Feb 11, 1985 - Positions of the Areae centrales an the screen were plotted by the method of Fernald and Chase (12). Stimulation was performed by moving ...
ACTA NEuROBI~L. EXP. 1985, 45: Tt-Sd
DYNAMIC AND STATIC PROPERTIES OF NEURONS IN THE LATERAL SUPRASYLVIAN AREA OF THE CAT B. A. HARUTIUNIAN-KOZAK, R. L. DJAVADIAN, NI. B. AFRIKIAN and S. A. KHACHATRIAN Laboratory of Physiology of Sensory Systems, Orbeli Institute of Physiology, Academy of Sciences of Armenian SSR Orbeli 22, 375028 Erevan, USSR
Key words: receptive field, stimulus oantrast reversal, dynamic properties, dark sensitive neurons, lateral suprasylvian area, cat
Abstract. The response properties and receptive field organization of 106 LSA neurons were investigated in pretrigeminal preparations using moving dark and bright stimuli with particular reference to the dynamic and static structure of receptive fields. About 61Q/o neurons revealed equal sensitivity to the motions of dark and bright stimuli. A majority of them had an ON-OFF static structure of receptive fields. Nearly 24O/o of cells had higher sensitivity to the motiomn of dark stimuli in comparison with the bright ones. Their receptive fields constituted the OFF-uniform spatial distribution when tested by stationary flmhing lights. No clear-cut correlations were found between the static and dynamic properties of LSA neurons. It was shown that the same region of the receptive field is responsible for the reactions to dark or bright moving stimuli. A group of dark-sensitive neurons (24O/o of the total) was described, some examples of which had no stationary receptive fields at all. INTRODUCTION
Lateral suprasylvian area (LSA) was first described as a visually responsive regian of the cat cortex by Marshall et al. (26). Later Clare
and Bishop (8) confirmed these data and thus a new visually sensitive region of the cat cortex has been outlined apart from the well-known 17, 18, 19 visyal areas. According to the recent investigations LSA occupies almost the entire length of the suprasylvian sulcus (9, 28, 32). Visually sensitive neurons were found in its both banks and in its fundus. It receives direct afferents from the dorsal lateral geniculate body (24, 29, 30) and inputs from visual cortical areas 17, 18, 19 (8, 21). The LSA receives projections also from extrageniculate visual pathways via the midbrain and posterior thalamic nuclei (13, 15, 24, 25). The LSA is thus a point of convergence of two main visual inputs, geniculostriate and extrageniculate. Such an organization suggests that this visual region plays an important and integrative role in central visual processing. Hubel and Wiesel (19) were the first to record single unit activity in LSA (or Clare-Bishop area). According to Hubel and Wiesel (19) LSA neurons had extremely high sensitivity to moving visual stimuli and rather weak reactions to stationary flashing lights. These observations were confirmed by other authors investigating the neuronal activity in the LSA of the cat's cortex (7, 34). In our previous investigations (14, 23) we described an additional group of neurons sensitive to movement of dark stimuli (dark-sensitive neurons) in the LSA cell population. The function of the LSA was therefore thought to be related to analysis of moving stimuli. However, Turlejski (33), Spear and Baumann (32) had observed in the LSA mleurons sensitive to stationary flashing light. Furthermore, our own investigations (22, 23) had indicated that there were in the LSA neurons sensitive to the stationary stimulation of their receptive fields. Thus it became advisable to explore the receptive fields of these neurans by stationary flashing light spots and to describe their static structure as well. This property of LSA neurons gives us an opportunity to investigate the relationship between responses to stationary and moving stimuli. Some investigators (6, 31) of striate cortex failed to find any correspondence between static-field plots and responses to moving stimuli. On the other hand Emerson and Gerstein (lo), Palmer and Davis (27), were able to predict responses to moving stimuli from the static-field plots of neurans investigated. Until now, no attempts were made to investigate this problem in LSA neurons. Having in mind the high sensitivity of LSA neurons to moving visual stimuli, it is worthwhile to search for some predictive factors in their receptive field structure. In this study we present the results concerning the static and dynamic properties of the receptive fields of LSA neurons.
METHODS
Cats weighing 2.5-3.5 kg were used in the experiments. They were anesthetized with ether for initial surgical procedure. Tracheotomy and cannulation of the femoral artery and subsequently brain stem pretrigeminal transections were performed (3, 35). Thus pain was removed without pharmacological intervention. The animal's head was fixed in a stereotaxic apparatus (Horsley-Clarke, modified for visual research). After trepanation, the window in the skull was filled with 3OIo agar in O.gO/o NaCl solution. The wounds on the head were infiltrated by injections of Novocain (5O/o). Immobilization of the animal was achieved by the intramuscular injection of the myorelaxant Ditilin (diiodide dicholine ester of succinic acid) 7 mg/kg. Artificial respiration was administered (19 strokedmin, stroke volume 20 ml/kg body weight). The body temperature was kept at 38'C by a heating pad. The pupils were dilated by topical application O.lO/o atropine solution and corneas were protected from drying with zero power contact lenses. Nictitating membranes were retracted by instilling 1°/o Neosynephrine into the conjunctival sac. Additional spectacle lenses were commonly used to achieve optimal focus of the eyes on the perimeter screen. Arterial blood pressure was continuously measured and remained at 90-100 mm Hg. The heart activity and EEG were monitored occasionally. Single unit activity was recorded 2-3 h after the cessation of the ether anesthesia. Tumgsten microelectrodes (17) covered by vinyl varnish, with a bare tip diameter of 2-5 pm were used. Single unit activity was recorded by conventional methods and analysed with an ANOPS101 analyzer using the poststimulus time histogram (PSTH) program, generally with a time base of 2 s and bin width of 4 ms. Averaging was achieved by repeating a stimulus 16 times. The receptive fields of neurons were plotted on a cancave screen that could swing, thus covering 180' of the visual angle; it was situated in front of the cat's head at a distance of 1 m from the nodal points of the cat's eyes. Positions of the Areae centrales an the screen were plotted by the method of Fernald and Chase (12). Stimulation was performed by moving bright and dark spots of different sizes (subtending 3'-5') with an angular velocity of 40 deg/s, which was optimal for most LSA neurons. The values of contrast for light and dark stimuli against the background were kept constant in all experiments. The bright spots were 7 lx against 2 lx background and dark spots were, conversely, 2 lx luminance against 7 lx of background. Reflective index of the screen
was 0.85. Thus the ambient illumination was kept in the mesopic range and helped to keep the contrast sensitivity of the cell constant. Dark spots were the shadows projected on the screen from the same projector system which served the bright spots. Motion of stimuli was achieved by a galvanometer system end a trapezoidal waveform generator. At the end of the experiment coagulation was performed at recording points (10 yA for 5 s). Perfusion of the brain with physiological saline and later fixation with a 10°/o formalin solution was made routinely and the electrode track was reconstructed after the examination of 30 pm histological sections. RESULTS
The units chosen were recorded in the left LSA (Horsley-Clarke frontal plane P-2 to A-10, lateral plane 12-13). A total of 106 neurons were investigated, these being the units from which sufficiently complete sets of static and dynamic response properties were obtained. To simplify a description of the characteristics of neurons we have categorized them according to their reactions to moving dark and bright spots. In this connection attention was paid to the comparative sensitivity of neurons to dark versus bright moving visual stimuli. Receptive fields were plotted on the perimeter screen by hand-held black stimuli and stationary light spots. It is important to emphasize that the dimensions of a receptive field depend very much on the nature of the stimulus used. Generally, hand-plotted receptive fields are considerably smaller than those estimated by the automated stationary stimuli. We confirm the observations of Kato et al. (20) in this respect. 1. Nearly 61°/o of the neurons investigated were equally sensitive to dark and bright moving stimuli. In a majority of cases the receptive fields of these neurons showed a uniform spatial distribution of sensitivity to both stimuli all over the receptive field surface. Responses of a neuron with the above described properties are shown in Fig. 1. This neuron is directionally selective and it- does not change its pattern of responses when the stimulus contrast is reversed (11). It is seen from the figure that in every trace of movement of dark or bright stimuli over the receptive field surface similar patterns of responses were elicited. What is more interesting in this neuron, is that the responses to the motion of dark and bright stimuli were elicited from the same part of the receptive field (shown in Fig. ID). The receptive field of this neuron, as tested by stationary flashing lights, shows ON-OFF responses in all points tested (not shown in the figure), There were no spatially distinct ON and OFF zones in this field, which presence could be responsible for the responses to dark and bright stimuli.
RF AC
'
.
Hand Plot
0
-
C = l e
M 0
Fig. 1. Poststimulus time histograms (PSTH) of responses of a directionally-selective neuron with equal sensitivity to the dark and bright moving stimuli. A, receptive field location in relation to Areae centralets (AC) of the right (contralateral) eye as it appeared on the perimeter screen. Solid line indicates the receptive field's dimensions as measured by a hand-held black stimulus (5' X 3'). Broken line indicate~sreceptivie field !sizes as dietermined by a flashing a statiolocations across the receptive field. Bright spot illunary spot (5') at sucae~s~sive 7 lx, background 2 lx. B, C, PSTH of responses to the motion mination of dark and bright spots at each of 6 different receptive field positions separated by 5' (shown in A by arabic numbers). Preferred direction is froan left to right. D, responws to the movienneolt of bright (a) and dark (b) s p d s at position 2 in the receptive field. Note the exact correspondence of the receptive field's regions reacting to bright and dark spots. Arrows indicate the directions of stimulus momement. Broken lines in B, C and D indicate the turning points of the direction of m o v e m t . The spots moved at a 40 deg/s velocity. Abscissae in each histogram had 2 s duration. Bin width - 4 m. Moving bright spot illumination was 7 lx on the 2 lx background illumination. Moving dark spots had 2 lx illumination surrounded by a 7 lx background. Explanations are the same for the subsequent figures.
-
-
Some neurons of this group did not have uniform spatial organization of their receptive fields, although essentially they revealed equal sensitivity to dark and bright stimuli. These neurons showed some differences in the response patterns related to the spatially different positions of stimulus motion. We have already mentioned such receptive fields in our previous paper (14), where an example was given of the different sensitivity of parts of the field to dark and bright stimuli. Here we present a somewhat different example. Figure 2 represents the PSTH of responses of a neuron which is directionally asymmetric (11) and which changes its pattern of responses according to stimulus con-
trast. It is clearly seen from the figure, that the upper parts of the receptive field had directional sensitivity for the dark stimulus but not for the bright one, whereas the lower parts of the field had opposite characteristics. Thus, the receptive field of the neuron in Fig. 2 is obviously non-uniform. It is rather confusing that the flashing light spot elicits ON-OFF responses uniformly distributed along the entire receptive field, as in the preceding example (not shown in the figure). The general impression was that the neurons which exibited equal sensitivity to dark and bright moving stimuli had a spatially uniform ON-OFF organization of receptive fields. Figure 3 represents PSTH's of responses of a neuron typical for this group. In B and C responses to the moving dark and bright spots are presented as recorded by scanning the receptive field from top to bottom (Fig. 3A). The neuron is directionally selective. The responses of the same neuron to stationary flashing lights are shown in Fig. 3D. As seen from the figure, ON-OFF responses are elicited from almost every point of the receptive field
Fig. 2. Responses of a neuron with a non-uniform spatial organization of its dynamic properties. A, receptive field sizas as measured by a 5' diameter bright static stimulus (broken line) and a hand-heLd (5' X 3') black stimulus (solid line). B, respcmsew of the neuron to the ohodal m o v e m t (5' steps) of a 6' diam dark spat across dx positiolm in the receptive field. C, rer;,pmses of the same neuron to the chordal movement of a 5' diam bright spot across the same positions in receptive field.
tested, although the field periphery shows a prevalence of OFF-reactions. This deviation from uniformity of the receptive field static structure is insufficient to explain the reactions of the cell to moving dark and bright stimuli. There are no separate ON and OFF regions in this receptive field which, as Albus and Fries (2) have shown in the striate cortex, could be the basis of organization of responses to dark (OFF region) and bright (ON - region) moving stimuli. 2. The second group of neurons revealed more sensitivity to the moving bright spots than to dark spots. They constitute some 15O/o of the population of neurons investigated. The responses of one of these
Fig 3. Dynamic versus static properties of a directionally-selective neuron with equal sem~itivityto [the dark amd bright moving spots. A, receptive field sizes as determined by a 5' X 3' size hand-held dark stimulus (solid line) and stationary (5' diam) flashing light spot (broken line). B, msipmes to the motion of 5' diam dark spot across five positions in the receptive field (5O apart). C, PSTH of respmses to th~emotion of a bright lsipot (5' diameter) acma the same positioaw in receptive field as indicated above. D, responses to stationary flashing light mot (5' diam) a t successiv~e locations across each of 5 positions in receptive field. Black strip, OFF time (1 s); light strip, ON time (1 s). Explanations a r e the same for the subsequent figures.
neurons are presented in Fig. 4, where B is the scanning of the receptive field by the dark spot and C - by the bright spot of the same size. As is seen from the figure, the motion of the dark spot elicits monomodal responses, whereas the bright spot elicits bimodal responses. At first sight one could think that the static structure of this neuron's receptive field has to be constructed in a sandwich manner with the ON periphery and OFF central zone where two peripheral zones evoke
bimodal responses to bright moving spot and central OFF zone - monomodal responses to moving dark spot. The static receptive field, however, as outlined by the 5' flashing light spot positioned side by side along each scanning trace (Fig. 4D), shows an ON-OFF structure all over the field surface with a prevalence of ON response components in the center of the receptive field and OFF - responses in the periphery. Thus no obvious correlation between the static and dynamic properties of this receptive field is detectable here. The balance between ON- and OFF-compments of an ON-OFF response is sometimes a very important factor in organizing the cell responses pattern to moving stimuli.
r
A
B
C
RF
D Briqht Static
-I-, L
--------- - -
'
fi
60 WUES/BIN
Fig. 4. Dynamic versus static properties of the receptive field of a neuron with a high sensitivity to the motion of a bright spot as compared with a dark moving spot. A, receptive field sizas as measured by a 5' X 3' hand-held black stimulus (solid line) and a 5' diam stationary flashing spot (broken line). B, PSTH of responses to the movement of a 3' diam dark spot at 4 positions in reoeptive field, Note monomodal responses of the cell. C, PSTH d responses of the samle cell to the motion of 3' diam bright spot. Bimodal responses are evident. D, respomels to a 3' diam stationary flashing light sa~otlocated at successive points (3' steps at elaoh of 5 pors~itioinsim reoeptive field).
3. The third group (24O/o of the total number) of neurons investigated were the "dark sensitive" neurons (Figs. 5 and 6). These neurons exhibited a high sensitivity to the movement of dark stimuli and rather weak reactions, or none at all, to the motion of bright stimuli. We have already described them in the previous paper (14). In the present study the dynamic and static structures of the receptive fields of this group of neurons are presented. These (neurons are mostly directionally asyrnmetric end their directionally non-sensitive responses become directim-
Fig. 5. Dynamic versus static properties of the receptive field of a directionallyasymmetric neuron with high senisitivity to the motion of dark spot in comparison with bright moving spot. A, Receptive field sizes determined by hand-held 5' X 3' black stimulus (solid lme) and stationary flashing 5O diam light spot ( b ~ o h e nline). B, Dinectionally non-sensitive responsels of the neuron to the movement of a 5O diam dark s , p t a t 6 positions in receptive field. C, Directionally sensitive responses of the same neuron to the motion of a 5' diam bright sipot. D, PSTH of responses to static presentation of a 5' diam bright spot at successive locations in each of 3 different (2-4) positions of receptive field.
C
D Briaht Static
Fig. 6. Dynamic versus static properties of a receptive field of a directionally-selective neuron with a high sensitivity to the motion of a d a r k spot, A, receptive field sizes plotted by a 5' X 3' hand-held stimulus (solid line) and stationary 5' diam flashing light spot (broken line). B, PSTH of relsiponses to the motion of 5O diam dark spot a t different p~o~s~ltions in the rece~ptivefield. C, PSTH of responses to the motion of a 5' diaun bright spot a t the same positions in receptive field as in B. D, static presentations of a 5' diam flashing light spot a t successive points of each of four, (2-5) positions in the receptive field.
ally-sensitive with a reversal of the stimulus contrast. The receptive field size of the neuron of Fig. 5, as measured by hand plot using dark stimuli is smaller in comparison with that using bright stimuli; this is characteristic for almost all neurons investigated. The intensity of responses to the movement of the dark spot is higher (Fig. 5B) than that elicited by the movement of the bright spot (Fig. 5C). This neuron had well-defined responses to stationary flashing lights, although some neurons of this group did not. The static structure of its receptive field is uniformly OFF (Fig. 50). The directionally asymmetric response of the cell i.e., directional in C and non-directional in B, must somehow be organized from a uniform OFF receptive field. Most puzzling are the local differences: trace 5 shows no response to the bright stimulus, whereas the trace 3 having the same OFF static structure, shows strong reactions to the bright spot. Again one could not find any correlation
Briqht Static I I
a iMwwwu
L
L I
7
-
Fig. 7. Properties of the receptive field of a pure dark-sensitive neuron. A, sizes of the receptive field as measured by hand-held 5' X 3' black stimulus (solid line). Broken line here indicates the approximately measured space around the hand plotted reoeptive field wherefrom responses to the moving dark spot could be elicited. a, b, c indicates the successive locatims of stationary 5O diam flashing light spot a t position 3 in the rewptive fiel'd. B, PSTH of mspo~uuesto a moving 5' diam dark spot. C, PSTH of responses of the same neurm to a moving 5 O diam bright s p o t D, pmsentiathns cd stationary 5O diam flashing spots a t successive points in position 3 of the receptive field.
between the dynamic characteristics of the neuron and static properties of its receptive field. The same is true for the neuron presented in Fig. 6. This neuron is directionally-selective (preferred direction from left to right, Fig. 6B and C). The static structure of this neuron is again uniformly OFF (Fig. 6D). Thus evidently the static organization of receptive fields of directionally-asymmetric as well as directionally-selective neurons had almost identical, spatially uniform OFF-characteristics. A few neurons of this group were, most interestingly, not sensitive to the bright stimuli at all. A majority of these neurons are directionally selective and respond to moving dark objects only. Responses to the stationary flashing spot were absent in these neurons. Figure 7 shows a typical example of responses of one such neuron. In B the responses to the scanning of receptive field by a dark spot are presented. There are direction-sensitive responses with the preferred direction from left to right. In C the almost negligible responses to the moving bright spot are illustrated. The stationary flashing spot did not elicit responses of the cell at all and this is shown in Fig. 70, where PSTH's were prese$nted taken at successive test points in the receptive field as indicated as a, b, c, in Fig. 7A. Thus the static and dynamic properties of the LSA neurons are only loosely correlated in comparison with the same properties of neurons in geniculostriate pathways.
DISCUSSION
The correlation between the static organization of the receptive fields of visually sensitive neurons and their dynamic characteristics has beeln the main interest of majny investigators in vision research (1, 2, 6, 10, 11, 18). A wealth of data have been accumulated according to which the spatial static structure of the receptive field could predict the pattern of dynamic responses of the cell (10, 11, 27). Nevertheless, some authors observed a few examples where discrepancies between the stationary and dynamic structures of receptive field were evident and this was true especially at the cortical level (1, 2, 6). Data presented in this study confirm these latter observations and show that LSA neurons have even more loose correlations between their static and dynamic properties as compared to those of st,riate cortex. LSA neurons had mainly uniform ON-OFF, OFF or rarely ON static fields which could not explain the mechanisms of generation of various patterns of responses to the moving stimuli. For example, in LSA neurons one could not
explain the effects of stimulus contrast reversal on the basis of the spatial organization of discharge centers. This is well shown in Figs. 1 to 3, where the same region of receptive field could generate similar responses to the bright moving stimulus as well as to the dark one. Thus, in the case of ON-OFF static receptive fields, the stimulus brings into action certain components of the ON-OFF response, corresponding to the type of stimulus (bright or dark). It means that the ON-component of ON-OFF response would be involved in the action when the leading edge of the bright, or trailing edge of the dark, stimulus enters the receptive field and the OFF-component, when the trailing edge of the bright stimulus, or the leading edge of the dark stimulus, is entering the receptive field. Thus, a delicate balance between the components of the ON-OFF responses could be responsible for the observed effects. But this explanation is inadequate when the dark-sensitive neurons with uniform OFF receptive fields are considered and, especially, when the ,neurons without static receptive fields are taken into account. This fact indicates that some neurons in this extrageniculostriate structure are subject to somewhat different influences when organizing their pattern of responses. Our observations indicate that the organization of dynamic and static properties of LSA neurons in most cases show essential differences. The main conclusion is that spatial factor is probably less important in the mechanisms of organization of response patterns of LSA ineurons. It may be that the temporal factor is more essential in this case. One must check this possibility before a final judgement on the mechanisms of organization of contrast reversal effects in LSA neurons can be made. It this statement were true, then, contrary to the geniculostriate neurons, where the spatial arrangement of the ON and OFF zones is an essential factor in the organization of cell responses (4, 5, 16), the temporal factor could be of high importance in the organization of specialized responses of neurons to moving stimuli in extra-geniculostriate pathways. In order to elucidate these problems, we propose to study the LSA neurons using two or three light spots with appropriate time delays between presentations of the individual spots.
REFERENCES 1. ALBUS, K. 1980. T h e detection of movement direction a n d effects of contrast revensal i n t h e cat's striate cortex. Vision Res. 20: 289-283. 2. ALBUS, K. and FRIES, W. 1980. Inhibitory sidebands of complex receptive fields i n the cat's sbitrilate cortex. Vision Res. 20: 38-372.
BATINI, C., MORUZZI, G., PALESTINI, M., ROSSI, G. F. a,& ZANCHETTI, A. 1959. Effects of complete pontine transections m t h e sleep-wakefullness rhythms: the midpontine pretrigeminal preparation. Arah. Ital. BioL 97: 1-12. BISHOP, P. O., COOMBS, J. S. and HENRY, G. H. 1971. Responses to visual contours: spatio-temporal aspects of excitation in the receptive fields of simple striate neurons. J. Physiol. 219: 685-658. BISHOP, P. O., COOMBS, J. S. and HENRY, G. H. 1971. Interaction effects of visual contours on the discharge frequency of simple striate neurons. J. Physiol. 219: 659-6&8. BISHOP, P. O., DREHER, B. and HENRY, G. H. 1972. Simple striate cells: comparison of responses to stationary and moving stimuli. J. Physiol. 227: 15P. CAMARDA, R. and RIZZOLATTI, G. 1976. Visual receptive fields in the lateral suprasylvian area (Clare-Bishop area) of the cat. Brain Res. 101: 427-444. CLARE, M. H. and BISHOP, G. H. 1954. Responses from an association area secondarily activated from optic oortex. J. Neuraphysiol. 17: 271-277. DJAVADIAN, R. L. and HARUTIUNIAN-KOZAK, B. A. 111983. R e t i i o t q i c organization of the lateral suprasylvian area of the cat. Acta Neurobiol. Exp. 43: 251-261. EMERSON, R. C. and GERSTEIN, G. L. 1977. Simple striate neurons in the cat. I. Comparison of responses to moving and stationary stimuli. J. Neurophysiol 40: 119-135. EMERSON, R. C. and GERSTEIN, G. L. 1977. Simple striate neurons in the cat. 11. Mechanisms underlying directional asymmetry and directional selectivity. J. Neurophysiol. 40: 136-155. FERNALD, R. and CHASE, R. 1'971. An improved m e t h d for plotting retinal landmarks and focusing the eyes. Vision Res. 1,l: 95436. GRAYBIEL, A. M. 1972. Some ascending comectfons of the pulvinar and nucleus lateralis posterior of the thala~musin the cat. Brain &s. 4.4: 99125. HARUTIUNIAN-KOZAK, B. A., DJAVADIAN, R. L. and MELKUMIAN, A. V. 1984. Responses of neurons in cat's lateral suprasylvian area to moving light and dark stimuli. Vision Res. 24: 189-195. HEATH, C. J. and JONES, E. C. 1971. An experimental study of a~scendiig connections from the posterior group of thalamic nuclei in the cat. J. Comp. Neurol. 141: 397-426. HENRY, G. H. 1977. Receptive field classes of cells h t h e striate cortex of the cat. Brain Res. 133: 1-28. HUBEL, D. H. 1957. Tungsten microelectrodes for recording from single units. Science 125: 549-550. HUBEL, D. H. and WIESEL, T. N. 1965. Beceptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28: 229-289. HUBEL, D. H. and WIESEL, T. N. 19fB. Visual area of thle lateral suprasylvian gyrus (Clare-Bishop area) of the cat. J. Physiol. 202: 251-260. KATO, H., BISHOP, P. 0. and ORBAN, G. A. 11978. Hypercomplex and complex cell classifications in cat striate cortex. J. Neurophysiol. 41: 10711095.
21. KAWAMURA, S. 1874. Topical organization of t h e extrageniculak visual system in the cat. Expl. Neurol. 45: 451-461. 22. KHACHVANKIAN, D. K. a d HARUTIUNIAN-KOZAK, B. A. 1.881. Properties of visually sensitive neurons in lateral suprasylvian area of t h e cat. A d a Neurobiol. Exp. 41: 299-314. 23. KHACHVANKIAN, D. K., HARUTIUNIAN-KOZAK, B. A., DJAVADIAN, R.L. and GRIGORIAN, G. G. 1982. Heceptive fields of the neurons of the cat's lateral suprasylvian area. Neir~fiziologia 14: 278-283. 24. MACIEWICZ, R. J. 1974. Afferents t o t h e lateral suprasylvian gyrus of t h e cat traced with horseradish peroxidase. Brain Res. 78: 139-143. 25. MARCOTTE, R. R. and UPDYKE, B. V. 1981. T h a l m i c projections onto the visual areas of thle middle suprasylvian sulcus i n t h e cat. Anat. Rec. 199: 16OA. 26. MARSHALL, W. H., TALBOT, S. A. and ADES, H. W. 1943. Cortical response of the anesthetized cat t o gross photic and electrical afferent stimulation. J. Neurophysiol. 6: 1-15. 27. PALMER, L. A. and DAVIS, T . L. 1981. Receptive-field structure in cat striat e cortex. J. Neurophysiol. .46: 260-276. 28. PALMER, L. A., ROSENQUIST, A. C. and TUSA, R, J. 19718. The retino-ic organization of lateral suprasylvian area in t h e cat. J. Comp. Neurol. d77: 237-256. 29. RACZKOWSKI, D. and ROSENQUIST, A. C. 1980. Connections of the parvocellular C laminae of the dorsal lateral geniculate nucleus with t h e visual cortex in the cat. Brain Res. 199: 447-459. 30. ROSENQUIST, A. C., EDWARDS, S. B. and PALMER, L. A. 1974. An autoradiographic study of the projections of t h e dorsal lateral geniculate nucleus and the posterior nucl~ews i n the cat. Brain Res. 80: 71-94. 31. SCHILLER, P. H., FINLEY, B. L. and VOLMAN, S. F. 11976. Quantitative studies of single cell properties in monkey striate cortex. I. Spatiote~nporal organization of receptive fields. J . Neurophysiol. 39: 1288-1319. 32. SPEAR, P. D. and BAUMANN, T. P. 1975. Rece~ptive field characteristias of single neurons in lateral suprasylvian visual a r e a of t h e cat. J. Neurophysiol. 38: 1403-1420. 33. TURLEJSKI, K. 1975. Visual r e s p o n s s of neurons in the Clare-Bishop area of the cat. Acta Neurobiol. Exp. 35: 189-208. 34. WRIGHT, M. J. 19169. Visual mceptive fields of cells in a cortical area remote f r o m t h e striate cortex in the cat. Nature 223: 873-975. 35. ZERNICKI, B. 1968. Pretsigerninal cat: a review. Brain Res. 9: 1-14. Accepted 11 February 1985
