC has no effect on spatial resolution (see Fig. 4) or the optimal spatial frequency of PMLS neurons (Guido et al., 1990b, 1992). Taken together, the results indicate that in normally reared adult cats, PMLS neurons use inputs from ipsilateral areas 17 and 18 for the elaboration of motion sensitivity, direction selectivity, and orientation selectivity. Many other properties that are not affected by VC removal must therefore be elaborated on the basis of thalamic or other cortical inputs, independent of areas 17, 18, or 19 (see Spear, 1988). These properties include responses to flashed stimuli, receptive-field size, spatial summation, surround inhibition, responses to different stimulus velocities, and spatial-frequency tuning. Some inputs, such as those from the contralateral areas 17, 18, and 19 and ipsilateral area 19, do not appear to be used for receptive-field formation. Presumably, these inputs have modulatory functions that are yet to be studied. Changing the inputs during development
When inputs from ipsilateral areas 17, 18, and 19 are removed on the day of birth, the subsequent development of projections from the thalamus is
altered. This originally was shown by a transneuronal anterograde tracing study in which radioactive tracers were injected into the eye 6 months or more after neonatal VC removal (Tong et al., 1984). This study found an increase in the retinothalamo-cortical projection to PMLS cortex ipsilateral to the neonatal VC lesion. Enhanced projections from thalamus also have been shown by retrograde tracing studies in which tracers were injected into PMLS cortex (Kalil et al., 1991; Lomber et al., 1995). These studies found a 5-10-fold increase in the numbers of C-layer LGN cells that project to PMLS cortex ipsilateral to a neonatal VC lesion. In addition, projections from the LGN A-layers, which are present at birth and normally withdraw and disappear during development (Kato et al., 1986; Bruce and Stein, 1988; Tong et al., 19911, stabilize and remain into adulthood following neonatal removal of VC inputs. No such enhanced projections to PMLS cortex are present following removal of VC in adults, even after long survival times (Tong et al., 1984; Kalil et al., 1991; Lornber et al., 1995). Thus, PMLS cortex cells receive very different inputs in normal adult animals and adult animals that had VC removed at birth. Normal PMLS cells receive inputs from ipsilateral areas 17, 18, and 19, whereas PMLS cells in animals with neonatal VC removal do not. Normal PMLS cells receive weak inputs from the LGN C-layers and none from the A-layers, whereas PMLS cells in animals with neonatal VC removal receive strong inputs from the C-layers and a significant anomalous projection from the A-layers. The question that arises is, How do the receptive-field properties compare in these two groups of PMLS cells with their very different sets of inputs? Fig. 3 shows the results for motion sensitivity and direction selectivity (Spear et al., 1980; see also Tong et al., 1984, 1987; Guido et al., 1990a). Animals that grow up following VC removal at birth have a normal complement of directionselective cells. Moreover, the directional tuning of the direction-selective cells is very similar to that of normal-adult PMLS cells. This is quite differ-
227
ent than what happens after VC removal in adults, where there is a marked reduction in motion and direction sensitivity (Fig. 2). Thus, physiological compensation is seen in PMLS cortex following neonatal VC removal, and the cells develop direction-selective properties like those seen in normal adults.
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Similar results are observed for orientation sensitivity (Danilov, Moore, King and Spear, unpublished). Following VC removal at birth, the animals grow up to have about 42% orientationsensitive cells in PMLS cortex Although this is not as high a percentage as in normal cats (70%), it is higher than in cats with VC inputs removed as adults (15%). Thus, there is a partial compensation of orientation sensitivity in PMLS cortex following neonatal removal of inputs from VC. The orientation tuning is quite broad among the orientation-sensitive cells in cats with a neonatal lesion, just like that in normal adult PMLS cortex. Thus, there is no evidence that the PMLS cells develop sharply tuned orientation sensitivity like that of striate cortex Fig. 4 shows results for spatial resolution. As already noted, neither acute nor long-term removal of VC in adult cats has any effect on the spatial resolution PMLS cells. Very similar results are seen in cats with neonatal removal of VC (Guido et al., 1992). The distribution of spatial resolutions is similar to that in normal PMLS cortex and following adult VC removal. The same results were seen for optimal spatial frequency (Guido et al., 1992). Conclusions
RECEPTIVE FIELD
DIRECTIONAL RANGE (DEGREES) Fig. 3. Summary of the long-term effects of neonatal VC removal on receptive-field properties of PMLS neurons. Pan-
els on the left show the percentages of PMLS cells with different receptive-field properties. Receptive-field classes are: D, direction selective; M,movement sensitive; S, stationaly; I, indefinite. Panels on the right show the directional tuning for direction-selective cells in each condition. The total range of directions of stimulus movement to which each cell responded is shown on the abscissa. N is the number of cells studied. Top shows the results in normal adult cats; bottom shows results from adult cats that had received a VC lesion on the day of birth. Data from Smith and Spear (19791, Spear and Baumann (1975) and Spear et al. (1980).
Fig. 5 presents a simplified summary of the results and conclusions. In normal adult cats, PMLS neurons respond selectively to stimulus motion (MS), direction (DS), orientation (OS), and spatialfrequency content (SF). The orientation tuning is broad, and spatial resolution and optimal spatial frequency are low. Experiments in which VC is removed in adult cats indicate that the motion, direction, and orientation sensitivities are elaborated on the basis of inputs from ipsilateral areas 17 and 18. The spatial-frequency tuning is elaborated on the basis of remaining inputs, perhaps those from the C-layers of the LGN. Removal of ipsilateral area 19 and contralateral areas 17,18, and 19 have no obvious effect on the
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Acknowledgements
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The research reported here was supported by USPHS Grant EY01916.
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receptive-fields of PMLS neurons, and their roles remain a mystery. Following neonatal VC damage, PMLS cells have markedly different inputs than in normal adults. They are missing their ipsilateral inputs from areas 17, 18, and 19, they have heavier than normal inputs from the LGN C-layers, and they have anomalous inputs from the LGN A-layers. Yet the receptive-field properties of the neurons are virtually identical to those of PMLS neurons in normal adult cats. The properties that are lost following adult VC removal are present after neonatal VC removal. mually important, the cells have not developed anomalous properties, such as the narrow orientation tuning or high spatialfrequency sensitivity that are characteristic of the striate cortex neurons that were removed. This is so even though the PMLS cells now receive inputs from the LGN A-layers, which normally project to striate cortex. Thus, the PMLS cells have used a vastly abnormal set of afferents to develop receptive-field properties that are normal for PMLS cells. This suggests that there is something inherent in PMLS cortex that leads neurons to develop particular properties based on whatever inputs are available.
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Fig. 4. Spatial resolution (visual acuity) of PMLS neurons in normal adult cats (NORMAL.), cats that were studied within 1-3 days of a VC lesion that was received as an adult (ADULT ACUTE VC LESION), cats that were studied 2 6 months after a VC lesion received as an adult (ADULT VC LESION), and cats that were studied 2 6 months after a VC lesion received on the day of birth (1 DAY VC LESION). N, number of cells studied in each group of cats. Spatial resolution was defined as the highest spatial frequency (cycles/deg, C/D) to which the cell gave a statistically significant response. Data from Guido et al. (1992).
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MS DS 0 s (broad) SF (low)
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Fig. 5. Simplified diagrams of inputs to posteromedial lateral suprasylvian (PMLS) cortex in normal adult cats, cats with VC removed as adults (Adult VC Lesion), and adult cats that had VC removed on the day of birth (Neonatal VC Lesion). LGN, lateral geniculate nucleus. A, C, the corresponding groups of LGN layers. VC, visual cortex (areas 17, 18, and 19). MS, motion sensitive. DS, direction selective. OS, orientation selective. SF, spatial-frequency sensitive.
References Blakemore, C. and Zumbroich, T.J. (1987) Stimulus selectivity and functional organization in the lateral suprasylvian visual cortex of the cat. J. Physiol., Land., 389 569-603. Bruce, L.L. and Stein, B.E. (1988) Transient projections from the lateral geniculate to the posteromedial lateral suprasylvian visual cortex in kittens. J. Comp.Neurol., 278: 287-302. Bullier, J. (1986) Axonal bifurcation in the afferents to cortical areas of the visual system. In: J.D. Pettigrew, KJ. Sanderson and W.R. Levick (Eds.), Visual Neuroscience, Cambridge University Press, Cambridge, pp. 239-259. Camarda, R. and Rizzolatti, G. (1976) Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat. Bmin Res., 101: 427-443. Danilov, Y.,Moore, R.J., King, V.R. and Spear, P.D. (1995a) Are neurons in cat posteromedial lateral suprasylvian visual cortex orientation sensitive? Tests with bars and gratings. Vwual Neurosci., 12: 141-151. Danilov, Y.,Moore, R.J., King, V.R. and Spear, P.D. (1995b) Function of feedback from extrastriate to striate cortex in
the cat: comparison of cooling and lesion effects. SOC. Neurosci Abs., 359.9. Dreher, B. (1986) Thalamocortical and corticocortical interconnections in the cat visual system: relation to the mechanisms of information processing. In: J.D. Pettigrew, K.J. Sanderson and W.R. Levick (Eds.), V~ualNeuroscience, Cambridge University Press, Cambridge, pp. 290-314. Gizzi, M.S., Katz, E., Schumer, R.A. and Movshon, J.A. (1990) Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. J. Neurophysiol.,63: 1529-1543. Guido, W., Spear, P.D. and Tong, L. (1990a) Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens. Eip. Bmin. Res., 83: 219-224. Guido, W., Tong, L. and Spear, P.D. (1990b) Afferent bases of spatial-frequency and temporal-frequency processing, by neurons in the cat’s posteromedial lateral suprasylvian cortex - effects of removing areas 17, 18, and 19. J. Neurophysiol., 64: 1636-1651. Guido, W., Spear, P.D. and Tong, L. (1992) How complete is
230 physiological compensation in extrastriate cortex after visual cortex damage in kittens. Bmin Res., 91: 455-466. Hamada, T. (1987) Neural response to the motion of textures in the lateral suprasylvian area of cats. Behuu. Bmin Res., 25: 175-186. Hubel, D.H. and Wiesel, T.N. (1%9) Visual area of the lateral suprasylvian gym (Clare-Bishop area) of the cat. J. Physiol, land., 202: 251-260. Kalil, R.E., Tong, L. and Spear, P.D. (1991) Thalamic projections to the lateral suprasylvian visual area in cats with neonatal or adult visual cortex damage. J. Comp. N e m l . , 314 512-525. Kato, N., Kawaguchi, S. and Miyata, H. (1986) Postnatal development of afferent projections to the lateral suprasylvian visual area in the cat: An HRP study. J. Comp. Neuml., 252 543-554. Lomber, S.G., MacNeil, M.A. and Payne, B.R. (1995) Amplification of thalamic projections to middle suprasylvian cortex following ablation of immature primary visual cortex in the cat. Cerebml Cortex, 2 166-191. McCall, M.A., Tong, L. and Spear, P.D. (1988) Development of neuronal responses in cat posteromedial lateral suprasylvian visual cortex. Bmin Res., 447: 67-78. Morrone, M.C., Di Stefano, M. and Burr, D.C. (1986) Spatial and temporal properties of neurons of the lateral suprasylvian cortex of the cat. J. Nemphysiol., 5 6 969-986. Palmer, L.A., Rosenquist, A.C. and Tusa, R.J. (1978) The retinotopic organization of lateral suprasylvian visual areas in the cat. J. Comp. Neml., I n 237-256. Rosenquist, A.C. (1985) Connections of visual cortical areas in the cat. In: A. Peters and E.G. Jones (Eds.), Cerebml Cortex, Plenum Publishing Corporation, New York, pp. 81-117. Smith, D.C. and Spear, P.D. (1979) Effects of superior colliculus removal on receptive field properties of neurons in lateral suprasylvian visual area of the cat. J. Neumphysiol., 4 2 57-75. Spear, P.D. (1985) Neural mechanisms of compensation following neonatal cortex damage. In: C.W. Cotman (Ed.), Synaptic Plasticity and Re&hg, Guilford Press, New York, pp. 111-167. Spear, P.D. (1988) Influence of ares 17, 18, and 19 on receptive-field properties of neurons in the cat’s posteromedial lateral suprasylvian visual cortex In: T.P. Hicks and G. Benedek (Eds.), hgress in Bmin Researchr Vuwn within Extmgeniculo-Striate Systems, Elsevier, Amsterdam, pp. 197-210. Spear, P.D. (1991) Functions of Extrastriate Visual Cortex. In A. Leventhal (Ed.), The Neuml Basis of Vim1 Function, Macmillan Press, England pp. 339-370. Spear, P.D. and Baumann, T.P. (1975) Receptive-field characteristics of single neurons in lateral suprasyivian visual area of the cat. J. Newrophysol., 3 8 1403-1420.
m.
Spear, P.D. and Baumann, T.P. (1979) Effects of visual cortex removal on receptive-field properties of neurons in lateral suprasylvian visual area of the cat. J. Neurophysiol., 4 2 31-56. Spear, P.D. and Baumann, T.P. (1979) Neurophysiological mechanisms of recovery from visual cortex damage in cats: Properties of lateral suprasylvian visual area neurons following behavioral recovery. Exp. Bmin Res., 35: 161-176. Spear, P.D., Kalil, R.E. and Tong, L (1980) Functional compensation in lateral suprasylvian visual area following neonatal visual cortex removal in cats. J. Neumphysiol., 43: 851-869. Spear, P.D., Tong, L., McCall, M.A. and Pastemak, T. (1985) Developmentally induced loss of direction-selective neurons in the cat’s lateral suprasylvian visual cortex. Dewl. Bmin Res., 20: 281-285. Spear, P.D., Tong, L. and McCall, M.A. (1988) Functional influence of areas 17, 18, and 19 on lateral suprasylvian cortex in kittens and adult cats: implications for compensation following early visual cortex damage. Bmin Res., 447: 79-91. Tong, L., Kalil, R.E. and Spear, P.D. (1984) Critical periods for functional and anatomical compensation in lateral suprasylvian visual area following removal of visual cortex in cats. J. Nemphysiol.., 5 2 941-960. Tong, L., Spear, P.D. and Kalil, R.E. (1987) Effects of corpus callosum section on functional compensation in the posteromedial lateral suprasylvian visual area after early visual cortex damage in cats. J. C o w . Neuml., 256 128-136. Tong, L,Kalil, R.E. and Spear, P.D. (1991) Development of thalamic projections to the cat’s lateral suprasylvian visual area of cortex. J. Comp. Neurol., 314: 526-533. Toyama. K., Komatsu, Y., Kasai, H., Fujii, K. and Umetani, K. (1985) Responsiveness of Clare-Bishop neurons to visual cues associated with motion of a visual stimulus in three-dimensional space. Vuwn Res., 25: 407-414. Turlejski, K. (1975) Visual responses of neurons in the ClareBishop area of the cat. Act. NeurobioL Exp., 35: 189-208. von Grunau, M. and Frost, B.J. (1983) Double-opponent-prcF cess mechanism underlying RF-structure of directionally specific cells of cat lateral suprasylvian visual area. 4. Bmin Res., 4 9 84-92. Wright, M.J. (1969) Visual receptive fields of cells in a cortical area remote from the striate cortex in the cat. Nuture, 223: 973-975. Zumbroich, T.J. and Blakemore, C. (1987) Spatial and temporal selectivity in the suprasylvian visual cortex of the cat. 1. Nemsci., 7: 482-500. Zumbroich, T.J., von Grunau, M., Poulin, C. and Blakemore, C. (1986) Differences of visual field representation in the medial and lateral banks of the suprasylvian cortex (PMLS/PLLS) of the cat. Exp. Bmin Res., 64: 77-93.
Pmgress in Bmin Research. Vol 112 Q 1996
Elsevier Science BV. All rights reserved.
CHAPTER 16
Afferent and developmentally inherent mechanisms of form and motion processing in cat extrastriate cortex Peter D. Spear* Department of PJrchologyand Centerfor Neuroscience, Universi~ of Wiiconsin-Madhn, 1202 West Johnson St., Madison, WI 53706, USA
Introduction Every mammalian species that has been studied has been shown to have multiple extrastriate cortical areas devoted to vision (see Spear, 1991, for a review). Each of these extrastriate areas receives multiple sources of afferent information, including inputs from other visual cortical areas and from several thalamic nuclei. The recipient neurons somehow process and integrate these multiple sources of input to produce their own output visual receptive-field properties. How is this done? That is, how do the recipient neurons use the multiple sources of afferent information? Do they combine specific input receptive-field properties from each afferent source to produce the output receptive-field? Or do some inputs have only modulatory functions that are not reflected in specific output receptive-field properties? During development, do the extrastriate neurons have their receptive-field properties imposed on them by their inputs, or do the neurons themselves have inherent properties that determine their output receptive-field characteristics? For example, if the inputs to extrastriate 'Corresponding author. Tel.: + 1 303 492 7294; fax: 4944, email: [email protected]
+ 303 492
neurons are changed during development, will the output receptive fields also change, or will the neurons use the different inputs to produce the same output receptive-field properties that they normally would have? My laboratory has addressed many of these questions in the course of our studies of the mechanisms of compensation for visual cortex damage in adult cats and newborn kittens. As part of these studies, we have investigated the effects of both acute and long-term removal of inputs from areas 17, 18, and 19 (referred to collectively as visual cortex, or VC) on the receptive-field properties of neurons in the posteromedial lateral suprasylvian (PMLS) extrastriate visual area of cortex. This has allowed us to determine the role of various inputs in the elaboration of PMLS receptive fields in normal adult animals. In addition, it has provided evidence that the development of certain receptivefield properties depends upon intrinsic characteristics of the PMLS neurons, not simply upon the particular inputs to the neurons. Normal motion and form processing in PMLS cortex
It has long been known that PMLS cortex is involved in processing information about stimulus
224
motion. Thus, the vast majority of the neurons are motion sensitive and direction selective. They respond better to moving than to stationary flashing stimuli, and their responses depend upon the direction of stimulus movement (e.g., Hubel and Wiesel, 1969; Wright, 1969; Spear and Baumann, 1975; Turlejski, 1975; Camarda and Rizzolatti, 1976). This direction-selective motion processing can be quite complex. For example, many cells have opponent direction-selectivity between the receptive-field center and surround regions (von Grunau and Frost, 1983). In addition, the direction selectivity extends beyond simple sensitivity to the direction of motion in the frontoparallel plane, and many cells respond differentially to stimuli moving toward or away from the animal (Toyama et al., 1985). PMLS neurons also are sensitive to various aspects of stimulus form. For example, many of the receptive fields have inhibitory surrounds (e.g., Spear and Baumann, 1975; Camarda and Rizzolatti, 19761, which makes the cells sensitive to the size of a stimulus. Tests with sine-wave grating stimuli also demonstrate that PMLS cells are sensitive to the spatial-frequency content of visual stimuli (e.g., Morrone et al., 1986; Zumbroich and Blakemore, 1987; Gizzi et al., 1990; Guido et al., 199ob). However, both the optimal spatial frequencies and the spatial resolutions of PMLS neurons tend to be quite low. Thus, the spatial-frequency sensitivity is very crude compared to that in striate cortex. Recent studies also have shown that PMLS neurons are sensitive to stimulus orientation (Blakemore and Zumbroich, 1987; Hamada, 1987; Gizzi et al., 1990; Danilov et al., 1995a), another aspect of form processing. Like spatial-frequency sensitivity, however, the orientation sensitivity is very crude compared to that of neurons in striate cortex. For example, PMLS cells respond to a much wider range of stimulus orientations than do striate cortex neurons. Thus, normal PMLS neurons are sensitive to stimulus form as well as to stimulus motion and direction. However, the form processing is fairly crude, and the neurons do not appear to be
providing information for detail vision. Correspondingly, the receptive fields tend to be quite large, and the topographic organization of PMLS cortex is quite course (e.g., Spear and Baumann, 1975; Palmer et al., 1978; Zumbroich et al., 1986). These and other properties of PMLS neurons have led to suggestions that PMLS cortex is involved in the processing of image motion, to specialized aspects of attention and orientation, or to the near response (lens accommodation, pupillary constriction, and convergent eye movements) that occurs when an object moves closer to the eyes (see Spear, 1991, for a review). Influence of afferents to PMLS cortex in adults The PMLS cortex receives convergent inputs from several pathways (for reviews see Rosenquist, 1985; Spear, 1985; Bullier, 1986; Dreher, 1986). The main visual inputs are summarized in Fig. 1. There is a direct retinogeniculate pathway to PMLS cortex via the geniculate wing (GW), medial interlaminar nucleus (MINI, and C layers of the dorsal lateral geniculate nucleus (LGN). This pathway includes inputs from LGN Y-cells and W-cells, but not X-cells.A second visual pathway comes from the tectothalamic system. The upper layers of the superior colliculus (SC) project to portions of the LGN, the lateral posterior nucleus (Lp), and the posterior nucleus (PN) of the thalamus that project to PMLS cortex. A third pathway consists of a projection from the pretectal nucleus of the optic tract (PRE-TECD to portions of the LGN and pulvinar (PUL) that project to PMLS cortex. PMLS cortex also receives direct corticocortical inputs from areas 17, 18, and 19 of both hemispheres and from a variety of other extrastriate cortical areas. Unlike areas 17 and 18 (Fig. 1, right), PMLS cortex does not receive projections from layers A and A1 of the E N . If one surgically removes the inputs from ipsilateral visual cortex (areas 17, 18, and 19). the receptive-field properties of PMLS cells change dramatically. As shown in Fig. 2 (cf. A and B), the percentage of direction-selective cells decreases
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Fig. 1. Diagrams showing the 'primary' retino-geniculo-cortical pathways to areas 17,18, and 19 (right) and the projections to the posteromedial lateral suprasylvian (LS) extrastriate visual area of cortex (left). A and A1 refer to the corresponding layers of the dorsal lateral geniculate nucleus (LGN). C refers to the C complex of the LGN, which includes four hidden layers (C, C1, C2,and C3).MIN, medial interlaminar nucleus. GW, geniculate wing. LP, lateral posterior nucleus. PUL, pulvinar nucleus. PN, posterior nucleus. SC, superior colliculus. PRE-TECT, pretectal nuclei.
from about 80% of the responsive cells in normal cats to about 20% in cats with ipsilateral VC inputs removed. This decrease is accompanied by an increase in the percentage of cells that respond best to moving stimuli but lack direction selectivity (cells in the movement-sensitive class). However, the increase in movement-sensitive cells corresponds to only about half of the decrease in direction-selective cells. There also is an increase in the percentage of cells that respond as well to stationary flashed stimuli as to stimulus movement (stationary class). Thus, the VC removal appears to produce a reduction in both direction selectivity and movement sensitivity. These effects occur within hours of removing inputs from ipsilateral VC, and no further changes occur during a period of more than a year after the lesion. Thus, the effects are due to removal of inputs from VC and not to secondary consequences of the lesion, such as retrograde degeneration in the thalamus or in PMLS cortex itself (which projects back to areas 17, 18, and 19).
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Fig. 2. Summary of acute and long-term effects of adult VC removal on the receptive-field properties of PMLS neurons. Panels show the percentages of PMLS cells with different receptive-field properties in normal cats (A) and cats with or bilateral (D) removal of ipsilateral (B), contralateral (0, areas 17, 18, and 19. Cross-hatched portions of each bar are results from cats studied within a day of the cortical lesion (acute lesion). Open portions of each bar are results from cats studied 2 weeks to more than a year after the lesion (long-term lesion). N is the number of cells in each condition. Receptive-field classes are: D, direction selective; M, movement sensitive; s, stationary; I, indefinite. Data in A are combined from Spear and Baumann (1979, Smith and Spear (1979). Spear et al. (19851, and McCall et al. (1988). Data in B are combined from Spear and Baumann (1979a1, Spear et al. (1980,19881, and Tong et al. (1984). Data in C are from Spear and Baumann (1979a). Data in D are combined from Spear and Baumann (1979a,b) and Spear et al. (1988). Figure from Spear (1988).
Fig. 2C shows that unilateral VC removal has little or no effect on the receptive-field properties of the PMLS neurons in the contralateral hemisphere. In addition, bilateral removal of VC produces effects that are very similar to ipsilateral
226
removal (Fig. 2D). Other studies have shown that similar effects are produced by removal of inputs from areas 17 and 18, and that removal of inputs from area 19 has little or no effect on the properties that have been studied (Spear and Baumann, 1979a; Spear, 1988). Removing inputs from ipsilateral VC also affects the orientation sensitivity of PMLS neurons (Danilov et al., 1995a,b). In normal cats, approximately 70% of responsive PMLS cells are orientation sensitive to a grating stimulus independent of the spatial phase of the grating. Following removal of ipsilateral VC inputs, only about 15% of the cells are orientation sensitive. Thus, orientation sensitivity also depends upon inputs from ipsilateral VC. In contrast, the spatial-frequency tuning properties of PMLS neurons do not depend upon cortico-cortical inputs. Removal of ipsilateral VC has no effect on spatial resolution (see Fig. 4) or the optimal spatial frequency of PMLS neurons (Guido et al., 1990b, 1992). Taken together, the results indicate that in normally reared adult cats, PMLS neurons use inputs from ipsilateral areas 17 and 18 for the elaboration of motion sensitivity, direction selectivity, and orientation selectivity. Many other properties that are not affected by VC removal must therefore be elaborated on the basis of thalamic or other cortical inputs, independent of areas 17, 18, or 19 (see Spear, 1988). These properties include responses to flashed stimuli, receptive-field size, spatial summation, surround inhibition, responses to different stimulus velocities, and spatial-frequency tuning. Some inputs, such as those from the contralateral areas 17, 18, and 19 and ipsilateral area 19, do not appear to be used for receptive-field formation. Presumably, these inputs have modulatory functions that are yet to be studied. Changing the inputs during development
When inputs from ipsilateral areas 17, 18, and 19 are removed on the day of birth, the subsequent development of projections from the thalamus is
altered. This originally was shown by a transneuronal anterograde tracing study in which radioactive tracers were injected into the eye 6 months or more after neonatal VC removal (Tong et al., 1984). This study found an increase in the retinothalamo-cortical projection to PMLS cortex ipsilateral to the neonatal VC lesion. Enhanced projections from thalamus also have been shown by retrograde tracing studies in which tracers were injected into PMLS cortex (Kalil et al., 1991; Lomber et al., 1995). These studies found a 5-10-fold increase in the numbers of C-layer LGN cells that project to PMLS cortex ipsilateral to a neonatal VC lesion. In addition, projections from the LGN A-layers, which are present at birth and normally withdraw and disappear during development (Kato et al., 1986; Bruce and Stein, 1988; Tong et al., 19911, stabilize and remain into adulthood following neonatal removal of VC inputs. No such enhanced projections to PMLS cortex are present following removal of VC in adults, even after long survival times (Tong et al., 1984; Kalil et al., 1991; Lornber et al., 1995). Thus, PMLS cortex cells receive very different inputs in normal adult animals and adult animals that had VC removed at birth. Normal PMLS cells receive inputs from ipsilateral areas 17, 18, and 19, whereas PMLS cells in animals with neonatal VC removal do not. Normal PMLS cells receive weak inputs from the LGN C-layers and none from the A-layers, whereas PMLS cells in animals with neonatal VC removal receive strong inputs from the C-layers and a significant anomalous projection from the A-layers. The question that arises is, How do the receptive-field properties compare in these two groups of PMLS cells with their very different sets of inputs? Fig. 3 shows the results for motion sensitivity and direction selectivity (Spear et al., 1980; see also Tong et al., 1984, 1987; Guido et al., 1990a). Animals that grow up following VC removal at birth have a normal complement of directionselective cells. Moreover, the directional tuning of the direction-selective cells is very similar to that of normal-adult PMLS cells. This is quite differ-
227
ent than what happens after VC removal in adults, where there is a marked reduction in motion and direction sensitivity (Fig. 2). Thus, physiological compensation is seen in PMLS cortex following neonatal VC removal, and the cells develop direction-selective properties like those seen in normal adults.
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Similar results are observed for orientation sensitivity (Danilov, Moore, King and Spear, unpublished). Following VC removal at birth, the animals grow up to have about 42% orientationsensitive cells in PMLS cortex Although this is not as high a percentage as in normal cats (70%), it is higher than in cats with VC inputs removed as adults (15%). Thus, there is a partial compensation of orientation sensitivity in PMLS cortex following neonatal removal of inputs from VC. The orientation tuning is quite broad among the orientation-sensitive cells in cats with a neonatal lesion, just like that in normal adult PMLS cortex. Thus, there is no evidence that the PMLS cells develop sharply tuned orientation sensitivity like that of striate cortex Fig. 4 shows results for spatial resolution. As already noted, neither acute nor long-term removal of VC in adult cats has any effect on the spatial resolution PMLS cells. Very similar results are seen in cats with neonatal removal of VC (Guido et al., 1992). The distribution of spatial resolutions is similar to that in normal PMLS cortex and following adult VC removal. The same results were seen for optimal spatial frequency (Guido et al., 1992). Conclusions
RECEPTIVE FIELD
DIRECTIONAL RANGE (DEGREES) Fig. 3. Summary of the long-term effects of neonatal VC removal on receptive-field properties of PMLS neurons. Pan-
els on the left show the percentages of PMLS cells with different receptive-field properties. Receptive-field classes are: D, direction selective; M,movement sensitive; S, stationaly; I, indefinite. Panels on the right show the directional tuning for direction-selective cells in each condition. The total range of directions of stimulus movement to which each cell responded is shown on the abscissa. N is the number of cells studied. Top shows the results in normal adult cats; bottom shows results from adult cats that had received a VC lesion on the day of birth. Data from Smith and Spear (19791, Spear and Baumann (1975) and Spear et al. (1980).
Fig. 5 presents a simplified summary of the results and conclusions. In normal adult cats, PMLS neurons respond selectively to stimulus motion (MS), direction (DS), orientation (OS), and spatialfrequency content (SF). The orientation tuning is broad, and spatial resolution and optimal spatial frequency are low. Experiments in which VC is removed in adult cats indicate that the motion, direction, and orientation sensitivities are elaborated on the basis of inputs from ipsilateral areas 17 and 18. The spatial-frequency tuning is elaborated on the basis of remaining inputs, perhaps those from the C-layers of the LGN. Removal of ipsilateral area 19 and contralateral areas 17,18, and 19 have no obvious effect on the
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Acknowledgements
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The research reported here was supported by USPHS Grant EY01916.
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receptive-fields of PMLS neurons, and their roles remain a mystery. Following neonatal VC damage, PMLS cells have markedly different inputs than in normal adults. They are missing their ipsilateral inputs from areas 17, 18, and 19, they have heavier than normal inputs from the LGN C-layers, and they have anomalous inputs from the LGN A-layers. Yet the receptive-field properties of the neurons are virtually identical to those of PMLS neurons in normal adult cats. The properties that are lost following adult VC removal are present after neonatal VC removal. mually important, the cells have not developed anomalous properties, such as the narrow orientation tuning or high spatialfrequency sensitivity that are characteristic of the striate cortex neurons that were removed. This is so even though the PMLS cells now receive inputs from the LGN A-layers, which normally project to striate cortex. Thus, the PMLS cells have used a vastly abnormal set of afferents to develop receptive-field properties that are normal for PMLS cells. This suggests that there is something inherent in PMLS cortex that leads neurons to develop particular properties based on whatever inputs are available.
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Fig. 4. Spatial resolution (visual acuity) of PMLS neurons in normal adult cats (NORMAL.), cats that were studied within 1-3 days of a VC lesion that was received as an adult (ADULT ACUTE VC LESION), cats that were studied 2 6 months after a VC lesion received as an adult (ADULT VC LESION), and cats that were studied 2 6 months after a VC lesion received on the day of birth (1 DAY VC LESION). N, number of cells studied in each group of cats. Spatial resolution was defined as the highest spatial frequency (cycles/deg, C/D) to which the cell gave a statistically significant response. Data from Guido et al. (1992).
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Fig. 5. Simplified diagrams of inputs to posteromedial lateral suprasylvian (PMLS) cortex in normal adult cats, cats with VC removed as adults (Adult VC Lesion), and adult cats that had VC removed on the day of birth (Neonatal VC Lesion). LGN, lateral geniculate nucleus. A, C, the corresponding groups of LGN layers. VC, visual cortex (areas 17, 18, and 19). MS, motion sensitive. DS, direction selective. OS, orientation selective. SF, spatial-frequency sensitive.
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the cat: comparison of cooling and lesion effects. SOC. Neurosci Abs., 359.9. Dreher, B. (1986) Thalamocortical and corticocortical interconnections in the cat visual system: relation to the mechanisms of information processing. In: J.D. Pettigrew, K.J. Sanderson and W.R. Levick (Eds.), V~ualNeuroscience, Cambridge University Press, Cambridge, pp. 290-314. Gizzi, M.S., Katz, E., Schumer, R.A. and Movshon, J.A. (1990) Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. J. Neurophysiol.,63: 1529-1543. Guido, W., Spear, P.D. and Tong, L. (1990a) Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens. Eip. Bmin. Res., 83: 219-224. Guido, W., Tong, L. and Spear, P.D. (1990b) Afferent bases of spatial-frequency and temporal-frequency processing, by neurons in the cat’s posteromedial lateral suprasylvian cortex - effects of removing areas 17, 18, and 19. J. Neurophysiol., 64: 1636-1651. Guido, W., Spear, P.D. and Tong, L. (1992) How complete is
230 physiological compensation in extrastriate cortex after visual cortex damage in kittens. Bmin Res., 91: 455-466. Hamada, T. (1987) Neural response to the motion of textures in the lateral suprasylvian area of cats. Behuu. Bmin Res., 25: 175-186. Hubel, D.H. and Wiesel, T.N. (1%9) Visual area of the lateral suprasylvian gym (Clare-Bishop area) of the cat. J. Physiol, land., 202: 251-260. Kalil, R.E., Tong, L. and Spear, P.D. (1991) Thalamic projections to the lateral suprasylvian visual area in cats with neonatal or adult visual cortex damage. J. Comp. N e m l . , 314 512-525. Kato, N., Kawaguchi, S. and Miyata, H. (1986) Postnatal development of afferent projections to the lateral suprasylvian visual area in the cat: An HRP study. J. Comp. Neuml., 252 543-554. Lomber, S.G., MacNeil, M.A. and Payne, B.R. (1995) Amplification of thalamic projections to middle suprasylvian cortex following ablation of immature primary visual cortex in the cat. Cerebml Cortex, 2 166-191. McCall, M.A., Tong, L. and Spear, P.D. (1988) Development of neuronal responses in cat posteromedial lateral suprasylvian visual cortex. Bmin Res., 447: 67-78. Morrone, M.C., Di Stefano, M. and Burr, D.C. (1986) Spatial and temporal properties of neurons of the lateral suprasylvian cortex of the cat. J. Nemphysiol., 5 6 969-986. Palmer, L.A., Rosenquist, A.C. and Tusa, R.J. (1978) The retinotopic organization of lateral suprasylvian visual areas in the cat. J. Comp. Neml., I n 237-256. Rosenquist, A.C. (1985) Connections of visual cortical areas in the cat. In: A. Peters and E.G. Jones (Eds.), Cerebml Cortex, Plenum Publishing Corporation, New York, pp. 81-117. Smith, D.C. and Spear, P.D. (1979) Effects of superior colliculus removal on receptive field properties of neurons in lateral suprasylvian visual area of the cat. J. Neumphysiol., 4 2 57-75. Spear, P.D. (1985) Neural mechanisms of compensation following neonatal cortex damage. In: C.W. Cotman (Ed.), Synaptic Plasticity and Re&hg, Guilford Press, New York, pp. 111-167. Spear, P.D. (1988) Influence of ares 17, 18, and 19 on receptive-field properties of neurons in the cat’s posteromedial lateral suprasylvian visual cortex In: T.P. Hicks and G. Benedek (Eds.), hgress in Bmin Researchr Vuwn within Extmgeniculo-Striate Systems, Elsevier, Amsterdam, pp. 197-210. Spear, P.D. (1991) Functions of Extrastriate Visual Cortex. In A. Leventhal (Ed.), The Neuml Basis of Vim1 Function, Macmillan Press, England pp. 339-370. Spear, P.D. and Baumann, T.P. (1975) Receptive-field characteristics of single neurons in lateral suprasyivian visual area of the cat. J. Newrophysol., 3 8 1403-1420.
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Spear, P.D. and Baumann, T.P. (1979) Effects of visual cortex removal on receptive-field properties of neurons in lateral suprasylvian visual area of the cat. J. Neurophysiol., 4 2 31-56. Spear, P.D. and Baumann, T.P. (1979) Neurophysiological mechanisms of recovery from visual cortex damage in cats: Properties of lateral suprasylvian visual area neurons following behavioral recovery. Exp. Bmin Res., 35: 161-176. Spear, P.D., Kalil, R.E. and Tong, L (1980) Functional compensation in lateral suprasylvian visual area following neonatal visual cortex removal in cats. J. Neumphysiol., 43: 851-869. Spear, P.D., Tong, L., McCall, M.A. and Pastemak, T. (1985) Developmentally induced loss of direction-selective neurons in the cat’s lateral suprasylvian visual cortex. Dewl. Bmin Res., 20: 281-285. Spear, P.D., Tong, L. and McCall, M.A. (1988) Functional influence of areas 17, 18, and 19 on lateral suprasylvian cortex in kittens and adult cats: implications for compensation following early visual cortex damage. Bmin Res., 447: 79-91. Tong, L., Kalil, R.E. and Spear, P.D. (1984) Critical periods for functional and anatomical compensation in lateral suprasylvian visual area following removal of visual cortex in cats. J. Nemphysiol.., 5 2 941-960. Tong, L., Spear, P.D. and Kalil, R.E. (1987) Effects of corpus callosum section on functional compensation in the posteromedial lateral suprasylvian visual area after early visual cortex damage in cats. J. C o w . Neuml., 256 128-136. Tong, L,Kalil, R.E. and Spear, P.D. (1991) Development of thalamic projections to the cat’s lateral suprasylvian visual area of cortex. J. Comp. Neurol., 314: 526-533. Toyama. K., Komatsu, Y., Kasai, H., Fujii, K. and Umetani, K. (1985) Responsiveness of Clare-Bishop neurons to visual cues associated with motion of a visual stimulus in three-dimensional space. Vuwn Res., 25: 407-414. Turlejski, K. (1975) Visual responses of neurons in the ClareBishop area of the cat. Act. NeurobioL Exp., 35: 189-208. von Grunau, M. and Frost, B.J. (1983) Double-opponent-prcF cess mechanism underlying RF-structure of directionally specific cells of cat lateral suprasylvian visual area. 4. Bmin Res., 4 9 84-92. Wright, M.J. (1969) Visual receptive fields of cells in a cortical area remote from the striate cortex in the cat. Nuture, 223: 973-975. Zumbroich, T.J. and Blakemore, C. (1987) Spatial and temporal selectivity in the suprasylvian visual cortex of the cat. 1. Nemsci., 7: 482-500. Zumbroich, T.J., von Grunau, M., Poulin, C. and Blakemore, C. (1986) Differences of visual field representation in the medial and lateral banks of the suprasylvian cortex (PMLS/PLLS) of the cat. Exp. Bmin Res., 64: 77-93.