RECEPTIVE FIELDS AND RESPONSE PROPERTIES OF NEURONS IN THE RAT VISUAL CORTEX’ C. SHAW’.U. YINONand E. AUERBACH Vision Research Laboratory. Hadassah University Hospital. Jerusalem. Israel (Received 3 May 197-t) Abstract-Most receptive fields of neurons in the visual cortex (area 17) of rats could be mapped with moving and stationary stimuli. Neurons were most effectively driven by moving stimuli. They were classified as motion (37 per cent). orientation (I I per cent). or direction selective (4 per cent) and indefinite cells (41 per cent). Many cells had only a weak response to stationary stimuli: however, pure “on”. “off’ or “on-off’ receptive fields were found for some neurons; others were of the complex type with mixed response regions in the receptive field. Receptive field sizes were usually quite large (range of the major receptive field axes for the most common class of cells--motion selective-was I5’-50’) as expected considering the sizes of retinal ganglion and LGN cell receptive fields as found in the rat by other investigators. ISTRODUCTION
The processing of information by neurons of the visual cortex has been extensively investigated for the cat (Hubel and Wiesel 1959, 1962; Spinelli and Barrett 1969; Bishop and Henry 1972; Bishop, Coombs and Henry 19733,and lessextensively for the rabbit (Arden, Ikeda and Hill 1967; Chow, Masland and Stewart 1971) and monkey (Hubel and Wiesel 1967; Poggio 1972). Neuronal activity in the visual cortex of the rat has been scarcely investigated (Montero, Rojas and Torrealba 1973; Shaw. Yinon and Auerbach 1974). The exploration of receptive field properties of visual cortical cells in rats offers an opportunity to study an animal with a relatively primitive visual system and lateral vision. Comparison of properties of neurons in the rat to species with more complex vision may allow a better understanding of receptive field properttes and the development of these properties in higher mammals. We report here the results of experiments on receptive field organization and properties of neurons of the rat visual cortex. Preliminary results with the rat of neural properties and retinotopic organization have appeared in the literature (Montero, Rojas and Torrealba 1973; Shaw, Yinon and Auerbach 1974). XIETHODS Thirty-two albino adult rats (2oCr6OOg) of the Sabra Strain of the Hebrew University, both males and females. were used. Using the albino type. no differences in receptive field size or organization of retinal ganglion and LGN cells. in comparison to the pigmented raf were found (Brown and Rojas 1965; Montero and Brugge 1969). ’ Research supported by Stiftung Volkswagenwerk under contract number I I 1538. L Present address: Department of Zoology. Hebrew University of Jerusalem. Jerusalem, Israel. -.
Anesthesia was provided by urethane (ethyl carbamate) 120-135 mg/kg i.p. Additional urethane (IC-20 per cent of the initial dose) was given during the experiment as needed. Urethane provides a stable. long lasting anesthesia; furthermore. it seems not to affect receptive field properties of rat retinal ganglion, lateral geniculate or superior colliculus neurons (Brown and Rojas 1965; Montero and Brugge 1969: Humphrey 1965). Maintained unit activity in rat hypothalamus and cortex seems also to be unaffected (Holmes and Houchin 1966; Cross and Dyer 1971). However, some effects of urethane on neuron properties in the cortex cannot be totally discounted: initially, urethane in the dosages used produced a profound depression of cortical activity lasting for a number of hours. Usually, for this reason. 6-24 hr were allowed to elapse before commencing unit recordings. A suitable state for unit recording was when a pinch to a hind paw elicited only a weak withdrawal reflex. In addition to the general anesthesia. incisions and pressure points were infiltrated i.m., with lignocaine (2 per cent) or covered with benzocaine ointment (IO per cent). The eyes were dilated with 1-2 per cent atropine sulfate. Dextrose (5 per cent) in saline was administered, i.p., at regular intervals. When respiratory problems due to urethane occurred, atropine sulfate (2 per cent) was administered i.m. The refractive error was determined by ophthalmoscopy in all rats prior to the experiments. The measurements have shown a refractive error of between + 7 and + I ID. This is in agreement with Block (1969) and Massof and Chang (I 972) who found hypermetropia in the rat. Other investigators (Brown and Rojas 1965; Montero, Brugge and Beitel 1968) claimed, on the other hand. that the rat is a myopic animal. During the experiments. lenses of the appropriate diopter plus a correction for the distance to the screen were placed before the eyes. Standard surgical techniques were used to expose the visual cortex bi- or unilaterallv. The dura was reflected and the exposed cortex covered w’ith mineral oil or +S% agar in normal saline. The animals’ body temperature (rectal) was maintained between 35 and 38°C with a d.c. heating pad or water bottle. The eyes were kept moist by frequent rinsing with normal saline. Animals were kept in the darkadapted state during all electrophysiological recordings.
203
Eke movements were rarely encountered using deep urethane anesthesia. In order to avoid eye movements in cases uith fighter anesthesia. adjustable silver rings were pressed lirml! around e3ch eye and securely attached to thz sterrotaxic apparatus: in some experiments. the conjunctiva was sutured to the ring. Microelectrodes were prepared irom stainless steel insect pins sharpened electrolytically to a tip diameter of l-5 pm and coated with 1x4-x or GC No. 56-1 (Waisco) insulating and dipping varnish. Unit activity was conventionally amplified by Grass AC P5l I preamplifier and filtered at 200 cis-3 kc s (Multimetrics AF-200 Active tiltcr). An HIP 511 Probe was connected between the microelectrode and the preampli~er. Spikes were monitored by a loudspeaker. The indifferent electrode was a metal clamp connected to the scalp. Unit activity was recorded by means of a tape recorder (Ampex SP3OO)or photographed. Stimulus pulses were recorded on a separate channel. For the recordings the rat visual cortex was identified using the maps of Krieg (1916a.b) and Yinon and Auerbach (1972). Electrode penetrations were made perpendicular to the cortical surface and the location was measured from either bregma or iambda by means of a Baltimore stereotaxic apparatus and micromanipulator. Only units no deeper than 1.15 mm in the cortex were considered (KGnig and Klippel 1963: Albe-Fessard er a[.. 1973).Most cells were recorded at depths between 0.5 and I.Omm. Histological controls were made with several animals in order to establish depth of the cortex for different regions. These measurements allowed a strong confidence that the units recorded were actually of cortical origin. Cells were found by slowly advancing the microelectrode in steps of 1j recorded and analyzed for 3 min periods. RESCLTS The cortical map for single units activated by visual stimuli was found to be similar to that one obtained previously with the VEP (Yinon and Auerbach 1973). Most recordings were made from area 17: only a few cells were recorded from area 18. No preference was found in the distribution of the different types of neurons by cortical area OF depth. Cell clusters were often found which extended over several hundred microns. These usually had overlapping receptive fields and similar response properties. Similar cell clusters have been reported for rabbit visual cortex (Hughes 1971). No evidence for cortical columns was found: adjacent cells in an electrode penetration could have different response properties and spatial positions. However. we cannot exclude differences due to slight experimental errors such as the angle ofelectrode penetration. Xany units responded to diffuse light stimulation but the responses were much waker than to discrete stationary or moving stimuli. The response to diffuse Iight often showed either kilitntion or inhibition to binocular stimuli (Shaw. Yinon and Aucrbach 1974). Receptive field sizes. mapped with stationary or moving stimuli. were usually quite large. Figure 1 shows receptive field sizes for rat cortical neurons compared to receptive field sizes of the cat (Hubel and Wiese1 1967) recorded from the area centralis projection area. The enormous difference between these species is
CAT
RAI
Fig. 1. Comparison betivsen receptive field sizes of neurons from the visual cortex of rat and cat. Per cent of total for the mt (36 neurons} and cat (I 19 neurons!. The histogram for the cat has been pooled from simple and complex cells {Hrtbel and %‘eisel 1962. Fig. 9).
Receptive fields and response properties SpikQS
ld-
4-i 13’
Fig. 2. Receptive field of a motion-selective cell of the rat visual cortex plotted by stationary light of spots of -1’ dia. Light intensity I4 R-c.; no background illumination was
used. 0 “off’ response: q “on-off’ response; 0 no response. Density of lines indicate strength of responses. readily apparent. and expected considering the differences between them in receptive field sizes of retinal ganglion and LGN cells (Hubel and Wiesel 1961; Brown and Rojas 1965; Montero, Brugge and Beitel 1968; Ikeda and Wright 1972). Many units were not responsive to stationary stimuli. However, some units mapped with small spots of light or bars showed complex receptive fields (Hubel and Wiesel 1962) composed of mixed “on”, “off” or “on-off” regions, without any apparent concentric or
c
I
0
45
&
Fig. 3. Post stimulus time histograms (PSTHs) showing response of a motion-selective cell of the rat visual cortex to a moving stimulus. The stimulus was a slit (20.2’ x 1.74’). moved with different orientations through the receptive field (8.6’ x 20.2’) at a speed of 7’;~. Light intensity 14ft-c. Ten repetitions were made.
26O Drg /sec.
39O
Fig. 4. Response of a motion-selective cell to different speeds of movement of a vertical slit (25’ x 1.1’). Light intensity I.4 ft-c. Receptive field size 57.3’ x 25’. The graph was made from histograms (10 repetitions at each speed) and shows the average number of spikes per sweep in either the nasal to temporal direction (O---O) or the temporal to nasal direction (-0).
zones (Fig. 2). Other cells had homogenous receptive fields to stationary stimuli. firing only at “on” or “off” or “on-off’. Similar responses to stationary stimuli were reported by Humphrey (1965) for rat superior colliculus neurons. Table I shows the distribution of cell types. classified particularly on the basis of their response to moving visual stimuli in the contralateral visual field. Four types of cells were found, classified after Chow, Masland and Stewart (1972). Motion selective cells responded optimally to stimuli of any size or orientation moving in any direction through their receptive fields (Fig. 3). The majority of receptive fields were elongated in either the vertical or horizontal axis. Usually white as well as black stimuli were effective. The range of lengths of the major receptive field axes was 15-50”. with an exceptional case measuring 115”.Most cells showed little specificity for speed of movement. Stimuli moving as slowly as IO’/ set or as rapidly as l8O”/sec typically elicited bursts of firing as the stimulus crossed the receptive field. Furthermore, cells which failed to respond to very slow stimulus, were broadly tuned for medium or fast speeds. In a few cases, however, some speed specificity was noted (Fig. 4). Orientation selective cells resemble complex cells of the rabbit (Chow, Masland and Stewart 1972). The significant feature of these cells was that the stimulus eliciting the maximum response was always a moving slit or black bar with a particular orientation parallel to the long axis of the receptive field. Stimuli of other orientations elicited weaker responses; however, these cells were normally broadly tuned for orientation adjacent
206
C. SHAW.
L’. YINON
and E. AUERBACH
Spontaneous activity
Fig. 5. Orientation-selective cell of the rat visual cortex. Responses to a slit (6.9” x 1.9”)moving at a speed of about 17”/ sec. Receptive field size: 6.9” x 7.2’. Light intensity 1.4 ft-c. Calibration 03 sec. Spikes are redrawn from the film record.
selectivity (Fig. 5). The weakest response was at an orientation 90’ to the preferred orientation. Different cells preferred different orientations and no apparent preference for any particular orientation was found. The lengths of the major receptive field axis ranged from 5’ to 30”. Direction selective cells comprised only a small part of the cortical cell population. They fired maximally to a stimulus moving in a given direction and failed to respond or showed inhibition of the maintained activity with stimulus movement in the opposite (null) direction. The significant feature of these cells was that the non-responsive direction was at 180” to the optimal direction. Sometimes other directions of stimulus movement could drive a cell. However. the activity was inferior to that in the optimal direction. In most cases, the preferred direction to moving stimuli was perpendicular to the long axis of the receptive field if the cells were also orientation selective; otherwise the preferred direction was along the long axis of the receptive field as observed in few cells. The size range for the major receptive field axis was IO”-30”. The direction selective properties were not due to optical distortions (e.g. astigmatism) or light scatter since both black and white stimuli elicited the direction selective response.. Indefinite cells comprised a large number of cells in the rat visual cortex. Although visually evoked, no consistent response to visual stimuli could be elicited (Fig. 6). The significant feature of these cells was the fact that no discrete receptive field could be mapped. Most of these indefinite cells fired to diffuse light stimuli, light spots and moving slits in many areas of the visual field and for all stimulus sizes and orientations. There were, however, some cells which responded only to stationary and diffuse light stimuli;
Fig. 6. PSTHs of an indefinite cell of the rat visual cortex. The stimulus was a vertical slit (33.4‘ x I.6 I moving at a speed of 14’/sec. Light intensity I.4 R-c. The two histograms were made from eight sweeps in each direction and compared to spontaneous rate for the same number of sweeps.
others only to moving stimuli. Furthermore. habituation was common for these cells. A small number of cells was found in area 17 which were not responsive to visual stimuli. They seemed to have normal spontaneous activity and could often be held for long periods of time while both eyes were stimulated. It is possible that these cells require only more specific or complex visual stimuli than provided in the present experiments. Spontaneous activity of most cells with a specific response to visual stimuli was low with a mean rate of 3.8 spikes/set. Considering only those cells with rates of higher than 1 spikeisec. the range was from I spike: set to about 20 spikesisec. Time intervals and patterns of firing were similar to that of neurons of the cat visual cortex (Griffith and Horn 1966; Sanseverino, Agnati and Maroli 1973). No correlation between spontaneous activity and cell response type was noted.
DISCL’SSION
Receptive field size and responses to movement. orientation and direction of neurons of the rat visual cortex are similar to those of the other lower mammalian species with almost pure rod retinae such as the rabbit, the opossum and the mouse, although the number of cells in each group differ (Chow, Masland and Stewart I97 I ; Rocha-Miranda et ol.. 1973; Hubel 1974). As in these species the optimal stimulus for the rat cortical neurons is movement. Responses to diffuse or stationary stimuli were comparatively weak. However, receptive field organization is similar to that of complex cells of the cat visual cortex (Hubel and Wiese1 1962).
207
Receptive fields and response properties Table 1.
Rat: Rabbit (Chow er al. 1972)
Hyper-
Concentric
Uniform
Motion
Direction selectivet
Simple
Complex*
complex
Indefinite
response
0 I’-
0 3
37 I5
4 19
0 17
II 8
0 4
II 13
7 9
NO
In our classification all orientation selective cells were like complex cells of the rabbit. t All these cells were classified by us as direction selective regardless of whether they were also orientation selective, as most of them were. : Some cells with normal activity from “normal” cortex of monocularly deprived rats are also included. l
Receptive field sizes for most cells in the rat cortex were quite large and about similar in size to the receptive fields of the opossum (Rocha-Miranda et al., 1973) and the rabbit (Chow, Masland and Stewart 1971). In contrast, receptive fields from cat and monkey cortical cells are much smaller (Hubel and Wiesel 1962; Poggio 1972). Our classification of cell types (as mentioned in the Results section) is based on that of Chow, Masland and Stewart (1971) for the rabbit. However, some cell types reported by them were not found in the rat and the number ofcells in each group differed between species. Table 1 shows the percentage of cells in each group of the present study and for the rabbit. Cells similar to the. motion cells studied here have been described for the opossum (Rocha-Miranda et a/., 1973), rabbit (Chow, Masland and Stewart 1971) and monkey cortex (Poggio 1972) and for the rat superior colliculus (Humphrey 1968). Orientation and direction selective cells have been described for opossum (Rocha-Miranda et al.. 1973) rabbit (Chow, Masland and Stewart 1971). cat and monkey cortex (Hubel and Wiesel 1962; Poggio 1972). These cells are usually divided into simple and complex cells on the basis of the organization of the receptive field mapped with stationary stimuli. Most of the cells found by us in the rat cortex are complex; we found no simple receptive fields in this study. Further, no concentrically organized receptive fields or hypercomplex cells were found. The large number of cells with indefinite response properties was thought for a time to be a result of anesthesia or refractive error of the eye. However, indefinite cells were often found immediately before or after recording from cells with specific response properties with the animal at the same anesthetic level and with the same refractive correction. Furthermore. similar cell types have been reported for the visual cortex of the unanesthetized rabbit (Chow, Masland and Stewart 1971) and cat (Spinelli and Barrett 1969). The linear relationship between receptive field size and distance from area centralis found in cats (Ikeda and Wright 1972) indicates that detailed vision needs “fine grain” receptive fields. From the results of the
present study with the large dimensions of receptive fields and the non-specific properties of most cells, it seems unlikely that the rat possesses detailed pattern vision. Priority is probably given to any object moving in the visual field, disregarding its shape. Behavioral experiments with the rat seem to fit the electrophysiological findings (Herman 1958; Sutherland. Carr and Mackintosh 1962). REFERENCES
Albe-Fessard D., Stutensky F.. Libouban S. and hleonard P. (1973) Alas stereotaxique dw dirncephal du rat blanc. Ed. Centre Nat. Res. Scie. Arden G. B.. Ikeda H. and Hill R. M. (1967) Rabbit visual cortex: Reaction of cells to movement and contrast. Nature. Land. 214. 909-912. Bishop P. 0.. Coombs J. S. and Henry G. H. (1973) Receptive fields of simple cells in the cat striate cortex. J. P/IJ siol. 231. 3 I-60. Bishop P. 0. and Henry G. H. (1972) Striate neurons: Receptive field concepts. Incest. Ophthal. 1I, 346-354. Blau D. (1971) A simple device for moving an electrically driven micromanipulator. Electroenceph. ch. .Veurophysiol. 30, 465. Block M. T. (1969) A note on the refraction and image formation of the rat’s eye. Vision Res. 9, 705-712. Brown J. E. and Rojas J. A. (1965) Rat retinal ganglion cells: Receptive field organization and maintained activity. J. NeurophysioL 28. 1073-1090. Chow K. L., Masland R. H. and Stewart D. L. (1971) Receptive field characteristics of striate cortical neurons in the rabbit. Brain Res. 33. 337-351. Cross B. A. and Dyer R. G. (1971) Unit activity in rat diencephalic islands-the effect of anesthetics. J. Ph,rsiol. 212, -167-451. Griffith J. S. and Horn G. (1966) an analysis of spontaneous impulse activity of units in the striate cortex of unrestrained cats. J. Physiol. 186, 516-534. Hermann G. (19%) Beitrlte zur Physiologie des Rattenauges. Z. Tierpsycho/. 15,462-5 18. Holmes 0. and Houchin J. (1966) Units in the cerebral cortex of the anesthetized rat: The correlations between their discharges. J. Phpiol. 187, 65 l-67 I. Hubel D. H. (1974) Personal communication. Hubel D. H. and Wiesel T. N. (1959) Receptive fields of single neurons in cat’s striate cortex. J. Phpsiol. 148, 574591.
Hubzl D H. snd n’ierel T N. (19611 Integrative action m the cat‘s lateral yenlcuiatr bad). 1. Phxsiol. 1%. X1%39% Hub& D. H. and IView T. X f I9615 Receptive fields. binocuIar interattion. and functionai archittcture in the cat’s visual cortex. f. Pitysial. I#. I&-i5-L Wubrf D H. and =A%scl f. Ii;. il967) Receptive fields and
functional architecture of monkey striate cortex. i. Phv.siai. 195. 3 I CJJ3. Hughes .A.(1971I Topographical relationships betwzn anatomy and physiology of the rabbit visual system. DowJ)IL’I!fti opiriir. 311.33-i 60.
ikedn H. and iVright hl. J. (1971) DifQrenrial effects of refractive errors and recepti\s field organization of central and peripheral ganglion cslIs. ~‘~SXVI Res. 12, l-165 1-176. K&i: J. F. R. and Klippef R. .A. [I9631 7% Rnr Br&: ‘-1 Sfmwrssic .ffh. Ct’itliams 6;: Wiikins. Baltimore. Krieg W. J. S. (I94hat Connections of the cerebral cortex. The albino rat. A. Topography of the cortical areas. J. Co1rrp..Verrroi.84. 13 l-175. Krieg W. J. S. (1946b) Connections of the cerebral cortes. The albino r;lt. B. Structure of the cortical area. J. ctwi~?..vMd 8-t. n-24. !&sd R. W. and ChangF. ts. { I9Z) .A resision of the rat schem;ttic e!r. i isinjr Res. $2. 793-796. M~~del J. and 5non G. (19731 Electronic controt of microelectrodes b? parts of a micron. E:lrctrorrw?@, Ch aYrwc~p/r~~~~~l. 31, 553-5%.
Xiontero V. 5L. and Bcugge 1. F. (1969) Direction of movement as the significant stimulus parameter for some laterat geniculat; cells in the rat. E’iGwtRrs. 9. ?I-%. Montero V. M.. Brwse Relation _- J. F. and Beitei R. E. f 19651 of the visual field to the lateral geniculate body of the albino rat. j. .Yeuroplr~siol. 31, 21 t-356. Montrro V. 51.. Rojas A. and Torrealba F. i 1973) Retinotopit organization of striate and peristriatrr visual cortex in the albino rat. Brairl Res. 53, 197-201. Poggio G. F. (1971) Spatial properties of neurons in striate cortex of unanest~et~zed macaque monkey. Inwsr. Oylrrlrai. 11, 368-377. Rocha-Miranda C. E,. Bombardieri R. A. Jr.. de Monasterio F, M. and Linden R. (1973) Receptive iields in the visual cortex of the opossum. Brain Rrs. 63. 361-367. Sanseverino E. R.. Agnati L. F.. Maroli 11. G. and Galletti C. (1973) Maintained activity of single neurons in striate and non-striate areas of cat visual cortex. Brain Rrs. 54, 123-242. Shaw f.. Yincn U. and Auerbach E. ji974 Single unit activity in the rat visual cwtex. Vision Res. 11. 3 11-Z I_%
Spinelli D. N. and Barrett T. W. (19691 Visual receptive fields ofsingle units in the cat’s visual,cortsx. E.xpl. .Vrurol. 24, 76-98. Sutherland N. S.. Carr A. E. and Mackintosh J. A. (1962) Visual discrimination of open and ciosed shapes by rats. 1. Trair&g Q. JI
The processing of information by neurons of the visual cortex has been extensively investigated for the cat (Hubel and Wiesel 1959, 1962; Spinelli and Barrett 1969; Bishop and Henry 1972; Bishop, Coombs and Henry 19733,and lessextensively for the rabbit (Arden, Ikeda and Hill 1967; Chow, Masland and Stewart 1971) and monkey (Hubel and Wiesel 1967; Poggio 1972). Neuronal activity in the visual cortex of the rat has been scarcely investigated (Montero, Rojas and Torrealba 1973; Shaw. Yinon and Auerbach 1974). The exploration of receptive field properties of visual cortical cells in rats offers an opportunity to study an animal with a relatively primitive visual system and lateral vision. Comparison of properties of neurons in the rat to species with more complex vision may allow a better understanding of receptive field properttes and the development of these properties in higher mammals. We report here the results of experiments on receptive field organization and properties of neurons of the rat visual cortex. Preliminary results with the rat of neural properties and retinotopic organization have appeared in the literature (Montero, Rojas and Torrealba 1973; Shaw, Yinon and Auerbach 1974). XIETHODS Thirty-two albino adult rats (2oCr6OOg) of the Sabra Strain of the Hebrew University, both males and females. were used. Using the albino type. no differences in receptive field size or organization of retinal ganglion and LGN cells. in comparison to the pigmented raf were found (Brown and Rojas 1965; Montero and Brugge 1969). ’ Research supported by Stiftung Volkswagenwerk under contract number I I 1538. L Present address: Department of Zoology. Hebrew University of Jerusalem. Jerusalem, Israel. -.
Anesthesia was provided by urethane (ethyl carbamate) 120-135 mg/kg i.p. Additional urethane (IC-20 per cent of the initial dose) was given during the experiment as needed. Urethane provides a stable. long lasting anesthesia; furthermore. it seems not to affect receptive field properties of rat retinal ganglion, lateral geniculate or superior colliculus neurons (Brown and Rojas 1965; Montero and Brugge 1969: Humphrey 1965). Maintained unit activity in rat hypothalamus and cortex seems also to be unaffected (Holmes and Houchin 1966; Cross and Dyer 1971). However, some effects of urethane on neuron properties in the cortex cannot be totally discounted: initially, urethane in the dosages used produced a profound depression of cortical activity lasting for a number of hours. Usually, for this reason. 6-24 hr were allowed to elapse before commencing unit recordings. A suitable state for unit recording was when a pinch to a hind paw elicited only a weak withdrawal reflex. In addition to the general anesthesia. incisions and pressure points were infiltrated i.m., with lignocaine (2 per cent) or covered with benzocaine ointment (IO per cent). The eyes were dilated with 1-2 per cent atropine sulfate. Dextrose (5 per cent) in saline was administered, i.p., at regular intervals. When respiratory problems due to urethane occurred, atropine sulfate (2 per cent) was administered i.m. The refractive error was determined by ophthalmoscopy in all rats prior to the experiments. The measurements have shown a refractive error of between + 7 and + I ID. This is in agreement with Block (1969) and Massof and Chang (I 972) who found hypermetropia in the rat. Other investigators (Brown and Rojas 1965; Montero, Brugge and Beitel 1968) claimed, on the other hand. that the rat is a myopic animal. During the experiments. lenses of the appropriate diopter plus a correction for the distance to the screen were placed before the eyes. Standard surgical techniques were used to expose the visual cortex bi- or unilaterallv. The dura was reflected and the exposed cortex covered w’ith mineral oil or +S% agar in normal saline. The animals’ body temperature (rectal) was maintained between 35 and 38°C with a d.c. heating pad or water bottle. The eyes were kept moist by frequent rinsing with normal saline. Animals were kept in the darkadapted state during all electrophysiological recordings.
203
Eke movements were rarely encountered using deep urethane anesthesia. In order to avoid eye movements in cases uith fighter anesthesia. adjustable silver rings were pressed lirml! around e3ch eye and securely attached to thz sterrotaxic apparatus: in some experiments. the conjunctiva was sutured to the ring. Microelectrodes were prepared irom stainless steel insect pins sharpened electrolytically to a tip diameter of l-5 pm and coated with 1x4-x or GC No. 56-1 (Waisco) insulating and dipping varnish. Unit activity was conventionally amplified by Grass AC P5l I preamplifier and filtered at 200 cis-3 kc s (Multimetrics AF-200 Active tiltcr). An HIP 511 Probe was connected between the microelectrode and the preampli~er. Spikes were monitored by a loudspeaker. The indifferent electrode was a metal clamp connected to the scalp. Unit activity was recorded by means of a tape recorder (Ampex SP3OO)or photographed. Stimulus pulses were recorded on a separate channel. For the recordings the rat visual cortex was identified using the maps of Krieg (1916a.b) and Yinon and Auerbach (1972). Electrode penetrations were made perpendicular to the cortical surface and the location was measured from either bregma or iambda by means of a Baltimore stereotaxic apparatus and micromanipulator. Only units no deeper than 1.15 mm in the cortex were considered (KGnig and Klippel 1963: Albe-Fessard er a[.. 1973).Most cells were recorded at depths between 0.5 and I.Omm. Histological controls were made with several animals in order to establish depth of the cortex for different regions. These measurements allowed a strong confidence that the units recorded were actually of cortical origin. Cells were found by slowly advancing the microelectrode in steps of 1j recorded and analyzed for 3 min periods. RESCLTS The cortical map for single units activated by visual stimuli was found to be similar to that one obtained previously with the VEP (Yinon and Auerbach 1973). Most recordings were made from area 17: only a few cells were recorded from area 18. No preference was found in the distribution of the different types of neurons by cortical area OF depth. Cell clusters were often found which extended over several hundred microns. These usually had overlapping receptive fields and similar response properties. Similar cell clusters have been reported for rabbit visual cortex (Hughes 1971). No evidence for cortical columns was found: adjacent cells in an electrode penetration could have different response properties and spatial positions. However. we cannot exclude differences due to slight experimental errors such as the angle ofelectrode penetration. Xany units responded to diffuse light stimulation but the responses were much waker than to discrete stationary or moving stimuli. The response to diffuse Iight often showed either kilitntion or inhibition to binocular stimuli (Shaw. Yinon and Aucrbach 1974). Receptive field sizes. mapped with stationary or moving stimuli. were usually quite large. Figure 1 shows receptive field sizes for rat cortical neurons compared to receptive field sizes of the cat (Hubel and Wiese1 1967) recorded from the area centralis projection area. The enormous difference between these species is
CAT
RAI
Fig. 1. Comparison betivsen receptive field sizes of neurons from the visual cortex of rat and cat. Per cent of total for the mt (36 neurons} and cat (I 19 neurons!. The histogram for the cat has been pooled from simple and complex cells {Hrtbel and %‘eisel 1962. Fig. 9).
Receptive fields and response properties SpikQS
ld-
4-i 13’
Fig. 2. Receptive field of a motion-selective cell of the rat visual cortex plotted by stationary light of spots of -1’ dia. Light intensity I4 R-c.; no background illumination was
used. 0 “off’ response: q “on-off’ response; 0 no response. Density of lines indicate strength of responses. readily apparent. and expected considering the differences between them in receptive field sizes of retinal ganglion and LGN cells (Hubel and Wiesel 1961; Brown and Rojas 1965; Montero, Brugge and Beitel 1968; Ikeda and Wright 1972). Many units were not responsive to stationary stimuli. However, some units mapped with small spots of light or bars showed complex receptive fields (Hubel and Wiesel 1962) composed of mixed “on”, “off” or “on-off” regions, without any apparent concentric or
c
I
0
45
&
Fig. 3. Post stimulus time histograms (PSTHs) showing response of a motion-selective cell of the rat visual cortex to a moving stimulus. The stimulus was a slit (20.2’ x 1.74’). moved with different orientations through the receptive field (8.6’ x 20.2’) at a speed of 7’;~. Light intensity 14ft-c. Ten repetitions were made.
26O Drg /sec.
39O
Fig. 4. Response of a motion-selective cell to different speeds of movement of a vertical slit (25’ x 1.1’). Light intensity I.4 ft-c. Receptive field size 57.3’ x 25’. The graph was made from histograms (10 repetitions at each speed) and shows the average number of spikes per sweep in either the nasal to temporal direction (O---O) or the temporal to nasal direction (-0).
zones (Fig. 2). Other cells had homogenous receptive fields to stationary stimuli. firing only at “on” or “off” or “on-off’. Similar responses to stationary stimuli were reported by Humphrey (1965) for rat superior colliculus neurons. Table I shows the distribution of cell types. classified particularly on the basis of their response to moving visual stimuli in the contralateral visual field. Four types of cells were found, classified after Chow, Masland and Stewart (1972). Motion selective cells responded optimally to stimuli of any size or orientation moving in any direction through their receptive fields (Fig. 3). The majority of receptive fields were elongated in either the vertical or horizontal axis. Usually white as well as black stimuli were effective. The range of lengths of the major receptive field axes was 15-50”. with an exceptional case measuring 115”.Most cells showed little specificity for speed of movement. Stimuli moving as slowly as IO’/ set or as rapidly as l8O”/sec typically elicited bursts of firing as the stimulus crossed the receptive field. Furthermore, cells which failed to respond to very slow stimulus, were broadly tuned for medium or fast speeds. In a few cases, however, some speed specificity was noted (Fig. 4). Orientation selective cells resemble complex cells of the rabbit (Chow, Masland and Stewart 1972). The significant feature of these cells was that the stimulus eliciting the maximum response was always a moving slit or black bar with a particular orientation parallel to the long axis of the receptive field. Stimuli of other orientations elicited weaker responses; however, these cells were normally broadly tuned for orientation adjacent
206
C. SHAW.
L’. YINON
and E. AUERBACH
Spontaneous activity
Fig. 5. Orientation-selective cell of the rat visual cortex. Responses to a slit (6.9” x 1.9”)moving at a speed of about 17”/ sec. Receptive field size: 6.9” x 7.2’. Light intensity 1.4 ft-c. Calibration 03 sec. Spikes are redrawn from the film record.
selectivity (Fig. 5). The weakest response was at an orientation 90’ to the preferred orientation. Different cells preferred different orientations and no apparent preference for any particular orientation was found. The lengths of the major receptive field axis ranged from 5’ to 30”. Direction selective cells comprised only a small part of the cortical cell population. They fired maximally to a stimulus moving in a given direction and failed to respond or showed inhibition of the maintained activity with stimulus movement in the opposite (null) direction. The significant feature of these cells was that the non-responsive direction was at 180” to the optimal direction. Sometimes other directions of stimulus movement could drive a cell. However. the activity was inferior to that in the optimal direction. In most cases, the preferred direction to moving stimuli was perpendicular to the long axis of the receptive field if the cells were also orientation selective; otherwise the preferred direction was along the long axis of the receptive field as observed in few cells. The size range for the major receptive field axis was IO”-30”. The direction selective properties were not due to optical distortions (e.g. astigmatism) or light scatter since both black and white stimuli elicited the direction selective response.. Indefinite cells comprised a large number of cells in the rat visual cortex. Although visually evoked, no consistent response to visual stimuli could be elicited (Fig. 6). The significant feature of these cells was the fact that no discrete receptive field could be mapped. Most of these indefinite cells fired to diffuse light stimuli, light spots and moving slits in many areas of the visual field and for all stimulus sizes and orientations. There were, however, some cells which responded only to stationary and diffuse light stimuli;
Fig. 6. PSTHs of an indefinite cell of the rat visual cortex. The stimulus was a vertical slit (33.4‘ x I.6 I moving at a speed of 14’/sec. Light intensity I.4 R-c. The two histograms were made from eight sweeps in each direction and compared to spontaneous rate for the same number of sweeps.
others only to moving stimuli. Furthermore. habituation was common for these cells. A small number of cells was found in area 17 which were not responsive to visual stimuli. They seemed to have normal spontaneous activity and could often be held for long periods of time while both eyes were stimulated. It is possible that these cells require only more specific or complex visual stimuli than provided in the present experiments. Spontaneous activity of most cells with a specific response to visual stimuli was low with a mean rate of 3.8 spikes/set. Considering only those cells with rates of higher than 1 spikeisec. the range was from I spike: set to about 20 spikesisec. Time intervals and patterns of firing were similar to that of neurons of the cat visual cortex (Griffith and Horn 1966; Sanseverino, Agnati and Maroli 1973). No correlation between spontaneous activity and cell response type was noted.
DISCL’SSION
Receptive field size and responses to movement. orientation and direction of neurons of the rat visual cortex are similar to those of the other lower mammalian species with almost pure rod retinae such as the rabbit, the opossum and the mouse, although the number of cells in each group differ (Chow, Masland and Stewart I97 I ; Rocha-Miranda et ol.. 1973; Hubel 1974). As in these species the optimal stimulus for the rat cortical neurons is movement. Responses to diffuse or stationary stimuli were comparatively weak. However, receptive field organization is similar to that of complex cells of the cat visual cortex (Hubel and Wiese1 1962).
207
Receptive fields and response properties Table 1.
Rat: Rabbit (Chow er al. 1972)
Hyper-
Concentric
Uniform
Motion
Direction selectivet
Simple
Complex*
complex
Indefinite
response
0 I’-
0 3
37 I5
4 19
0 17
II 8
0 4
II 13
7 9
NO
In our classification all orientation selective cells were like complex cells of the rabbit. t All these cells were classified by us as direction selective regardless of whether they were also orientation selective, as most of them were. : Some cells with normal activity from “normal” cortex of monocularly deprived rats are also included. l
Receptive field sizes for most cells in the rat cortex were quite large and about similar in size to the receptive fields of the opossum (Rocha-Miranda et al., 1973) and the rabbit (Chow, Masland and Stewart 1971). In contrast, receptive fields from cat and monkey cortical cells are much smaller (Hubel and Wiesel 1962; Poggio 1972). Our classification of cell types (as mentioned in the Results section) is based on that of Chow, Masland and Stewart (1971) for the rabbit. However, some cell types reported by them were not found in the rat and the number ofcells in each group differed between species. Table 1 shows the percentage of cells in each group of the present study and for the rabbit. Cells similar to the. motion cells studied here have been described for the opossum (Rocha-Miranda et a/., 1973), rabbit (Chow, Masland and Stewart 1971) and monkey cortex (Poggio 1972) and for the rat superior colliculus (Humphrey 1968). Orientation and direction selective cells have been described for opossum (Rocha-Miranda et al.. 1973) rabbit (Chow, Masland and Stewart 1971). cat and monkey cortex (Hubel and Wiesel 1962; Poggio 1972). These cells are usually divided into simple and complex cells on the basis of the organization of the receptive field mapped with stationary stimuli. Most of the cells found by us in the rat cortex are complex; we found no simple receptive fields in this study. Further, no concentrically organized receptive fields or hypercomplex cells were found. The large number of cells with indefinite response properties was thought for a time to be a result of anesthesia or refractive error of the eye. However, indefinite cells were often found immediately before or after recording from cells with specific response properties with the animal at the same anesthetic level and with the same refractive correction. Furthermore. similar cell types have been reported for the visual cortex of the unanesthetized rabbit (Chow, Masland and Stewart 1971) and cat (Spinelli and Barrett 1969). The linear relationship between receptive field size and distance from area centralis found in cats (Ikeda and Wright 1972) indicates that detailed vision needs “fine grain” receptive fields. From the results of the
present study with the large dimensions of receptive fields and the non-specific properties of most cells, it seems unlikely that the rat possesses detailed pattern vision. Priority is probably given to any object moving in the visual field, disregarding its shape. Behavioral experiments with the rat seem to fit the electrophysiological findings (Herman 1958; Sutherland. Carr and Mackintosh 1962). REFERENCES
Albe-Fessard D., Stutensky F.. Libouban S. and hleonard P. (1973) Alas stereotaxique dw dirncephal du rat blanc. Ed. Centre Nat. Res. Scie. Arden G. B.. Ikeda H. and Hill R. M. (1967) Rabbit visual cortex: Reaction of cells to movement and contrast. Nature. Land. 214. 909-912. Bishop P. 0.. Coombs J. S. and Henry G. H. (1973) Receptive fields of simple cells in the cat striate cortex. J. P/IJ siol. 231. 3 I-60. Bishop P. 0. and Henry G. H. (1972) Striate neurons: Receptive field concepts. Incest. Ophthal. 1I, 346-354. Blau D. (1971) A simple device for moving an electrically driven micromanipulator. Electroenceph. ch. .Veurophysiol. 30, 465. Block M. T. (1969) A note on the refraction and image formation of the rat’s eye. Vision Res. 9, 705-712. Brown J. E. and Rojas J. A. (1965) Rat retinal ganglion cells: Receptive field organization and maintained activity. J. NeurophysioL 28. 1073-1090. Chow K. L., Masland R. H. and Stewart D. L. (1971) Receptive field characteristics of striate cortical neurons in the rabbit. Brain Res. 33. 337-351. Cross B. A. and Dyer R. G. (1971) Unit activity in rat diencephalic islands-the effect of anesthetics. J. Ph,rsiol. 212, -167-451. Griffith J. S. and Horn G. (1966) an analysis of spontaneous impulse activity of units in the striate cortex of unrestrained cats. J. Physiol. 186, 516-534. Hermann G. (19%) Beitrlte zur Physiologie des Rattenauges. Z. Tierpsycho/. 15,462-5 18. Holmes 0. and Houchin J. (1966) Units in the cerebral cortex of the anesthetized rat: The correlations between their discharges. J. Phpiol. 187, 65 l-67 I. Hubel D. H. (1974) Personal communication. Hubel D. H. and Wiesel T. N. (1959) Receptive fields of single neurons in cat’s striate cortex. J. Phpsiol. 148, 574591.
Hubzl D H. snd n’ierel T N. (19611 Integrative action m the cat‘s lateral yenlcuiatr bad). 1. Phxsiol. 1%. X1%39% Hub& D. H. and IView T. X f I9615 Receptive fields. binocuIar interattion. and functionai archittcture in the cat’s visual cortex. f. Pitysial. I#. I&-i5-L Wubrf D H. and =A%scl f. Ii;. il967) Receptive fields and
functional architecture of monkey striate cortex. i. Phv.siai. 195. 3 I CJJ3. Hughes .A.(1971I Topographical relationships betwzn anatomy and physiology of the rabbit visual system. DowJ)IL’I!fti opiriir. 311.33-i 60.
ikedn H. and iVright hl. J. (1971) DifQrenrial effects of refractive errors and recepti\s field organization of central and peripheral ganglion cslIs. ~‘~SXVI Res. 12, l-165 1-176. K&i: J. F. R. and Klippef R. .A. [I9631 7% Rnr Br&: ‘-1 Sfmwrssic .ffh. Ct’itliams 6;: Wiikins. Baltimore. Krieg W. J. S. (I94hat Connections of the cerebral cortex. The albino rat. A. Topography of the cortical areas. J. Co1rrp..Verrroi.84. 13 l-175. Krieg W. J. S. (1946b) Connections of the cerebral cortes. The albino r;lt. B. Structure of the cortical area. J. ctwi~?..vMd 8-t. n-24. !&sd R. W. and ChangF. ts. { I9Z) .A resision of the rat schem;ttic e!r. i isinjr Res. $2. 793-796. M~~del J. and 5non G. (19731 Electronic controt of microelectrodes b? parts of a micron. E:lrctrorrw?@, Ch aYrwc~p/r~~~~~l. 31, 553-5%.
Xiontero V. 5L. and Bcugge 1. F. (1969) Direction of movement as the significant stimulus parameter for some laterat geniculat; cells in the rat. E’iGwtRrs. 9. ?I-%. Montero V. M.. Brwse Relation _- J. F. and Beitei R. E. f 19651 of the visual field to the lateral geniculate body of the albino rat. j. .Yeuroplr~siol. 31, 21 t-356. Montrro V. 51.. Rojas A. and Torrealba F. i 1973) Retinotopit organization of striate and peristriatrr visual cortex in the albino rat. Brairl Res. 53, 197-201. Poggio G. F. (1971) Spatial properties of neurons in striate cortex of unanest~et~zed macaque monkey. Inwsr. Oylrrlrai. 11, 368-377. Rocha-Miranda C. E,. Bombardieri R. A. Jr.. de Monasterio F, M. and Linden R. (1973) Receptive iields in the visual cortex of the opossum. Brain Rrs. 63. 361-367. Sanseverino E. R.. Agnati L. F.. Maroli 11. G. and Galletti C. (1973) Maintained activity of single neurons in striate and non-striate areas of cat visual cortex. Brain Rrs. 54, 123-242. Shaw f.. Yincn U. and Auerbach E. ji974 Single unit activity in the rat visual cwtex. Vision Res. 11. 3 11-Z I_%
Spinelli D. N. and Barrett T. W. (19691 Visual receptive fields ofsingle units in the cat’s visual,cortsx. E.xpl. .Vrurol. 24, 76-98. Sutherland N. S.. Carr A. E. and Mackintosh J. A. (1962) Visual discrimination of open and ciosed shapes by rats. 1. Trair&g Q. JI
