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Chapter 20 Potentiation of the extrageniculo-striate pathway: a possible role in visual pattern discrimination
T.P. Hicks, S. Molotchnikoff and T. Ono (Eds.) Progress in Brain Research, Vol. 95 0 1993 Elsevier Science Publishers B . V . All rights reserved
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CHAPTER 20
Potentiation of the extrageniculo-striate pathway: a possible role in visual pattern discrimination Svetlana I. Shumikhina Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the U.S.S.R., 117865 Moscow, U.S.S.R.
Introduction A problem in understanding brain mechanisms that are responsible for discrimination of visual stimuli has a fairly enough history. The pioneering studies of Hubel and Wiesel (1959, 1962, 1965), which allowed to distinguish in the cat primary visual cortex neurons with simple and complex receptive fields (RFs), were a basis for intensive investigations of different authors in this direction. Though different subtypes of RFs were described owing to later studies, the classification of Hubel and Wiesel has remained valid and shall be used throughout this article. As is known, many properties distinguish complex RFs of visual cortical neurons from simple ones as well as from RFs of geniculate neurons. According to Hubel and Wiesel (1962, 1965) simple cells comprise the first stage of cortical information processing while complex cells form the second stage of this process. Complex RFs consist of overlapping on and off areas, unlike simple RFs that consist of separate on and/or off areas, and that have inhibitory flanks in their RFs, which are absent in complex RFs. The size of complex RFs is larger than the size of the simple ones. Complex cells do not respond in linear fashion to activation of different points within their RFs in contrast to simple cells. As a rule, complex cells have some level of spontaneous activity and they are less narrow tuned to the orientation of stimuli. Such cells are more responsive to high velocities of stimulus movement (Hubel and
Wiesel, 1959, 1962, 1965; Henry, 1977; Leventhal and Hirsch, 1978; Supin, 1981; Sherman and Spear, 1982; Orban, 1984). Some properties of complex cells (larger RF, overlapping on and off areas) can be explained by the convergence of afferents of simple cells, as was suggested initially by Hubel and Wiesel, while other properties (spontaneous activity, sensitivity to higher velocities) are not. On the other hand, such properties of complex cells as their spontaneous activity, the larger size of their RFs, a broader orientation tuning and sensitivity to high velocities of moving stimuli as well as to low spatial and high temporal frequencies, can be explained by their having inputs from Y-like geniculate cells (the hypothesis of parallel processing of visual information: Stone, 1972, 1983; Stone and Dreher, 1973; Maffei and Fiorentini, 1973; Sherman and Spear, 1982; Spitzer and Hochstein, 1988). A problem, however, with the above hypothesis is that it does not properly explain other properties of complex RFs, such as for example, the structure of the RFs. Nevertheless, many data exist in conflict with both hypotheses. For example, the fact that some complex cells, like simple ones, receive monosynaptic input from the dorsal lateral geniculate nucleus (LGN) (Hoffmann and Stone, 1971; Bullier and Henry, 1979a,b,c; Tanaka, 1979), contradicts the hierarchical hypothesis of Hubel and Wiesel. The other fact that both simple and complex cells can receive inputs from X- as well as from Y-like geniculate neurons, contradicts the hypothesis of
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parallel processing. Data from experiments in which the antagonist of GABA receptors, bicuculline, was used (KrnjeviC and Schwartz, 1967; Sillito, 1984) showing an enlargement of RFs and a reduction of orientation and directional selectivity in some complex cells (Sillito, 1984; Volgushev, 1989), are not in agreement with both hypotheses, because the data propose a role of intracortical inhibition in the formation of complex RFs. These contradictions can be overcome, if we assume an involvement of an additional source of visual information into the process of the formation of complex RFs, such as input from the pulvinar-lateral posterior (Pulv-LP) complex (in the remaining part of the text, this will be referred to as the pulvinar or Pulv-LP). Arguments in favour of an involvement of pulvinar input in the process of formation of complex receptive fields
There are strong arguments to suppose that Pulv-LP takes part in the formation of complex RFs. My hypothesis, based on the involvement of the pulvinar input in the process of the formation of complex RFs, combines elements of both the hierarchical hypothesis of Hubel and Wiesel and the hypothesis of parallel processing, proposed by other authors (e.g., see Sherman and Spear, 1982; Stone, 1983; Spitzer and Hochstein, 1988), as well as taking into account intracortical inhibition as one of the factors of this process. The hypothesis is based on the following data. (1) The Pulv-LP complex receives direct input from the retina (Itoh et al., 1979; Kawamura et al., 1979; Guillery et al., 1980; Leventhal et al., 1980). The “geniculate wing” (Guillery et al., 1980), a site to which the retina projects is not an extension of the LGN, but it is a part of the pulvinar. This fact derives from the detailed studies of Hutchins and Updyke (1989) that the geniculate wing as well as the medial interlaminar nucleus of the LGN have their own incomplete representations of the visual field. (2) The Pulv-LP complex receives also direct retinotopically organized inputs from other visual
subcortical structures - superior colliculus and pretectum - i.e., from visual structures that receive retinal inputs as well (Kawamura and Kobayashi, 1975; Bermanand Jones, 1977; Graham, 1977; Berson and Graybiel, 1978; Graham and Berman, 1981) and can transmit to the pulvinar complex information from all types (X, Y, W) of ganglion cells of the retina (Godfraind et al., 1972; Hoffmann, 1973; Magalhaes-Castro et al., 1976; Ogawa and Takahashi, 1981; Sawai et al., 1985; Hada and Hayashi, 1990; see also Shumikhina, 1981; Stone, 1983). (3) All neurons of the Pulv-LP are spontaneously active (Mason, 1978), their RFs are larger than the RFs of geniculate neurons; directionally responsive and directionally selective neurons comprise the largest group of visually responsive cells of the PulvLPcomplex(Godfraindet al., 1969; Meuldersetal., 1971; Mason, 1978,1981; Harutiunian-Kozaket al., 1981b; Chalupa and Abramson, 1988). A majority of neurons responds especially well to fast moving stimuli (Mason, 1978). Pulv-LP neurons are revealed that have on/off responses in each point of the RF, as well as those with on or off responses, which have concentric and diffuse RFs and orientation selectivity (Godfraind et al., 1969; Mason, 1978; Harutiunian-Kozak et al., 1981a,b). (4) Under adequate conditions, visual sensitivity can be revealed in all cytoarchitectonic subdivisions of the Pulv-LP complex, and the percentage of visually responsive neurons has been estimated to be as high as 93% (Chalupa et al., 1983; Chalupa and Abramson, 1988; Hutchins and Updyke, 1989). (5) There is a direct input from all subdivisions of the Pulv-LP complex to the striate cortex (Albus et al., 1980; Hughes, 1980; Bullier et al., 1984; Shumikhina, 1990). (6) The Pulv-LP complex projects to layer Ia and to the border of layers IVP and V of area 17 (Miller and Benevento, 1979); i.e., pulvinar input can affect cells of all layers of the visual cortex. Pulvinar afferents establish contacts on thin branches and spines of dendrites and make asymmetric synapses (Adrianov, 1977; Miller and Benevento, 1979). (7) Input from the pulvinar has its own way of cor-
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tical excitation, that differs from the geniculate one (Shumikhina, 1984a). (8) Striate input from Pulv-LP is weaker than input from the LGN (Morillo, 1961; Shumikhina, 1984a; Malpeli et al., 1986). (9) Interaction of pulvinar and geniculate afferent inputs can be revealed in the visual cortex (Morillo, 1961; Shumikhina, 1984b, 1988). (10) Complex cells of the striate cortex are a cortical target for input from the Pulv-LP (Shumikhina and Volgushev, 1989, 1990a,b). (1 1) The visual activity, orientation and directional selectivity of complex cells are spared (although these become weaker) after the complete inactivation of all layers of the LGN and its medial interlaminar nucleus, while the visual activity of simple cells is blocked; additional inactivation of Pulv-LP results in the disappearance of the activity of complex cells (Malpeli, 1983; Malpeli et al., 1986). (12) Changes in efficacy of Pulv-LP input results in a reduction of orientation selectivity of complex cells having both pulvinar and geniculate inputs (Shumikhina and Volgushev, 1990b). I would now like to present in more detail our own data. It is well known that the visual activity of pulvinar neurons is unstable and depends significantly on type and depth of anaesthesia (Chalupa et al., 1983; Chalupa and Abramson, 1988; Hutchins and Updyke, 1989). Due to this factor, we conducted our experiments on awake cats. Recently, I have conducted chronic electrophysiological experiments on alert cats (Shumikhina, 1984a). I have recorded evoked potentials to stimulation of the LGN and the pulvinar, in area 17 of the visual cortex. Responses to stimulation of the pulvinar were recorded at latencies of 2.6 f 0.6 msec and to stimulation of the LGN at latedies of 2.0 f 0.5 msec (see Fig. 1). I did not find any significant difference between these latencies. There were differences in the shape of the evoked potentials to stimulation of these structures. The amplitude of these responses was significantly larger to geniculate stimulation under the same intensity of stimulation, and the latency of
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Fig. 1. Evoked potentials in the visual and association cortex to 1 Hz stimulation of the lateral geniculate nucleus (LGN, 0.3 mA) and pulvinar (Pulv, 0.6 mA) in the alert cat. Averaging from eight presentations; negativity upward. Calibration: 100 FV, 5 msec. (Adapted from Shumikhina, 1984a.)
a negative component N l was significantly shorter to geniculate than pulvinar stimulation (7.2 f 0.8 msecand 13.7 f 1.2msec). WhenIrecordedevoked potentials to paired stimulation of the LGN or the pulvinar, I found significant differences in the way area 17 was activated by inputs from the LGN and the pulvinar (Figs. 2, 3). If there is a strong depression of the test response to paired stimulation of the LGN at short interstimulus intervals and its gradual restoration at longer intervals, the depression of the test response to paired stimulation of the pulvinar is very short, and already at short enough interstimulus intervals (20 - 40 msec) a significant (2-4 times) facilitation of the test response is revealed (Shumikhina, 1984a). Similar facts has been obtained by others (Malis and Kriger, 1956; Schoolman and Evarts, 1959; Demetrescu and Steriade, 1965), but I have conducted a quantitative investigation and have examined recovery cycles of evoked potentials to pulvinar stimulation in unrestrained cats. I have also obtained evidence of interaction of afferent inputs from the pulvinar and the LGN in the striate cortex of awake cats (see
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Fig. 2. Recovery of evoked potentials during paired stimulation of the lateral geniculate nucleus in the visual and association cortex in the alert cat. A . Recovery curves in the association (1) and visual (2) cortex to stimulation of the lateral geniculate nucleus. Abscissa, intervals between test and conditioning stimuli; ordinate, amplitude of response to test stimulation as a percentage of the amplitude of the response to conditioning stimulation. Average data (7 cats, n = 104 for each point). B. Evoked potentials in the association (1) and visual (2) cortex to 1 Hz and paired stimulation of the lateral geniculate nucleus under varied interstimulus intervals (shown at left) in one of the cats. Averaging from eight presentations; negativity upward. Calibration: 100 p V , 50 msec (for lower oscillograms: 100 pV, 5 msec). (Adapted from Shumikhina, 1984a.)
Shumikhina, 1984b, 1988). Convergence of pulvinar and geniculate inputs on single cells in area 17 has also been shown by Morillo (1961). Shumikhina and Volgushev (1989, 1990a,b) showed that in alert cats prepared under local anaesthesia using a long-lasting anaesthetic (lidocaine hydrochloride), 33% of neurons in area 17 responded to electrical stimulation of Pulv-LP and the RFs of those neurons consist of overlapping on and off areas (Fig. 4). These cells can be classified as having complex RFs according to Hubel and Wiesel (1962,1965). We have recorded 46 neurons from 11 cats. Animals were immobilized with Dtubocurarine and artificially respired. Light flash stimuli (rectangles with sides from 0.5 to 3 deg, 21.2
cd/m2, 150 - 200 msec) were presented under conditions of mesopic light adaptation to one eye, while the other eye was closed. The variability of the latency served as the main criterion for orthodromic response. Additional criteria could be provided when we recorded cells in the superficial cortical layers, as it is known that corticogeniculate and corticopulvinar neurons are located in deep (V to VI) layers (Gilbert and Kelly, 1975; Abramson and Chalupa, 1985). We always verified the subcortical placement of the tips of the stimulating electrodes, as it is known that the cortico-reciuient zone is located in a definite region of the Pulv-LP (Updyke, 1977; Berson and Graybiel, 1978). High-frequency stimulation was not used for this purpose because it could affect the properties of cortical neurons. Four groups of neurons in the visual cortex were defined on the basis of presence/absence of input from two
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Fig. 3. Recovery of evoked potentials during paired stimulation of the pulvinar in the visual and association cortex in the alert cat. A . Recovery curves in the visual (2) and association (1) cortex to stimulation of the pulvinar. Average data (14 cats, n = 120 for each point). B. Evoked potentials in the visual (2) and association (1) cortex to 1 Hz and paired stimulation of the pulvinar in one of the cats. Symbols as in Fig. 2. (Adapted from Shumikhina, 1984a.)
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subcortical structures: (1) cells with inputs from Pulv-LP and the LGN (13 cells, 28%); (2) cells with input only from the LGN (10 cells, 22%); (3) cells with input only from Pulv-LP (2 cells, 4v0); and (4) cells non-responsive to electrical stimulation (0.2 msec, 10- 60 V) of these structures (21 cells, 46%). Stimulation of the LGN resulted in the excitation of 50% of cells from the 46 neurons tested, at latencies of 0.8 - 10.8 msec (mean 3.7 k 0.7 msec). Stimulation of the Pulv-LP elicited responses in 33% of the cells at latencies of 0.8 - 10.2 msec (mean 2.9 k 0.6 msec). Pulvinar and geniculate projections are closely connected with each other: 87% of neurons with Pulv-LP input also responded to geniculate stimulation, while 62% of neurons with geniculate input also responded to pulvinar stimulation. We have tested RF properties of 8 cells with both pulvinar andgeniculate inputs, 3 cells with input only from the LGN, and 1 cell with input only from the A
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Fig. 4.Three-dimensional plots of the receptive fields of neurons.
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the pulvinar. Vertical axis: number of spikes in response to presentation of stimuli in each of 100 (10 x 10) points of the visual field; the plane of the plot corresponds to the plane of the screen. (Adapted from Shumikhina and Volgushev, 1990b.)
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Fig. 5 . Orientation selectivity of a neuron with inputs from the pulvinar and the lateral geniculate nucleus. A . Schematic representation of the receptive field (RF). The RF-centre is the point of the maximal neuronal discharge. Solid line, on-response zone; hatched area, off-response zone; cross, centre of gaze; open circle, on centre; black circle, off-centre. B. Orientation tuning curve of the neuron before (dotted line) and after (solid line) high frequency pulvinar stimulation. Abscissa, stimulus orientation in degrees from the horizontal; ordinate, number of spikes in the response as a percentage of maximal. C. Peristimulus time histograms (PSTH) of neuronal responses to flashes presented to the centre of the RF (light bar 3 X 0.5 deg) at different orientations before (left) and after (right) high frequency pulvinar stimulation. Figures near each histogram, orientation of the stimulus. The PSTHs are based on 20 stimulus presentations. (Combined from Shumikhina and Volgushev, 1990b.)
pulvinar. The R F size of 9 neurons with pulvinar input varied from 2 to 54 deg2, and these cells had centres that were located 2 - 17 deg from the gaze. The RF width of 8 cells with both pulvinar and geniculate inputs varied from 1.5 to 8 deg (mean 5 f 1 deg) and their length varied from 1.5 to 12deg (mean 7 k 1 deg). 62% of these neurons were orientation-selective. The width of their orientation tuning curves varied from 22 to 150 deg (mean 82 +_ 13 deg). These neurons preferred horizontal
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stimulus orientations as a rule (75%) (Fig. 5 ) , while neurons with input only from the LGN more often preferred oblique stimulus orientations (this difference was not significant). The RF size of 3 neurons with inputs only from the LGN varied from 9 to 39 deg2, and these cells had centres that were located 2 - 14 deg from the gaze. The RF width of these cells varied from 3 to 8 deg (mean 5 k 1 deg) and their length varied from 3 to 10deg (mean 7 k 1 deg). The RF size of the neuron with input only from the pulvinar composed 24 deg2. The RF width of this neuron composed 6 deg and its length composed 6 deg as well. To test for a possible role of pulvinar input in the formation of complex RFs, we tried to use high-frequency stimulation (200 Hz, 10 sec, 25 V) of the pulvinar before the presentation of stimuli of different orientations. The tetanization resulted in a reduction of the orientation selectivity of complex cells in the visual cortex showing inputs from
Pulv-LP and the LGN (Fig. 5). This reduction was at the expense of a three-fold increase of the response to stimuli opposite to the optimal orientation. There was also a significant intensification (more than two-fold) of responses to stimuli of other orientations. Thus, we have shown that changes in efficacy of pulvinar input result in changes in properties of complex RFs of neurons in area 17, i.e., they evoke adaptive modifications of complex RFs. I would like to propose that pulvinar input tonically excites complex cells. Such tonic excitation is manifested as spontaneous activity in these neurons. The pulvinar input complicates the basic properties of complex RFs having inputs of simple or geniculate cells (see Fig. 6 , for details). As a result, complex cells have RFs of larger size and of broader orientation tuning than simple ones and acquire sensitivity to high velocities. The phasic character of the excitation of complex cells is deter-
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Fig. 6 . Scheme of the organization of complex cell inputs that determine its receptive field properties. A . A pyramidal neuron (PN, complex cell) receiving a monosynaptic pulvinar input and a disynaptic geniculate input (input from simple cell). B. A pyramidal neuron receiving monosynaptic pulvinar and geniculate inputs. SN, a stellate cell; EN, excitatory neuron; IN, inhibitory neuron. Interrupted line, connections that determine “vague” physiological mechanisms, revealed by the method of paired stimuli. Peristimulus time histograms, supposed response of the pyramidal neuron as a result of its excitation by pulvinar and geniculate inputs to optimally oriented stimuli. Here, well-known data are used, such as: (1) the majority of simple cells are located in layer IV of the striate cortex and these are stellate cells as a rule (Kelly and Van Essen, 1974; Bullier and Henry, 1979a,b,c); (2) the majority of complex cells are located in layers I1 + 111, V and VI of the striate cortex and these are pyramidal cells as a rule (Kelly and Van Essen, 1974; Lin et al., 1979); (3) both simple and complex cells can receive mono- as well as diskaaptic geniculate inputs (Hoffmann and Stone, 1971; Toyama et al., 1974; Bullier and Henry, 1979a,b,c; Ferster and Lindstrom, 1983); (4) simple cells can excite and inhibit complex cells as well (Volgushev, 1987,1988); ( 5 ) inhibition can be revealed between cells with both weakly and significantly distinctive preferred orientations (Blakemore and Tobin, 1972; Toyama et al., 1981; Volgushev, 1987).
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mined by inhibitory processes at the level of simple cells, or by input from inhibitory neurons. The adaptivity of complex RFs can be achieved in this case by changes in the efficacy of pulvinar input. These considerations are stated in short by Shumikhina (1991).
Conclusions At first sight it may seem paradoxical that the intensification of the pulvinar input can result in a reduction of the orientation selectivity of complex cells and, consequently, to a worsening of the discrimination of visual patterns. However, behavioural manifestations cannot always follow directly from physiological phenomena. As is known from studies of young animals, simple RFs are experienceinsensitive, while complex RFs possess a certain adaptivity (Hirsch, 1985). Complex cells are higherorder output neurons, which transmit information to other visual cortical areas (Hubel and Wiesel, 1965; Denney et al., 1968; Toyama et al., 1974; Gilbert and Wiesel, 1983), and properties of their RFs are formed later during the course of development (Sherman and Spear, 1982; Hirsch, 1985), but these cells have worse detector characteristics (larger size of RF, broader orientation tuning, a sensitivity to low spatial frequencies) than simple cells. It is hard to believe that this is only by chance. As has beenshown by different authors, the visual responses of Pulv-LP can be increased in situations of interest to visual stimuli, and the activity of Pulv-LP neurons depend on visually evoked eye movements (e.g., see Chalupa, 1977;Fabre-Thorpe et al., 1986). Experiments with lesions of Pulv-LP also have shown that this structure is involved in processes of visual discrimination and attention (Chalupa, 1977; Zihl and Von Cramon, 1979; Fabre-Thorpe et al., 1986). Consequently, it can be concluded from these data that potentiation of pulvinar input has to result in improvement of visual discrimination. I suppose, that the reduction of the orientation selectivity of complex cells after tetanization of the pulvinar input can mean that the selective attention to visual stimuli (our potentiation of pulvinar input may be con-
sidered as a model of this process) actively depresses (masks) some reactions of sign detectors and, as a result, subserves the finer discrimination of visual patterns. The involvement of pulvinar input into the process of the formation of complex RFs can be important for providing the plasticity of cortical reactions.
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Hoffmann, K.-P. (1973)Conduction velocity in pathways from retina to superior colliculus in the cat: a correlation with receptive-field properties. J. Neurophysiol., 36:409 - 424. Hoffmann,K.-P. andstone, J. (1971)Conductionvelocityof afferents to cat visual cortex: a correlation with cortical receptive field properties. Brain Res., 32: 460 - 466. Hubel, D.H. and Wiesel, T.N. (1959)Receptive fields of single neurons in the cat’s striate cortex. J. Physiol. (Lond.), 148: 574- 591. Hubel, D.H. and Wiesel, T.N. (1962)Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J . Physiol. (Lond.), 160: 106- 154. Hubel, D.H. and Wiesel, T.N. (1965)Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. J. Neurophysiol., 28: 229 - 289. Hughes, H.C. (1980)Efferent organization of the cat pulvinar complex, with a note on bilateral claustrocortical and reticulocortical connections. J. Comp. Neurol., 193: 937 - 964. Hutchins, B. and Updyke, B.V. (1989)Retinotopic organization within the lateral posterior complex of the cat. J. Comp. Neurol., 285: 350- 398. Itoh, K., Mizuno, N., Sugimoto, T., Nomura, S., Nakamura, Y. and Konishi, A. (1979)Cerebello-pulvino-corticaland retinopulvino-cortical pathways in the cat as revealed by the use of the anterograde and retrograde transport of horseradish peroxidase. J.Comp. Neurol., 187: 349- 357. Kawamura, S. and Kobayashi, E. (1975) Identification of laminar origin of some tecto-thalamic fibers in the cat. Brain Rex, 91: 281 -285. Kawamura, S., Fukushita, N. and Hattori, S. (1979) Topographical origin and ganglion cell type of the retinopulvinar projection in the cat. Brain Rex, 173: 419-429. Kelly, I.P. and Van Essen, D.C. (1974)Cell structure and function in the visual cortex of the cat. J. Physiol. (Lond.), 238: 515-547. KrnjeviC, K. and Schwartz, S. (1967) The action of 7aminobutyric acid on cortical neurons. Exp. Brain Res., 3: 320 - 336. Leventhal, A.G. and Hirsch, H.V. (1978)Receptive-field properties of neurons in different laminae of the visual cortex of the cat. J. Neurophysiol., 41: 948 -962. Leventhal, A.G., Keens, J. and Tork, I. (1980)The afferent ganglion cells and cortical projections of the retinal recipient zone (RRZ) of the cat’s “pulvinar complex”. J. Comp. Neurol., 194: 535 - 554. Lin, C.-S., Friedlander, M.F. and Sherman S.M. (1979)Morphology of physiologically identified neurons in the visual cortex of the cat. Brain Rex, 172: 344 - 348. Maffei, L. and Fiorentini, A. (1973)The visual cortex as a spatial frequency analyser. Vision Res., 13: 1255 - 1267. Magalhaes-Castro, H.H., Murata, L.A. and Magalhaes-Castro, B. (1976)Cat retinal ganglion cells as shown by the horseradish peroxidase method. Exp. Brain Res., 25: 541 - 549.
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Malis, L.J. and Kriger, L. (1956) Multiple response and excitability of cat’s visual cortex. J. Neurophysiol., 19: 172- 186. Malpeli, J.G. (1983) Activity of cells in area 17 of the cat in absense of input from layer A of lateral geniculate nucleus. J. Neurophysiol., 49: 595 - 610. Malpeli, J.G., Lee, C., Schwark, H.D. and Weyand, T.G. (1986) Cat area 17. I. Pattern of thalamic control of cortical layers. J. Neurophysiol., 56: 1062- 1073. Mason, R. (1978) Functional organization in the cat’s pulvinar complex. Exp. Brain Res., 31: 51 - 66. Mason, R. (1981) Differential responsiveness of cells in the visual zones of the cat’s LP-pulvinar complex to visual stimuli. Exp. Brain Res., 43: 25 - 33. Meulders, M., Veraart, C. and Godfraind, J.M. (1971) Quantitative analysis of visual receptive fields of cells in pulvinar, lateralis posterior and suprageniculatus nuclei in the cat. Brain Res., 31: 372. Miller, J.W. and Benevento, L.A. (1979) Multiple thalamic inputs to primary visual cortex in the monkey and cat. Anat. Rec., 193: 623 - 624. Morillo, A. (1961) Microelectrode analysis of some functional characteristics and inter-relationships of specific, association and non-specific thalamocortical systems. Electroenceph. Clin. Neurophysiol., 13: 9 - 20. Ogawa, T. and Takahashi, Y. (1981) Retinotectal connectivities within the superficial layers of the cat’s superior colliculus. Brain Res., 217: 1 - 11. Orban, G.A. (1984) Neuronal Operations in the Visual Cortex, Springer, Berlin, 368 pp. Sawai, H., Fukuda, Y. and Wakakuma, K. (1985) Axonal projections of X-cells to the superior colliculus nucleus of the optic tract in cats. Brain Rex, 341: 1-6. Schoolman, A. and Evarts, E.V. (1959) Responses to lateral geniculate radiation stimulation in cats with implanted electrodes. J. Neurophysiol., 22: 112- 129. Sherman, S.M. and Spear, P.D. (1982) Organization of visual pathways in normal and visually deprived cats. Physiol. Rev., 62: 138 - 855. Shumikhina, S.I. (1981) Functional Organization of TectoCortical Connections, Nauka, Moscow, 99 pp. Shumikhina, S.I. (1984a) Evoked potentials in the visual and association cortex of alert cats during paired uniform stimulation of the lateral geniculate body and pulvinar. Neurophysiology, 16: 394 -400. Shumikhina, S.I. (1984b) Monomodal convergence in the visual system of waking cats. Zh. Vyssh. Nervn. Deyat. im. I.P.Pavlova, 34: 1128- 1134. Shumikhina, S.I. (1988) Integration of geniculate, pulvinar, and collicular afferent inputs by visual and association cortices of alert cats. Perception, 17: 409. Shumikhina, S.I. (1990) Divergence between axonal collaterals of thalamic neurons running to the cat visual and association cortex. Neurophysiology, 22: 384- 389.
Shumikhina, S.I. (1991) Properties and adaptivity of complex receptive fields may not only be due to intracortical inhibition. Perception, 20: 1 1 1 . Shumikhina, S.I. and Volgushev, M.A. (1989) Receptive-field propert‘ies of cat visual cortex neurons with pulvinar input. Perception, 18: 5 1 1 -512. Shumikhina, S.I. and Volgushev, M.A. (1990a) Correlation between pulvinar and geniculate corticopetal projections with some receptive-field properties of cat visual cortex neurons. Perception, 19: 373. Shumikhina, S.I. and Volgushev, M.A. (1990b) Receptive-field properties of cat visual cortex neurons with pulvinar input. Sensornye Systemy, 4: 370 - 378. Sillito, A.M. (1984) Functional considerations of the operation of GABA-ergic inhibitory processes in the visual cortex. In: Cerebral Cortex, Vol. 12, Plenum Press, New York, London, pp. 91 - 117. Spitzer, H. and Hochstein, S. (1988) Complex-cell receptive field models. Prog. Neurobiol., 31: 285 - 309. Stone, J . (1972) Morphology and physiology of the geniculocortical synapse in the cat. The question of parallel input to the striate cortex. Invest. Ophthalmol., 11: 338 - 345. Stone, J. (1983) ParallelProcessing in the Visual System, Plenum Press, New York, 438 pp. Stone, J. and Dreher, B. (1973) Projection of X- and Y-cells of the cat’s lateral geniculate nucleus to area 17 and 18 of visual cortex. J. Neurophysiol., 36: 551 - 567. Supin, A.Y. (1981) Neurophysiology of Mammalian Vision, Nauka, Moscow, 252 pp. Tanaka, K. (1979) Afferent connection to the visual cortical cells from X and Y cells in the lateral geniculate nucleus of the cat. J. Physiol. SOC.Jap., 41: 325. Toyama, K., Matsunami, K., Ohno, T. and Tokashiki, S. (1974) An intracellular study of neuronal organization in the visual cortex. Exp. Brain Res., 21: 45 - 66. Toyama, K., Kimura, M. and Tanaka, K . (1981) Organization of cat visual cortex as investigated by cross-correlation technique. J. Neurophysiol., 46: 202 - 214. Updyke, B.V. (1977) Topographic organization of the projections from corlical areas 17, 18 and 19 onto the thalamus, pretectum and superior colliculus in the cat. J. Comp. Neurol., 173: 81 - 122. Volgushev, M.A. (1987) Comparison of the properties of excitatory and inhibitory neurons in cat visual cortex. Sensory Systems, 1: 381 - 389. Volgushev, M.A. (1988) Comparison of the properties of excitatory and inhibitory neurons in cat visual cortex. Perception, 17: 408. Volgushev, M.A. (1989) Role of cortical inhibition in reorganization of receptive fields of cat visual cortex neurons under different adaptation levels. Perception, 18: 5 12. Zihl, J. and Von Cramon, D. (1979) The contribution of the second visual system to directed visual attention in man. Brain, 102: 835 - 856.
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CHAPTER 20
Potentiation of the extrageniculo-striate pathway: a possible role in visual pattern discrimination Svetlana I. Shumikhina Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the U.S.S.R., 117865 Moscow, U.S.S.R.
Introduction A problem in understanding brain mechanisms that are responsible for discrimination of visual stimuli has a fairly enough history. The pioneering studies of Hubel and Wiesel (1959, 1962, 1965), which allowed to distinguish in the cat primary visual cortex neurons with simple and complex receptive fields (RFs), were a basis for intensive investigations of different authors in this direction. Though different subtypes of RFs were described owing to later studies, the classification of Hubel and Wiesel has remained valid and shall be used throughout this article. As is known, many properties distinguish complex RFs of visual cortical neurons from simple ones as well as from RFs of geniculate neurons. According to Hubel and Wiesel (1962, 1965) simple cells comprise the first stage of cortical information processing while complex cells form the second stage of this process. Complex RFs consist of overlapping on and off areas, unlike simple RFs that consist of separate on and/or off areas, and that have inhibitory flanks in their RFs, which are absent in complex RFs. The size of complex RFs is larger than the size of the simple ones. Complex cells do not respond in linear fashion to activation of different points within their RFs in contrast to simple cells. As a rule, complex cells have some level of spontaneous activity and they are less narrow tuned to the orientation of stimuli. Such cells are more responsive to high velocities of stimulus movement (Hubel and
Wiesel, 1959, 1962, 1965; Henry, 1977; Leventhal and Hirsch, 1978; Supin, 1981; Sherman and Spear, 1982; Orban, 1984). Some properties of complex cells (larger RF, overlapping on and off areas) can be explained by the convergence of afferents of simple cells, as was suggested initially by Hubel and Wiesel, while other properties (spontaneous activity, sensitivity to higher velocities) are not. On the other hand, such properties of complex cells as their spontaneous activity, the larger size of their RFs, a broader orientation tuning and sensitivity to high velocities of moving stimuli as well as to low spatial and high temporal frequencies, can be explained by their having inputs from Y-like geniculate cells (the hypothesis of parallel processing of visual information: Stone, 1972, 1983; Stone and Dreher, 1973; Maffei and Fiorentini, 1973; Sherman and Spear, 1982; Spitzer and Hochstein, 1988). A problem, however, with the above hypothesis is that it does not properly explain other properties of complex RFs, such as for example, the structure of the RFs. Nevertheless, many data exist in conflict with both hypotheses. For example, the fact that some complex cells, like simple ones, receive monosynaptic input from the dorsal lateral geniculate nucleus (LGN) (Hoffmann and Stone, 1971; Bullier and Henry, 1979a,b,c; Tanaka, 1979), contradicts the hierarchical hypothesis of Hubel and Wiesel. The other fact that both simple and complex cells can receive inputs from X- as well as from Y-like geniculate neurons, contradicts the hypothesis of
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parallel processing. Data from experiments in which the antagonist of GABA receptors, bicuculline, was used (KrnjeviC and Schwartz, 1967; Sillito, 1984) showing an enlargement of RFs and a reduction of orientation and directional selectivity in some complex cells (Sillito, 1984; Volgushev, 1989), are not in agreement with both hypotheses, because the data propose a role of intracortical inhibition in the formation of complex RFs. These contradictions can be overcome, if we assume an involvement of an additional source of visual information into the process of the formation of complex RFs, such as input from the pulvinar-lateral posterior (Pulv-LP) complex (in the remaining part of the text, this will be referred to as the pulvinar or Pulv-LP). Arguments in favour of an involvement of pulvinar input in the process of formation of complex receptive fields
There are strong arguments to suppose that Pulv-LP takes part in the formation of complex RFs. My hypothesis, based on the involvement of the pulvinar input in the process of the formation of complex RFs, combines elements of both the hierarchical hypothesis of Hubel and Wiesel and the hypothesis of parallel processing, proposed by other authors (e.g., see Sherman and Spear, 1982; Stone, 1983; Spitzer and Hochstein, 1988), as well as taking into account intracortical inhibition as one of the factors of this process. The hypothesis is based on the following data. (1) The Pulv-LP complex receives direct input from the retina (Itoh et al., 1979; Kawamura et al., 1979; Guillery et al., 1980; Leventhal et al., 1980). The “geniculate wing” (Guillery et al., 1980), a site to which the retina projects is not an extension of the LGN, but it is a part of the pulvinar. This fact derives from the detailed studies of Hutchins and Updyke (1989) that the geniculate wing as well as the medial interlaminar nucleus of the LGN have their own incomplete representations of the visual field. (2) The Pulv-LP complex receives also direct retinotopically organized inputs from other visual
subcortical structures - superior colliculus and pretectum - i.e., from visual structures that receive retinal inputs as well (Kawamura and Kobayashi, 1975; Bermanand Jones, 1977; Graham, 1977; Berson and Graybiel, 1978; Graham and Berman, 1981) and can transmit to the pulvinar complex information from all types (X, Y, W) of ganglion cells of the retina (Godfraind et al., 1972; Hoffmann, 1973; Magalhaes-Castro et al., 1976; Ogawa and Takahashi, 1981; Sawai et al., 1985; Hada and Hayashi, 1990; see also Shumikhina, 1981; Stone, 1983). (3) All neurons of the Pulv-LP are spontaneously active (Mason, 1978), their RFs are larger than the RFs of geniculate neurons; directionally responsive and directionally selective neurons comprise the largest group of visually responsive cells of the PulvLPcomplex(Godfraindet al., 1969; Meuldersetal., 1971; Mason, 1978,1981; Harutiunian-Kozaket al., 1981b; Chalupa and Abramson, 1988). A majority of neurons responds especially well to fast moving stimuli (Mason, 1978). Pulv-LP neurons are revealed that have on/off responses in each point of the RF, as well as those with on or off responses, which have concentric and diffuse RFs and orientation selectivity (Godfraind et al., 1969; Mason, 1978; Harutiunian-Kozak et al., 1981a,b). (4) Under adequate conditions, visual sensitivity can be revealed in all cytoarchitectonic subdivisions of the Pulv-LP complex, and the percentage of visually responsive neurons has been estimated to be as high as 93% (Chalupa et al., 1983; Chalupa and Abramson, 1988; Hutchins and Updyke, 1989). (5) There is a direct input from all subdivisions of the Pulv-LP complex to the striate cortex (Albus et al., 1980; Hughes, 1980; Bullier et al., 1984; Shumikhina, 1990). (6) The Pulv-LP complex projects to layer Ia and to the border of layers IVP and V of area 17 (Miller and Benevento, 1979); i.e., pulvinar input can affect cells of all layers of the visual cortex. Pulvinar afferents establish contacts on thin branches and spines of dendrites and make asymmetric synapses (Adrianov, 1977; Miller and Benevento, 1979). (7) Input from the pulvinar has its own way of cor-
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tical excitation, that differs from the geniculate one (Shumikhina, 1984a). (8) Striate input from Pulv-LP is weaker than input from the LGN (Morillo, 1961; Shumikhina, 1984a; Malpeli et al., 1986). (9) Interaction of pulvinar and geniculate afferent inputs can be revealed in the visual cortex (Morillo, 1961; Shumikhina, 1984b, 1988). (10) Complex cells of the striate cortex are a cortical target for input from the Pulv-LP (Shumikhina and Volgushev, 1989, 1990a,b). (1 1) The visual activity, orientation and directional selectivity of complex cells are spared (although these become weaker) after the complete inactivation of all layers of the LGN and its medial interlaminar nucleus, while the visual activity of simple cells is blocked; additional inactivation of Pulv-LP results in the disappearance of the activity of complex cells (Malpeli, 1983; Malpeli et al., 1986). (12) Changes in efficacy of Pulv-LP input results in a reduction of orientation selectivity of complex cells having both pulvinar and geniculate inputs (Shumikhina and Volgushev, 1990b). I would now like to present in more detail our own data. It is well known that the visual activity of pulvinar neurons is unstable and depends significantly on type and depth of anaesthesia (Chalupa et al., 1983; Chalupa and Abramson, 1988; Hutchins and Updyke, 1989). Due to this factor, we conducted our experiments on awake cats. Recently, I have conducted chronic electrophysiological experiments on alert cats (Shumikhina, 1984a). I have recorded evoked potentials to stimulation of the LGN and the pulvinar, in area 17 of the visual cortex. Responses to stimulation of the pulvinar were recorded at latencies of 2.6 f 0.6 msec and to stimulation of the LGN at latedies of 2.0 f 0.5 msec (see Fig. 1). I did not find any significant difference between these latencies. There were differences in the shape of the evoked potentials to stimulation of these structures. The amplitude of these responses was significantly larger to geniculate stimulation under the same intensity of stimulation, and the latency of
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Fig. 1. Evoked potentials in the visual and association cortex to 1 Hz stimulation of the lateral geniculate nucleus (LGN, 0.3 mA) and pulvinar (Pulv, 0.6 mA) in the alert cat. Averaging from eight presentations; negativity upward. Calibration: 100 FV, 5 msec. (Adapted from Shumikhina, 1984a.)
a negative component N l was significantly shorter to geniculate than pulvinar stimulation (7.2 f 0.8 msecand 13.7 f 1.2msec). WhenIrecordedevoked potentials to paired stimulation of the LGN or the pulvinar, I found significant differences in the way area 17 was activated by inputs from the LGN and the pulvinar (Figs. 2, 3). If there is a strong depression of the test response to paired stimulation of the LGN at short interstimulus intervals and its gradual restoration at longer intervals, the depression of the test response to paired stimulation of the pulvinar is very short, and already at short enough interstimulus intervals (20 - 40 msec) a significant (2-4 times) facilitation of the test response is revealed (Shumikhina, 1984a). Similar facts has been obtained by others (Malis and Kriger, 1956; Schoolman and Evarts, 1959; Demetrescu and Steriade, 1965), but I have conducted a quantitative investigation and have examined recovery cycles of evoked potentials to pulvinar stimulation in unrestrained cats. I have also obtained evidence of interaction of afferent inputs from the pulvinar and the LGN in the striate cortex of awake cats (see
228 B
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Fig. 2. Recovery of evoked potentials during paired stimulation of the lateral geniculate nucleus in the visual and association cortex in the alert cat. A . Recovery curves in the association (1) and visual (2) cortex to stimulation of the lateral geniculate nucleus. Abscissa, intervals between test and conditioning stimuli; ordinate, amplitude of response to test stimulation as a percentage of the amplitude of the response to conditioning stimulation. Average data (7 cats, n = 104 for each point). B. Evoked potentials in the association (1) and visual (2) cortex to 1 Hz and paired stimulation of the lateral geniculate nucleus under varied interstimulus intervals (shown at left) in one of the cats. Averaging from eight presentations; negativity upward. Calibration: 100 p V , 50 msec (for lower oscillograms: 100 pV, 5 msec). (Adapted from Shumikhina, 1984a.)
Shumikhina, 1984b, 1988). Convergence of pulvinar and geniculate inputs on single cells in area 17 has also been shown by Morillo (1961). Shumikhina and Volgushev (1989, 1990a,b) showed that in alert cats prepared under local anaesthesia using a long-lasting anaesthetic (lidocaine hydrochloride), 33% of neurons in area 17 responded to electrical stimulation of Pulv-LP and the RFs of those neurons consist of overlapping on and off areas (Fig. 4). These cells can be classified as having complex RFs according to Hubel and Wiesel (1962,1965). We have recorded 46 neurons from 11 cats. Animals were immobilized with Dtubocurarine and artificially respired. Light flash stimuli (rectangles with sides from 0.5 to 3 deg, 21.2
cd/m2, 150 - 200 msec) were presented under conditions of mesopic light adaptation to one eye, while the other eye was closed. The variability of the latency served as the main criterion for orthodromic response. Additional criteria could be provided when we recorded cells in the superficial cortical layers, as it is known that corticogeniculate and corticopulvinar neurons are located in deep (V to VI) layers (Gilbert and Kelly, 1975; Abramson and Chalupa, 1985). We always verified the subcortical placement of the tips of the stimulating electrodes, as it is known that the cortico-reciuient zone is located in a definite region of the Pulv-LP (Updyke, 1977; Berson and Graybiel, 1978). High-frequency stimulation was not used for this purpose because it could affect the properties of cortical neurons. Four groups of neurons in the visual cortex were defined on the basis of presence/absence of input from two
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Fig. 3. Recovery of evoked potentials during paired stimulation of the pulvinar in the visual and association cortex in the alert cat. A . Recovery curves in the visual (2) and association (1) cortex to stimulation of the pulvinar. Average data (14 cats, n = 120 for each point). B. Evoked potentials in the visual (2) and association (1) cortex to 1 Hz and paired stimulation of the pulvinar in one of the cats. Symbols as in Fig. 2. (Adapted from Shumikhina, 1984a.)
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subcortical structures: (1) cells with inputs from Pulv-LP and the LGN (13 cells, 28%); (2) cells with input only from the LGN (10 cells, 22%); (3) cells with input only from Pulv-LP (2 cells, 4v0); and (4) cells non-responsive to electrical stimulation (0.2 msec, 10- 60 V) of these structures (21 cells, 46%). Stimulation of the LGN resulted in the excitation of 50% of cells from the 46 neurons tested, at latencies of 0.8 - 10.8 msec (mean 3.7 k 0.7 msec). Stimulation of the Pulv-LP elicited responses in 33% of the cells at latencies of 0.8 - 10.2 msec (mean 2.9 k 0.6 msec). Pulvinar and geniculate projections are closely connected with each other: 87% of neurons with Pulv-LP input also responded to geniculate stimulation, while 62% of neurons with geniculate input also responded to pulvinar stimulation. We have tested RF properties of 8 cells with both pulvinar andgeniculate inputs, 3 cells with input only from the LGN, and 1 cell with input only from the A
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Fig. 4.Three-dimensional plots of the receptive fields of neurons.
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the pulvinar. Vertical axis: number of spikes in response to presentation of stimuli in each of 100 (10 x 10) points of the visual field; the plane of the plot corresponds to the plane of the screen. (Adapted from Shumikhina and Volgushev, 1990b.)
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Fig. 5 . Orientation selectivity of a neuron with inputs from the pulvinar and the lateral geniculate nucleus. A . Schematic representation of the receptive field (RF). The RF-centre is the point of the maximal neuronal discharge. Solid line, on-response zone; hatched area, off-response zone; cross, centre of gaze; open circle, on centre; black circle, off-centre. B. Orientation tuning curve of the neuron before (dotted line) and after (solid line) high frequency pulvinar stimulation. Abscissa, stimulus orientation in degrees from the horizontal; ordinate, number of spikes in the response as a percentage of maximal. C. Peristimulus time histograms (PSTH) of neuronal responses to flashes presented to the centre of the RF (light bar 3 X 0.5 deg) at different orientations before (left) and after (right) high frequency pulvinar stimulation. Figures near each histogram, orientation of the stimulus. The PSTHs are based on 20 stimulus presentations. (Combined from Shumikhina and Volgushev, 1990b.)
pulvinar. The R F size of 9 neurons with pulvinar input varied from 2 to 54 deg2, and these cells had centres that were located 2 - 17 deg from the gaze. The RF width of 8 cells with both pulvinar and geniculate inputs varied from 1.5 to 8 deg (mean 5 f 1 deg) and their length varied from 1.5 to 12deg (mean 7 k 1 deg). 62% of these neurons were orientation-selective. The width of their orientation tuning curves varied from 22 to 150 deg (mean 82 +_ 13 deg). These neurons preferred horizontal
230
stimulus orientations as a rule (75%) (Fig. 5 ) , while neurons with input only from the LGN more often preferred oblique stimulus orientations (this difference was not significant). The RF size of 3 neurons with inputs only from the LGN varied from 9 to 39 deg2, and these cells had centres that were located 2 - 14 deg from the gaze. The RF width of these cells varied from 3 to 8 deg (mean 5 k 1 deg) and their length varied from 3 to 10deg (mean 7 k 1 deg). The RF size of the neuron with input only from the pulvinar composed 24 deg2. The RF width of this neuron composed 6 deg and its length composed 6 deg as well. To test for a possible role of pulvinar input in the formation of complex RFs, we tried to use high-frequency stimulation (200 Hz, 10 sec, 25 V) of the pulvinar before the presentation of stimuli of different orientations. The tetanization resulted in a reduction of the orientation selectivity of complex cells in the visual cortex showing inputs from
Pulv-LP and the LGN (Fig. 5). This reduction was at the expense of a three-fold increase of the response to stimuli opposite to the optimal orientation. There was also a significant intensification (more than two-fold) of responses to stimuli of other orientations. Thus, we have shown that changes in efficacy of pulvinar input result in changes in properties of complex RFs of neurons in area 17, i.e., they evoke adaptive modifications of complex RFs. I would like to propose that pulvinar input tonically excites complex cells. Such tonic excitation is manifested as spontaneous activity in these neurons. The pulvinar input complicates the basic properties of complex RFs having inputs of simple or geniculate cells (see Fig. 6 , for details). As a result, complex cells have RFs of larger size and of broader orientation tuning than simple ones and acquire sensitivity to high velocities. The phasic character of the excitation of complex cells is deter-
n
7
7 I
I
Pulv
7
LGN
7
Fig. 6 . Scheme of the organization of complex cell inputs that determine its receptive field properties. A . A pyramidal neuron (PN, complex cell) receiving a monosynaptic pulvinar input and a disynaptic geniculate input (input from simple cell). B. A pyramidal neuron receiving monosynaptic pulvinar and geniculate inputs. SN, a stellate cell; EN, excitatory neuron; IN, inhibitory neuron. Interrupted line, connections that determine “vague” physiological mechanisms, revealed by the method of paired stimuli. Peristimulus time histograms, supposed response of the pyramidal neuron as a result of its excitation by pulvinar and geniculate inputs to optimally oriented stimuli. Here, well-known data are used, such as: (1) the majority of simple cells are located in layer IV of the striate cortex and these are stellate cells as a rule (Kelly and Van Essen, 1974; Bullier and Henry, 1979a,b,c); (2) the majority of complex cells are located in layers I1 + 111, V and VI of the striate cortex and these are pyramidal cells as a rule (Kelly and Van Essen, 1974; Lin et al., 1979); (3) both simple and complex cells can receive mono- as well as diskaaptic geniculate inputs (Hoffmann and Stone, 1971; Toyama et al., 1974; Bullier and Henry, 1979a,b,c; Ferster and Lindstrom, 1983); (4) simple cells can excite and inhibit complex cells as well (Volgushev, 1987,1988); ( 5 ) inhibition can be revealed between cells with both weakly and significantly distinctive preferred orientations (Blakemore and Tobin, 1972; Toyama et al., 1981; Volgushev, 1987).
23 1
mined by inhibitory processes at the level of simple cells, or by input from inhibitory neurons. The adaptivity of complex RFs can be achieved in this case by changes in the efficacy of pulvinar input. These considerations are stated in short by Shumikhina (1991).
Conclusions At first sight it may seem paradoxical that the intensification of the pulvinar input can result in a reduction of the orientation selectivity of complex cells and, consequently, to a worsening of the discrimination of visual patterns. However, behavioural manifestations cannot always follow directly from physiological phenomena. As is known from studies of young animals, simple RFs are experienceinsensitive, while complex RFs possess a certain adaptivity (Hirsch, 1985). Complex cells are higherorder output neurons, which transmit information to other visual cortical areas (Hubel and Wiesel, 1965; Denney et al., 1968; Toyama et al., 1974; Gilbert and Wiesel, 1983), and properties of their RFs are formed later during the course of development (Sherman and Spear, 1982; Hirsch, 1985), but these cells have worse detector characteristics (larger size of RF, broader orientation tuning, a sensitivity to low spatial frequencies) than simple cells. It is hard to believe that this is only by chance. As has beenshown by different authors, the visual responses of Pulv-LP can be increased in situations of interest to visual stimuli, and the activity of Pulv-LP neurons depend on visually evoked eye movements (e.g., see Chalupa, 1977;Fabre-Thorpe et al., 1986). Experiments with lesions of Pulv-LP also have shown that this structure is involved in processes of visual discrimination and attention (Chalupa, 1977; Zihl and Von Cramon, 1979; Fabre-Thorpe et al., 1986). Consequently, it can be concluded from these data that potentiation of pulvinar input has to result in improvement of visual discrimination. I suppose, that the reduction of the orientation selectivity of complex cells after tetanization of the pulvinar input can mean that the selective attention to visual stimuli (our potentiation of pulvinar input may be con-
sidered as a model of this process) actively depresses (masks) some reactions of sign detectors and, as a result, subserves the finer discrimination of visual patterns. The involvement of pulvinar input into the process of the formation of complex RFs can be important for providing the plasticity of cortical reactions.
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