Brain and conscious representation of outside reality

Neuropsychologlo, Vol. 19, No. Pnnted m Great Briram

4, pp.

543-551,

OOZS-~3932/Sl/O40543-002,00/O 0 1981 Pergamon Press Ltd.

1981.

BRAIN AND CONSCIOUS

REPRESENTATION REALITY*

OF OUTSIDE

ED~ARDO BISIACH,ERMINIOCAPITANI,CLAUDIO LUZZATTI and DANIELAPERANI Centro di Neuropsicologia dell’Universitli di Milano, via Francesco (Recei~rl22

Sforza. 35- 20122 Milano.

Italy

January 1981)

Abstract-Right brain-damaged patients with contralateral neglect proved unable to describe accurately the left half of recollected images. Analogical brain processes seem therefore to underlie these representations. It is suggested that the left half of the spatial framework of visual representations is impaired in these patients. The alternative explanation based on the unilateral involvement of a hypothetical scanning of inner images is criticized.

INTRODUCTION AMONG the current theories of representation, the imaginal and the linguistic correspond to different aspects under which a conscious representation may be considered : respectively, the personal, sensory-like experience and its verbal report. A third and more abstract theory, the propositional, is more consonant with artificial intelligence models. Though lamenting that “imagery theorists have failed to say precisely what an image is”, ANDERSON[l] refers to the “imagery position” as the position maintaining spatial and modality specific properties for representations; which does, however, seem quite sufficient to define the imaginal, or “analogue” theory of representations. The linguistic form of representation is outlined by PAIVIO [2], a proponent of the verbal-pictorial dual code theory. The concept of propositional representation is less easy to define: it implies an associative network of symbols connected by way of multiple relations; it bears no analogue relationships to the represented object; it is not continuous, being as discrete and articulated as a word string though more abstract and free, if we understand it accurately, from the serial constraints of language processing. A more extensive treatment of propositional representations can however be found elsewhere [l, 31. There is no need here to analyze the arguments developed in support of, or against each theory, since they have recently been reviewed by Anderson. This author has offered an argument for the impossibility, in principle, of identifying the structure of representations on the grounds of any data experimental psychology might provide. On the other hand, “no or neuroscientist”, he claims, “has found anything like direct evidence for propositions images”. SHEPARD and PODCORNY (4) seem to admit that Anderson’s argument cannot be answered since no real advances have been made to elucidate the neural basis of representations and of processes operating upon them. The results of the present investigation, supporting an analogue, imaginal model for representations, seem to provide a first, tentative approximation at such an elucidation. *Research

supported

by C.N.R. grant

78.01998.04.1

15.4935 543

544

EDOAKDO BISIA~H. EKMINIO CAPI~ANI, CLA~J~I~ LLJZZAITI and DANIFLA PFKANI

MATERIALS

AND

METHODS

The study was carried out on right-handed subjects. The control group (C) comprised 41 patients free from history or present evidence of any disease involving the nervous system above the cervical cord. The mean age in this group was 63.0X_+ 10.08. The brain-damaged patients had clinical and instrumental evidence of a lesion confined to the right cerebral hemisphere. They were subdwided into four groups according to: (a) the presence or absence of homonymous visual field defects,assessed by means of theconfrontation method [5]: (b) the presence or absence of contralateral neglect on a cancellation task 161: (cl the occurrence of misplacements in representational space (see and contralateral neglect P~~c~duw). The-first group, H-N - was made up of I? patients wthout hemianopia L>,

42

46

deep lesion superficial lesion dwp+wperficiaf les101-1

FK,. I CT scans of patients

H- N

BRAIN

AND

REPRESENTATION

545

(mean age: 62.08 + 10.93). The second, H + N -, of 10 patients with hemianopia, ranging from very mild to severe, but without contralateral neglect (mean age: 6 I .40 _+7.88). The third, H + N +, of I5 patients with hemianopia and contralateral neglect (mean age: 65.00+ 10.99). The 13 patients who committed representational mislocations were asslgned to the fourth group, ML (mean age: 62.92k6.75). All patients of this group had visual field defects and contralateral neglect. Three brain-damaged patients had a brain tumour (NN. 63,64 and 86). All the other patients had sustained a cerebra-vascular attack during the few days before the examination with the exception of patient N. 78, who was examined a month after the onset of a brain infarction. Figures I-4 show the locus and extent of the lesion of each patient in the four brain-damaged groups; they were obtained from CT scans following a standard technique [7]. In two patients (NN. 45 and 59) the CT scans performed shortly after the stroke gave negative results. Patients without visual field defects and without contralateral neglect (Figure I) had comparatively small lesions which were mainly deeply located. The mean size of the lesions in patients with visual field defects but without contralateral neglect (Fig. 2) was approximately intermediate, being somewhat larger than in the former group but definitely smaller than in patients with contralateral neglect. Mo-eover, in 5 out ofthe 9positive findings the lesion was exclusively subcortical. In patients with contralateral neglect (Figs. 3 and 4) the lesions, besides being more extensive, were cortico-subcortical in the vast majority of the observations (24 out of 28). In all these patients the damaged area involved the curwJour or was strictly adjacent to it. The only exception seems to be patient N. 77, who had an infarction of the lower mesial region of the right occipital lobe and of part of

k!!!a 60

61

63 FIG. 2. CT scans of patients

H+ N-

546

EDOARDO BISIAC.H, ERMINIO CAPIJANI, CLAUDIO LCJZTAITI and DAYI~LA PWANI

64

67

65

69

72

76

BKAIN

AND

547

REPRESENTATION

the juxtaventricular structures of the temporal lobe, with possible inclusion of the hippocampus. It must be added that in patient N. 78, the only case in our sample to be tested more than a month after the onset of the illness and still showing contralateral neglect, the lesion extended to the midbrain.

The subjects were asked to give a verbal description of a place which was previously ascertained to be familiar to all of them; the cathedral square in Milan. This place has the advantages, for our purposes, of being reasonably square and. what is more important still, of having approximately the same number ofprominent features on each

81

85

86

88

89

87

m &Q

deep leston superflclal

lesion

deep + superfwl i

FIG. 4. CT scans of pattents

ML

cedema

kson

EI)OAKDO BISIACH. EKMINIO CAPITANI, CLAU~IO L~:ZZAITI and DAYILLA PrKAhr

548

side. The subjects were first requested to ~mapme themselves facing the front of the cathedral from the opposite side of the square. Once reasonably sure that the description was terminated. the examiner asked the subject to describe the square once again, this time Imagining the vantage point to be the central entrance of the cathedral. A subsidiary version of the task then followed, detecting possible mislocations of details from one aide of the square to the other in the patients’ representations. Whereas the first two descriptions were free from any ?patlal constraint. in this cued condition each subject was subsequently asked to descrlbc the ricrsmn\ of the task were separatei) scored for each subject. Inclusions of details unrelated to the squaw occurrIng in both berGon\ of the taqk wcrc also scored as well as misplacements of detail\ from the left \ldc to the right or kicc \er~ in the cued condition. AI already mentioned. subjects committing one or more crrorq oF elthcr kind were cla\\lficd in the ML group

RESULTS Table 1 shows the mean scores of the experimental groups in the free description of the square. A statistical analysis was carried out of the scores of the first four groups the group of patients whose representations were inaccurate (ML) could compared to the others. For each subject a laterality index was calculated formula : r-l rtl

and in the cued only. Obviously, not logically be according to the

x 100

where r and I are. respectively. the sum of right- and left-sided details given in the description of the square from the two opposite vantage points. Table 2 shows the mean laterality indexes of groups C, H - N - , H + N - and H + N + in the free and in the cued conditions. Unlike the others. the group of patients with visual field defects and contralateral neglect is characterized by a laterality index which reveals a relative neglect of left-sided details in the free description of the square. After a control of the homogeneity of variances, the laterality indexes were submitted to a bivariate ANOVA [S], according to a complete randomized design. Adopting RAO’S [9] approximation of the Wilks’ criterion to the F-distribution, highly significant intergroup differences were found [F (6. 146) = 7.555, P i O.OOOl]. Multiple comparisons were therefore carried out [IO] among the groups and between the variables “free” and “cued”. Group H + N-t was found to differ significantly from all the others in the free condition, whereas neither the differences among the other three groups nor the pairwise comparisons among the four groups in the cued condition reached significance. Furthermore. the difference between the two conditions of the task was found to be significant only in the H + N + group. Mean leftward and rightward displacements in the cued condition of group ML are shown in Table 3. The difference between the two means fell short of significance (P =0.087).

N

IL

Free condition 1K 2L

2R

IL

Cued condition IR 1L

-‘K

BRAIN

AND

549

REPRESENTATION

Table 2. Mean laterality index of groups C, H - N -, H + N -, H + N -, and H + N + in the free and in the cued conditions

c Free Cued

H-N- 1.16k37.6 2.24* 8.9

- 1.56k25.8 - 3.07 f 14.0

H+N-5.39k31.5 2.56_+17.1

H+N+ 56.35 + 31.2 2.68 f 18.9

Table 3. Means of displacements in the ML group Left ward

Rightward

0.769

2.076

Paired t test: I (12)= - 1.86412, P=O.O87, ns.

DISCUSSION The results of the investigation confirm and enrich earlier observations of a singular disorder affecting visual representations in some patients with a focal lesion of the right cerebral hemisphere [I 1J. Besides manifesting neglect of the half-space contralateral to their injured hemisphere, such patients may prove unable to describe the left half of recollected images accurately. This occurrence suggests that the pattern of brain activity underlying these representations is to a degree isomorphic with the object being represented. More generally, it suggests that the imaginal space is topologically structured across the two hemispheres. It is not implied, of course, that similar spatial properties characterize the form in which the information needed for a representation is stored in the neural network. In fact the failure to distinguish a representation, i.e. the temporary surfacing of information to a conscious level, from the continuous, quiescent storage of that information gives rise to much of the disagreement about the structure of representations. Commenting upon the phenomenon of contralateral neglect of representational space, BADDELEY and LIEBERMAN Cl23 point out that “using the simple analogy of the visuo-spatial scratch pad as a screen on which spatial information may be represented, one might conclude either that part of the screen was inoperative, or that the process of scanning the screen was defective, in each case allowing only part of the system to be used”. Both these alternative conclusions seem to entail the acceptance of a topological embodiment of the “scratch pad” in the brain: the first is however, in this respect, less implicit and is also more eligible on grounds of simplicity. The second suggests the inward turning of an attentional system, with the implication of possible failures in the exploitation of an otherwise intact representation. In our opinion it is safer and more parsimonious to hypothesize that full awareness of a representation is nothing over and above the display of some information within a spatiotemporal structure, like the “scratch pad”, somewhere in the brain. As for the exact locus, the best candidate seems to be the association cortex of the parieto-temporo-occipital junction. The activity of neurons in the parietal association cortex is involved in the fulfilment of the spatial frame which. in an orderly manner, relates the organism to his environment [13] and it is significant that in our sample of patients a cortical lesion was almost always found in association with contralateral neglect, whereas exclusively subcortical lesions were most often discovered in patients who did not manifest this syndrome. The hypothesis of a representational map reduced to one half is also more consistent with the pattern of

mislocations occurring in the cued description of the square in the ML group. Such errors might in part be interpreted as indicating a concurrent. though unrelated, disorder of topographical memory. This seems especially true for the rare inclusions, either in the free or in the cued report, of items bearing no relationship to the perspective which had to be described (errors of this kind were only made by patients NN. 86.88 and 91). Nevertheless, in some instances, the mere transposition of details from the relevant to the opposite side might have had a different causation, more strictly related to contralateral neglect. This is suggested by the fact that displacements from left to right were almost three times as frequent as displacements in the opposite direction. The difference is striking, even if it falls short of significance on account, presumably, of the insufficiency of the observations. An inability to scan the left half of the representational map could hardly explain these findings. On the contrary, the lack of this portion of the map is compatible with the fact that in some instances the left half of the representation is globally involved whereas, in others, part of the information destined for the left half of the map is addressed to the right half, as it happens in allesthesia. These two possibilities are illustrated, e.g. by the different behaviour of two patients (not included in the present sample) asked to set the hours on a blank clock dial (Fig. 5): both patients ignored the left half but whereas one ofthem showed a neat tendency to set down accurately on the right half of the clock face only the hours from twelve to six, the other packed all the hours of the clock into the right half of the dial. That would also explain why those patients who committed mislocations reported an equal proportion of left- and rightsided details in the free description of the square in spite of their left-sided neglect in the cancellation task. Concluding, the notion that contralateral neglect also occurs in the conscious representation of outside reality is supported by the behaviour of our patients. It follows that these representations really seem to be conceivable as analogical brain processes, at least with reference to the spatial framework within which the related information is ordered. It must however be remembered, in agreement with Paivio’s theory, that there exist clinical observations of patients with pathological loss of visual imagery whose representation of the visual world seems to rely solely on non-sensory, propositional information. BASS<)ct nl. [ 141 have recently described one such patient whose left hemisphere lesion was approximately the

a FK;. 5. Different

behaviour

of two patients with contralateral clock dial.

b neglect in setting the hours on a blank

BRAIN

551

AND REPRESENTATION

mirror image of that found in the right brain-damaged N. 77 of the present sample. He had a right-sided hemianopia with no indications of contralateral neglect, a transient pure alexia and a subclinical disorder of colour gnosis. The painful experience of being deprived of visual images was rather dramatically expressed by his paradoxical thought of being “unable to think anymore”. One possible explanation is that the left hemisphere of this patient could not generate images nor, owing to a disconnection mechanism, could it verbally report images generated in the right hemisphere; thus, it could only retrieve information in a linguistic or propositional form.

REFERENCES 1. ANI~ERSON,J. R. Arguments concerning representations for mental imagery. Psycho/. Rev. 85,249-277, 1978. 2. PAIVIO, A. The relationship between verbal and perceptual codes. In Handbook oJ’Perc~ption, E. C. CARTERF~TE and M. P. FRIEI~MAN(Editors), Vol. 8, pp. 375 396. Academic Press, New York, 1978. 3. RUMELHART,D. E. and NORMAN, D. A. The active structural network. In Exploration in Cognifion, D. A. NORMAN and D. E. RUMELHART (Editors), pp. 35 -64. Freeman. San Francisco, 1975. 4. SHI:PARII, R. N. and POIX;ORNY, P. Cognitive processes that resemble perceptual processes. In Handbook oJ Learniny and Cognitive Procrssus, W. K. ESTFS (Editor), Lawrence Erlbaum, Hillsdale, NJ, 1978. 5. BISIACH, E. and FA(;LIONI, P. Recognition of random shapes by patients with unilateral brain lesions as a function of complexity, association value and delay. Cortr.r 10, IOI- 110, 1974. 6. BISIAC’H,E., L~!ZZATTI, C. and PCRANI, D. Unilateral neglect, representational schema and consciousness. Brain 102,609-618, 1979. 7. LLZ~ATTI, C., SCOT.TI, G. and GATTOYI, A. Further suggestions for cerebral CT-localization. Correx 15, 483 490, 1979. 8. ANIXRSON, T. W. 4n fntroducrion IO Mulfirariafc Statistical Analysis. John Wiley, New York, 1958. 9. RAO,C. R. An asymptoticexpansionofthedistribution of Wilks’criterion. Bull.int.stat. Inst.33, 177 198.1951. IO. Rev, S. N. and BOSE, R. C. Simultaneous confidence interval estimation. Ann. math. Sfaf. 24, 513 ~536, 1953. 11. BISIAC’H,E. and L~ZATTI, C. Unilateral neglect of representational space. Corfrx 14, 129-133, 1978. 12. BADDELEY,A. D. and LIERERMAN,K. Spatial working memory. In Attet~tion and PerJ&-mance, R. NITKI:RSON (Editor), Vol 8. Lawrence Erlbaum, Hillsdale, NJ. In press. 13. LYNCH, J. C. The functional organization of posterior parietal association cortex. Behur. Bruin Sci. 3,485-534, 1980. 14. B.~sso, A., BISIAC-H,E. and LIIZZATI-I, C. Loss of mental imagery: a case study. Neuropsycholoyia 18, 435-442, 1980.

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