tactile discrimination of surface curvature and shape...

J. Exp. Biol. (1964), 41, 433-445 4 3 3With 6 text-figures

Printed in Great Britain

TACTILE DISCRIMINATION OF SURFACE CURVATUREAND SHAPE BY THE OCTOPUS

BY M. J. WELLS

Department of Zoology, University of Cambridge

(Received 5 December 1963)

INTRODUCTION

Octopuses can readily be taught to distinguish between objects that differ in surfacetexture, or in taste. But they cannot be taught to recognize the distribution of irregu-larities on the surface of objects, or to discriminate between objects that differ only inweight (Wells, 1961a, 19636, Wells & Wells, 1956, 1957).

In visual experiments the animals can recognize the orientation of things that theysee, provided that the statocysts are intact. If these are removed, a reflex mechanismgoverning the orientation of the retina is upset, and discrimination fails (Wells, i960).In experiments with a maze, in which octopuses were required to learn to make adetour in order to get food, correct orientation was found to depend upon the main-tenance of visual contact with the partitions separating the octopus from its goal. Theanimals performed satisfactorily after removal of both statocysts but unilateral blind-ing led to systematic errors in which the octopuses regularly turned through 1800

without learning that this invariably led to a failure to collect the reward (Wells, 19646).These results all suggest that octopuses are unable to use information about the

position of parts of their own bodies (or their own orientation in space) as a basis forlearned responses. It is arguable that this state of affairs is not altogether surprisingin view of the extreme flexibility of the animal; that in a very flexible animal motorcontrol must of necessity be hierarchical and proprioceptive information must beutilized locally, a condition perhaps common to all animals which lack jointedskeletons. In such creatures proprioceptive inputs giving details of bodily positionprobably never penetrate to levels of the central nervous system concerned withlearned responses (Wells, 19616, 1963a).

In apparent contradiction of these results it was found that octopuses can distin-guish by touch between a sphere and a cube, a performance most readily explainedby supposing that the animals take into account the relative positions of the arms orsuckers used to grasp the objects. Transfer experiments, however, imply that this isnot the basis on which the octopus makes the discrimination. Instead it seems that theanimal must learn to recognize the presence of corners on the cube, not as right-anglechanges in plane, but as textural irregularities. Thus a narrow rod, presented to animalsalready trained to distinguish between a sphere and a cube, was treated as equivalentto the cube. Indeed it appeared from the experiments that the narrow rod used wasactually a ' better' cube, so far as the octopuses were concerned, since the proportionof errors made by the trained animals fell when it replaced the cube in a series ofdiscrimination experiments (Wells, 1964a).

28-2

434 M. J. WELLS

The experiments reported here follow up the cube/sphere discrimination experi-ments by showing that octopuses distinguish the diameter of rods touched from thedegree of distortion that these impose on the individual suckers in contact. It is sug-gested that this is the basis on which octopuses are sometimes able to distinguishbetween shapes in spite of being unable to recognize the relative positions of thesuckers in space.

MATERIALS AND METHODS

Octopus vtdgaris was used; the animals came from the Bay of Naples. Individualsweighed between 300 and 500 g. and were kept separately in large asbestos tanks withcirculating sea water. Each animal was kept under observation for 2 or 3 days and, assoon as it was feeding regularly, was operated upon, the optic nerves being cut on bothsides of the brain. Operational techniques have been described in Wells & Wells(1956, 1957). After blinding, the animals were fed frequently upon crabs and smallpieces offish. Training was started as soon as an individual was feeding regularly andvigorously grabbing food touched against any of the arms. In the text individualanimals are indicated by a letter and a number (Hio, J50, K2). The prefix H, J,and K show animals used in experiments during 1961, 1962 and 1963 respectively.

The animals were trained using a reward and punishment technique that has beenfully described elsewhere (Wells, 1962; Wells & Wells, 1956). At each trial one orother of two Perspex objects was presented by touching it gently against any con-veniently outstretched arm of the blind animal. The octopus was allowed to examinethe object and take or reject it. A positive response was scored if the test object waspassed under the interbrachial web towards the mouth, and the animal either rewardedwith a piece of fish, or punished by means of an 8 V. a.c. shock, given underwater bytouching the octopus with a pair of electrodes attached to a probe. If the animalresponded negatively, thrusting the object away or abandoning it after a few secondsexamination, the object was removed and no further action taken. There were fortytrials per day, carried out in two groups of twenty, systematized thus + — + — + +— — + - + — — + + — + —+ — (10 + , 10 — ). Individual trials in a groupwere at 5 min. intervals; the second group of the day was started not less than 6 hr.after the first. The animals had no pre-experimental contact with the test objects andthere was no pretraining to take the positive or reject the negative object.

Various test objects were used, all made from Perspex, with a bolt tapped into oneend for the attachment of a nylon line used to lower the object to the animals. Duringexamination and taking or rejecting of the object this line was left slack. The shapes anddimensions of the test objects are shown in Fig. 1.

EXPERIMENTAL RESULTS

(1) Experiments with cylinders

Octopuses were trained to discriminate between pairs of the cylinders shown inFig. 1. The cylinders differed in diameter, the smallest being 6 mm. across, the largest38 mm. The animals were trained for 200 trials in 10 groups of 20 trials at 40 trials perday. In all, 36 octopuses were trained in thirteen different discriminations. Three ofthe animals were used twice, the second set of trials being an impossible discrimination

Tactile discrimination of surface curvature and shape by the octopus 435

between two 19 mm. cylinders, carried out to show that the trial sequence did notinherently result in a ' discriminatory' score.

Preliminary experiments indicated that octopuses have no consistent preferencefor large or small cylinders within the range used. It was, however, thought possiblethat the animals might be more liable to fumble and drop relatively large heavy objectsand because of this the larger cylinder of any pair was generally used as the positivestimulus.

PC PSG

1 \

Cylinder cross-sections

°°oOOO6 8 12 19 ^ '

PSL

L J 30 mm.

Fig. 1. Test objects used in the experiments. All are drawn to the same scale, and all were madeof Perspex, with a flat-headed bolt threaded into the top for attaching a nylon line by whichthe object could be lowered to the octopus. In the text, cylinders from the main scries, hereshown as cross-sections only, are referred to by their diameter in millimetres, or by their unitdiameter followed by an asterisk in the case of the compound cylinders 6* and 8*. All were ofthe same length, 50 mm., excluding suspension bolt. Octopuses of the size used in the experi-ments have suckers ranging downwards from about 10 mm. diameter, measured when appliedto a flat glass surface.

Details of some typical experiments are given in Fig. 2. It is clear that octopusesdistinguish between some pairs of cylinders more readily than others, and that therelevant difference is not the ratio of the diameters of the cylinders. The distinctionbetween a 19 mm. cylinder and a 38 mm. cylinder was not, for example, made nearlyso readily as the distinction between cylinders of 6 and 12 mm. It is already knownthat octopuses cannot be taught to discriminate between objects differing in weight(Wells, 1961 a). There remains the possibility that their discrimination of cylinders ofdifferent diameter is based on differences in surface curvature.

The curvature of a cylindrical surface can be defined as the reciprocal of the radius,a figure that also expresses the bending moment required to fit a distortable object witha normally fiat surface around the cylinder. In Fig. 3 the proportion of errors made in

436 M. J. WELLS

a series of discrimination experiments is plotted against the difference in surfacecurvature measured in this way. Thirteen different pairs of cylinders were used and atotal of thirty-nine training experiments was made. Each point on Fig. 3 shows thenumber of mistakes that an individual octopus made in the second half of its trainingfor two hundred trials. There is considerable scatter in individual scores, as might beexpected. The animals were (as always with octopus experiments) from a wild popula-tion, not of identical size, presumably not all equally responsive to food or shock orequally experienced in identifying objects by touch. They had not all been kept in thelaboratory for exactly the same length of time before training was begun, and Fig. 2shows that the performance of at least some of them was still improving at the end of

J17 38 mm. t , 19 mm."10-

(b) 25 mm.+, 12 mm.

J27 12 mm.+, 6 mjn. J52 38-nim.+, 6* mm."

200Trials

Fig. 2. Details of some typical training experiments in which individual octopuses learned todiscriminate between cylinders of different diameter. There were 40 trials per day in two groupsof 20 (10 + , 10 — ). In Expts. (a), (b) and (c) the ratio of the diameters of the cylinders to bedistinguished was similar. In (d) the smaller cylinder had an overall diameter of 18 mm., beingmade up from seven 6 mm. units (see Fig. 1). Ease of discrimination is clearly not related to theratio of the diameters. The compound cylinder 6* mm. in (d) is much more readily distinguishedfrom the 38 mm. cylinder than is the simple 19 mm. cylinder in (a), despite its having very nearlythe same overall diameter.


the training period. It is nevertheless clear that the scores made in this sort of experi-ment are related to differences in surface curvature of the cylinders to be distinguished.This suggests that an octopus learns to recognize a cylinder from the degree of distor-tion this imposes on the arms or suckers used to grasp it.

- 4 0

-30

8o

"Random error*

O75 % correct

-20

-10 —

-0I I I I I

10I

20 30Difference In curvature measured as1/rx100

Fig. 3. Showing that the proportion of errors made varies with the difference in surfacecurvature of the objects to be distinguished. Each point plotted shows the result of an experi-ment in which an octopus was trained to discriminate between two cylinders of differentdiameter. The diameter of the cylinders used in each group of experiments are given along theabscissa; clearly the ratio of the diameters bears little relation to the number of errors made.The abscissa also shows the difference between the cylinders measured in terms of surfacecurvature; the proportion of errors made declines as the difference in curvature increases.Plots • and O respectively show the results of experiments with single and compound cylinders(see Fig. i), the stated diameter of the latter being the unit and not the overall diameter, whichwould appear to be irrelevant.

It can readily be shown that the curvature of the arm or arms grasping the cylinderis irrelevant. What the animal responds to is the distortion imposed on the individualsuckers actually in contact. Thus the composite cylinders 6* and 8* in Fig. 1 weretreated as being of the diameter of their component rods, instead of in relation to theiroverall diameter. 6*, for example, had an overall diameter of 18 mm. and a componentdiameter of 6 mm. When required to distinguish between this composite cylinder anda second, simple cylinder of 38 mm. diameter, three octopuses averaged 9-3 errors intheir second 100 training trials. In a similar experiment using a simple 19 mm.cylinder and the same 38 mm. cylinder, five octopuses averaged 43-6 errors (Fig. 2).

438 M. J. WELLS

The difference in the two sets of results is explicable if the composite cylinder istreated as being of the diameter of its components. Further experiments with com-posite cylinders, confirming this, are summarized in Fig. 3.

(2) Transfer tests

The object P1, a Perspex cylinder with grooves cut into it, must distort the rimsof any suckers in contact with it more than the grooveless but otherwise similar P4(Fig. 1). Presented to animals trained to prefer a large to a small diameter cylinder,one would expect P 4 to be accepted more often than P1, if distortion of the suckers isindeed the basis of the discrimination of the cylinders.

Table 1 summarizes the results of a number of tests in which Pi and P4 werepresented in place of the objects used in training. These tests were made after the endof training, and each object was presented 10 times, the order of presentation beingsystematized in the same way as in training. There were no rewards and no punish-

Table 1. Transfer tests following training to distinguish betweencylinders of different diameter

No. of times that eachobject was taken in ten presentations

Animal

J8 IJ9 \Jio J

Ji4J30J31J3O j

Discrimination(cy Under

j - . •

mm.)

25 + . 6 -

38 + , 12-

25+, 1 3 -

IQ + , 6 » -

38 + , 6 » -

12 + , 6 » -

8» + , 10-

vJlwUVCU

Pi

{•Total 5

2

{3Total 6

ftTotal 3

f 2

1 °I 0Total 2

{ITotal 12

Total

2

7341

1

18

P 4

799

25

4

910

19

IO2

1 2

IO

67

23

910

19

1

63331

1 7

->Smooth

12 mm.

z———40

4

51

0

6

10

5

15

—

—

z——

,cylinders

25 mm

—

—

—

—

92

11

91

1

11

10

414

—

—

z——

J50

J52J57J58

J63 IJ64 J

K2 ]K7

KillKnfK13K14J

• Compound cylinders made up of 6 mm. or 8 mm. diameter units, giving overall diameters of18 mm. and 24 mm. respectively. J30 and J31 were also tested with objects PSG and PCG, bothgrooved (see Fig. 1); both were rejected; J30 took PCG once only, and J3I each object once only.


ments. In all 12 sets of tests, following training in which the larger cyUnder was thepositive stimulus, P4 was taken more frequently than Pi (Table 1).

To check that P4 was not inherently a more attractive object than P i , transfer testswere used with a further six animals, trained to take 8* and reject a 19 mm. cylinder.In these tests P4 was taken 17 times and P1 18. Some further tests were carried outusing cylinders of 25 and 12 mm. diameter. The results of these tests are also sum-marized in Table 1; again the scores are in the expected directions.

(3) Training experiments with other shapes

In a previous report (Wells, 1964 a) it has been shown that octopuses can be trained todistinguish between a sphere and a cube (PS and PC in Fig. 1). Rounding the cornersof the cube (PC 2) leads to a decline in the performance of trained animals. Replacingthis ' cube' by a narrow rod (PR) having the same radius of curvature as the roundedcorners of PC 2 led to an immediate improvement in performance, the number oferrors made returning to the levels achieved in the original PS/PC discrimination.

It was argued from this that the rod is a satisfactory substitute for a cube becauseit constitutes, as nearly as is geometrically possible, a cube without flat surfaces.This would make discrimination from a sphere easier, since, so far as the round rimsof the suckers of an octopus are concerned, a sphere the size of PS is also a flat surface.The effective substitution of the rod PR for the cube PC is accountable if the octopusis assessing shape from the distortion imposed on individual suckers rather than fromtheir relative positions in space.

If this is the correct explanation, it should be possible to make a cube/sphere dis-tinction more difficult by roughening up the surface of the objects, so that bothdistort the suckers in contact. This was done in the case of the grooved objects PSGand PCG (Fig. 1) and had the expected results. Octopuses trained to distinguishbetween these two made more than twice as many errors as in discrimination of astraightforward cube and sphere (Fig. 46).

One further experiment was made using two objects, the cube PC and a slab (PSLin Fig. 1) with the same ratio of surface area to corner. Four animals were trained for340 trials. This proved to be a very dirEcult discrimination and the collective score ofthe four animals was not significantly different from chance for the first 200 trials oftraining (x2 = o'5^> P = > 25 %)• I n a ^^ X4° trials the four animals together made58 % correct responses, which is just significant at the 1 % level (jf = 6-9, P = < 1 %) .This result is again consistent with the view that objects are distinguished by thedistortion of the suckers; PSL, the slab, has areas where individual suckers can wraparound two corners at once. In textural terms, it is locally 'rougher' than anyplace on PC, except for the 3-plane corners, which both objects have in common.But the distinction remains very difficult, because the octopus will not always manageto grasp the object in such a way as to get a maximally 'rough' sample.

DISCUSSION

The experiments reported above continue earlier work (reviews, see Wells, 1962,1963 a) all of which indicates that octopuses are unable to learn to make discrimina-tions that would require them to take into account the relative positions of the suckers.

440 M. J. WELLS

The experiments with simple and compound cylinders show that an octopus does notassess the diameter of these from the bending of its arms. Instead, the animal judgesdiameter from surface curvature, measured by the degree of distortion that contactimposes on the rims of the suckers sampling the surface.

19 n. 19

200 300Trials

Fig. 4. Plots showing the course of five series of training experiments. Results (a) show: • , theerrors made when an attempt was made to train six octopuses to distinguish between two identi-cal 19 mm. cylinders. This was done to control the possibility that the testing sequence wasitself responsible for 'discriminatory' scores; O, the errors made when octopuses weretrained to distinguish between a cube and a flat slab having the same area to corner ratio(4 animals), and ©, the errors made in a simple textural discrimination between rough andsmooth cylinders (26 animals). ResultJ (b) similarly show: • , errors made in learning todistinguish between a cube and a sphere roughened by grooves (5 octopuses), and O, between asmooth cube and a smooth sphere (6 animals). Pictures of the objects used in these experi-ments are included in Fig. 1.

Two questions arise out of this. First, is the degree of sucker distortion the onlymeasure by which an octopus can assess the physical qualities of objects that it picksup? And, secondly, where are the sense organs concerned?

Tactile discrimination of surf ace curvature and shape by the octopus 441

The answer to the first query would appear to be 'yes'. Attempts have been madeto train octopuses to distinguish between objects differing in weight, and these havefailed despite the fact that octopuses obviously compensate for the weight of things thatthey handle. Muscle tension is increased to take the load, but the animals appear to bequite unable to learn to recognize this as indicating a property of the object lifted(Wells 1961a). Octopuses also seem to be unable to learn to recognize patterns ofstimulation affecting the suckers. All objects with grooves cut into them are treatedalike provided the ratio of grooved to smooth surface is the same; the arrangement ofthe grooves in terms of surface pattern and their orientation relative to the shape ofthe object both remain undetected (Wells & Wells, 1956, 1957). Moreover, the trans-fer tests and grooved cube/sphere experiment from the present series imply that tex-ture and surface curvature are measured in the same way, since one can be used as asubstitute for the other. It should in principle be possible to discover a surface textureequivalent of any specified shape so far as an octopus is concerned.

If distortion of the suckers is the measure by which octopuses assess the physicalproperties of objects that they touch, where are the sense organs concerned? Theycannot be in the stalks of the suckers, because these stretch and twist while the animalis grasping objects, apparently without affecting assessment of surface characteristics.It seems unlikely that they are on the infundibular surface because this is drawn upaway from the contact when a sucker grips. This leaves the rims and the outer partsof the sucker disks, which are known to be very sensitive to mechanical stimuli(ten Cate, 1928).

The anatomy and distribution of the sense organs in the suckers of Octopus havebeen carefully studied by Graziadei (Figs. 5 and 6; references see Graziadei, 1962,1964; Rossi & Graziadei 1958). He reports several types of cellular elements, particu-larly numerous in the epithelial layer at or near the rims of the sucker. At least someare chemoreceptors. Of the types shown in Fig. 5 the elongate form (5 a) with a capof clear cytoplasm extending to the surface through a hole in the cuticle is presumablyof this nature. Further elements with a rounded cap of clear cytoplasm (Fig. 5#)described both from the suckers (Rossi & Graziadei, 1958) and from the so-called'olfactory pit' at the entrance to the mantle (Watkinson, 1909; Wells, 1963b) arepossibly developmental stages of the same chemoreceptors. In vertebrates there is arapid turnover of taste receptors (Beidler, 1961) and it seems not improbable that thisis also true of the receptors in the octopus, which are in an even more exposedposition. These presumed chemoreceptors are the only sensory elements known topenetrate to the surface of the suckers.

Of the other three types so far described the rounded, deeply buried forms with finecollaterals (Fig. 5 c, d), at the base of the epithelial layer, seem best placed to respondto the pressures generated when the rim of a sucker is bent around a curved surface,or locally distorted by application to an irregular one. It is suggested that these are thedistortion detectors providing the information on which mechanotactile discriminationis based.

One further group of nervous elements in the suckers may have something to dowith mechanotactile discrimination. These are the large encapsulated cells (Fig. 5/)found in the muscles and connective tissue near the margins of the suckers.

These are themselves innervated by fine processes which appear to come from the

442 M. J. WELLS

epithelia of the rims of the suckers. Apparently homologous elements are found justbelow the epithelia in Loligo, and actually within the epithelial layer of Sepia (Grazia-dei, 1959). It seems improbable that the encapsulated endings in Octopus themselvesrespond to distortion of the sucker disk, because most of them occur in the loose con-nective tissue around the outer edge of the sucker, where they are unlikely to beaffected by pressures on the sucker disk (Fig. 6). Their function is perhaps to act asrelay stations summarizing information from the much more numerous epithelialmechanoreceptors (Graziadei, 1962).

Fig. 5. Sensory endings from the suckers of Octopus. All except (/) are found in the epitheliumwhich covers the sucker surface. Type (a) penetrates to the surface, where it opens througha pore in the thin cuticle secreted by the sucker surface; it is probably a chemoreceptor. Type (6)is perhaps a developmental stage of (a). Types (c) (d) and (e) (with a thin process extendingtowards the sucker surface) are presumed mechanoreceptors, being deeply buried among the tallepithelial cells of the rims of the suckers; collaterals from these cells, together with efferentfibres, form an extensive network at the base of the epithelial cells. Type (/), a larger ending, isfound encapsulated in the connective tissue outside the intrinsic musculature of the sucker(see Fig. 6). Type (/) is itself innervated, fine nerve endings, which synapse with it, coming, it isbelieved, from the more superficial receptors in the rims of the suckers, (a), (6) and (/) redrawnfrom figures and photographs in Graziadei (1962) ;(c), (J)and («) after Rossi & Graziadei (1958).

Repeated search has failed to reveal stretch receptors in the muscular disks orinfundibula of the suckers. Multipolar nerve cells are found among the muscles thatdirect the movements of each sucker as a whole, in association with the subacetabularganglion (Fig. 6), and there are good grounds for supposing that these are stretch


receptors (Graziadei 1964). But the movements of the sucker as a whole, its rotationand bending, extension and retraction are not correlated with the degree of distortionimposed on the sucker rim and disk when it grips or is applied to a surface, and the

Subacetabularganglion

Fig. 6. The distribution of the sense organs shown in Fig. 5. This figure shows, semi-diagrammatically, a longitudinal section through a sucker. In region 1, the inside of thesucker disk, sense organs of types (a) and (6) in Fig. 5 are most common. In the rim, region 2,(c), (d) and (e) are more abundant, and may number several thousands to a sucker. The largeencapsulated endings, E, ((/) in Fig. 5) are rarer, being numbered in tens rather than thousandsto each sucker. There are also muscle stretch receptors, in the extrinsic musculature of thesucker, grouped around the subacetabular ganglion. Repeated search has revealed no traceof proprioceptors within the intrinsic musculature, here shown shaded, or cross-hatched(sphincters) (mainly after Graziadei (1962)).

subacetabular stretch receptors cannot be responsible for the information on whichmechanotactile discriminations are based. Similar multipolar stretch receptors arefound in the arm muscles (Graziadei, 1964), but again these seem to play no part intouch learning, as the experiments with simpla and compound cylinders show. The

444 M. J. WELLS

situation, in short, closely resembles that in vertebrates such as ourselves, where toothe information supplied by muscular stretch receptors cannot be made the basis oflearned responses, in contrast with that supplied by mechanoreceptors in the jointsand skin (Merton, 1964). Cephalopods, like vertebrates, evidently enjoy two mechano-sensory systems, one related exclusively to the local adjustment of muscle tension, theother, superficial in origin, more immediately concerned with the animal's relationsto its external environment, signalling information to the highest parts of the brain,where it can play a part in learned processes (see Pringle, 1963). It seems reasonable tosuppose that a similar relationship between the learning brain and these two categoriesof receptor occurs in other invertebrate animals and that in the vast majority (all thosewith hydrostatic skeletons, for a start) performance is limited by the absence of joints,the information from muscular stretch receptors being used locally rather than centrallyand remaining unavailable as a basis for the modification of learned acts. In an octopusthe situation is merely more than usually obvious because the animal learns to recog-nize a wide variety of other inputs so rapidly.

SUMMARY

1. Experiments are described in which octopuses were trained to discriminate bytouch between pairs of Perspex cylinders of different diameter.

2. The proportion of errors made in experiments with thirteen different pairs ofcylinders shows that octopuses distinguish cylinders on a basis of the difference intheir surface curvature.

3. Curvature is detected from the degree of distortion of individual suckers. Thebend of the arm or arms grasping an object can be shown to be irrelevant by usingcomposite cylinders built up from narrower rods. These are treated as being of thediameter of their components.

4. Having been trained to take the larger and reject the smaller of two cylinders,octopuses tested with rough and smooth objects of the same size reject the rough andaccept the smooth. Apparently the sensory input produced by contact with an objecthaving a rough surface is similar to that produced by bending the suckers round asmooth curve of narrow radius.

5. The discrimination of cubes and spheres, which appears to be based on suckerdistortion at the corners of the cube, is upset by cutting grooves into the surfaces of thetwo objects.

6. These findings are discussed in relation to the anatomy of the sense organs in thesuckers. The development of two parallel mechanosensory systems, one relatedexclusively to the local adjustment of muscle tension, the other more concerned withthe animal's relations to its external environment and hence involved in learnedresponses, is common to the organization of cephalopods and vertebrates.

The author wishes to thank the director and staff of the Naples zoological stationfor their hospitality; Mr Michael Ashburner for helping carry out the 1963 series ofexperiments; and Dr Pasquale Graziadei for much useful discussion and permission toquote some of his unpublished anatomical work. The later part of this research wassupported by a grant from the Rockefeller foundation.


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BEIDLER, L. M. (1961). The mechanism of gustatory and olfactory receptor stimulation. In SensoryCommunication. Ed. W. A. Rosenblith. New York: John Wiley.

GRAZIADEI, P. (1959). Ricerche sul sistema nervoso di Molluschi Cefalopodi. Boll. Zool. tf>, 159-71.GRAZIADEI, P. (1962). Receptors in the suckers of Octopus. Nature, Land., 195, 57-9.GRAZIADEI, P. (1964); Muscle receptors in cephalopoda. (In the Press.)MERTON, P. A. (1964). Mammalian joint and muscle sense. Symp. Soc. Exp. Biol. 18 (in the Press).PRTNQLE, J. W. S. (1963). The proprioceptive background to mechanisms of orientation. Ergebn. Biol.

36, i-n.Rossi, F. & GRAZIADEI, P. (1958). Nouvelles contributions a la connaissance du systeme nerveux du

tentacle des Cephalopodes. IV. Le patrimonie nerveux de la ventouse de YOctopus vulgaris. Actaanat. 34 (Suppl.) 33, 1-79.

TEN CATE, J. (1928). Contribution a l'innervation des ventouses chez Octopus vulgaris. Arch nierl.Physiol. 13, 407-422.

WATKTNSON, G. B. (1909). Untersuchungen Uber die sogenannten Geruchsorgane der Cephalopoden.Jena. Z. Naturw. 37, 353-414.

WELLS, M. J. (i960). Proprioception and visual discrimination of orientation in Octopus. J. Exp. Biol.37, 489-W

WELLS, M. J. (1961a). Weight discrimination by Octopus. J. Exp. Biol. 38, 127-33.WELLS, M. J. (19616). Centres for tactile and visual learning in Octopus. J. Exp. Biol. 38, 811—26.WELLS, M. J. (1962). Brain and Behaviour in Cephalopods. London: Heinemann.WELLS, M. J. (1963a). The orientation of Octopus. Ergebn. Biol. 36, 40-54.WELLS, M. J. (19636). Taste by touch; some experiments with Octopus. J. Exp. Biol. 40, 187—93.WELLS, M. J. (1964a). Shape discrimination by Octopus. J. Exp. Psychol. (in the Press).WELLS, M. J. (19646). Detour experiments with octopuses. J. Exp. Biol. (in the Press).WELLS, M. J. & WELLS, J. (1956). Tactile discrimination and the behaviour of blind Octopus. Pubbl.

Staz. zool. Napoli, a8, 94-126.WELLS, M. J. & WELLS, J. (1957). The function of the brain of Octopus in tactile discrimination.

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