DEFICITS IN THE CONTROL OF THE ATTENTIONALFOCUS IN CHRONIC SCHIZOPHRENICS

Masafumi Mizuno1,2, Carlo Umiltà1 and Giuseppe Sartori1

(1Dipartimento di Psicologia Generale, Università di Padova, Italy; 2Department ofNeuropsychiatary, School of Medicine, Keio University, Japan)

ABSTRACT

The ability to control the size of the attentional focus and thus to modulate processingefficiency was investigated using simple reaction times in central vision in 17 chronicschizophrenic patients and 17 normal control subjects. The size of the attentional focus wasmanipulated by varying the size of a central box (i.e., a pre-cue), where the imperativestimulus appeared. In accordance with previous studies, in normal controls reaction timeincreased with box size. In contrast, in schizophrenic patients reaction time did not dependon box size. That is, schizophrenic patients did not show the inverse relation between sizeof the box and speed of processing, which is observed in normal controls. These resultssuggest that a deficit in controlling the size of the attentional focus is a basic impairment inchronic schizophrenia. It was also found that schizophrenics are more susceptible thancontrols to paracontrast.

Key words: attention, attentional focus, schizophrenia

INTRODUCTION

Neuropsychological investigations carried out on schizophrenic patients havehighlighted impairments of various cognitive functions. Cognitive deficits havebeen reported to involve object recognition (Anderson, 1988), short term verbalmemory (Rutschmann, Cornblatt and Erlenmeyer-Kimling, 1980), and semanticmemory (McKenna, Mortimer and Hodges, 1994).

Processes related to early stages of visual perception, like backward masking(Saccuzzo, Hirt and Spencer, 1974), picture integration (Knight, Sherer, Putchatet al., 1978), perceptual grouping (Cox and Deventhal, 1978; Schwartz andGilmore, 1980), and processing of low spatial frequencies (Schwartz andWinstead, 1982; Schwartz, McGinn and Winstead, 1987) were reported to bedefective in schizophrenic patients.

Posner, Early, Reiman et al. (1988) found that schizophrenics at their firstacute episode were selectively slow at re-orienting attention to the right visualfield after an invalid cue. They interpreted that as an impairment of the lefthemisphere attention orienting mechanisms. This asymmetry was replicated byPotkin, Swanson, LaBerge et al. (1990) in non-medicated chronic schizophrenicswith an acute exacerbation (but not in medicated ones).

Also Liotti, Dazzi and Umiltà (1993) suggested that specific attentional

Cortex, (1998) 34, 263-270

mechanisms are affected in schizophrenics. Their patients, who were underneuroleptic treatment, were less disrupted than controls by incorrect cueing andtook more advantage than controls by correct cueing.

In the present paper we will investigate a different aspect of visuospatialattention, namely the capability to control the extent of the attentional focus,thereby modulating processing efficiency within its borders.

A well-known metaphor for the deployment of attention in the visual spacelikens the focus of attention to the beam of a “spotlight” (see, e.g., reviews inPosner, 1980; Umiltà, 1988). Based on this metaphor, the attentional focuspossess three interesting properties. It moves from one location to another. Itmoves in analogue fashion rather than jumping instantaneously from onelocation to another. It is characterized by a specific size. Therefore, it illuminatesat different times different locations and the extent of the illuminated area at agiven time is restricted.

A slightly different metaphor is that proposed by Eriksen and his colleagues(Eriksen and St. James, 1986; Eriksen and Yeh, 1985; also, see Umiltà, 1988,for a review), who believe that a zoom, or variable power, lens is a more aptanalogy than a spotlight. The zoom lens can cover a variable portion of thevisual space, and resolution improves when this region is constricted.

Many authors have proposed two-stage models of the way attention isdeployed in the visual space (e.g., Bergen and Julez, 1983; Duncan, 1980;Hoffman, 1979), among which the one proposed by Jonides (1983) has been themost influential. According to Jonides, there are two modes of attending a visualdisplay: attentional resources can be allocated evenly across the entire display orthey can be concentrated on one display location only. In the diffuse mode, allthe display elements are processed in parallel at an uniform, and relatively slow,rate. In the focused mode, processing of the pre-cued element is facilitated,

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Fig. 1 – Schematic representation of the visual displays used in the experiment.

whereas processing of the other elements is inhibited.Several studies (e.g., Castiello and Umiltà, 1990, 1992; Egeth, 1977; Eriksen

and St. James, 1986; Henderson 1991; LaBerge, 1983; Usai, Umiltà andNicoletti, 1995) have shown that, when attention is in the focused mode, thespatial extent of the focus can vary, and an inverse relation between its size andprocessing efficiency can often been found. In particular, Castiello and Umiltà(1990, 1992) showed that the attentional focus can be made to fit a pre-cuedarea of variable size. They pre-cued visual areas by presenting empty boxes ofvariable size on a CRT screen (see Figure 1). Then, after a suitable interval, theimperative stimulus appeared inside the box. Efficiency of processing decreasedwhen the extent of the attentional focus increased, as indexed by the fact thatspeed of response to the imperative stimulus (i.e., simple reaction time) becameslower when the box size became larger.

The purpose of the present study was to explore whether the ability tocontrol the size of the attentional focus, and thus to modulate processingefficiency at its interior, is among those mechanisms of visuospatial attentionthat are impaired in schizophrenic patients.

MATERIALS AND METHODS

Subjects

The subjects were 17 chronic schizophrenic patients (14 males and 3 females) and 17normal controls (11 males and 6 females).

The patients were diagnosed by two independent psychiatrists. One was the head of thepsychiatric ward of Treviso General Hospital (Italy) and the other was one of the authors(M.M.). The diagnosis was based on DSM-III-R (American Psychiatric Association, 1987)criteria for chronic schizophrenia or chronic schizophrenia with acute exacerbation, on astructured psychiatric interview, and the Schedule for Affective Disorders and Schizophrenia(Endicott and Spitzer, 1978). The clinical symptoms of the patients were scored using theBrief Psychiatric Rating Scale (BPRS; Overall and Gorham, 1962) by trained clinicianswithout knowledge of the test results. Ten schzophrenics were out-patients of the MentalHealth Center in Treviso (Italy), a community psychiatric service. At the moment of testing,the other seven were, due to their exacerbation, in-patients of the Psychiatric Service ofTreviso General Hospital. In the case of this latter group, the experiment took place on theday of their discharge from the hospital, when the symptoms of exacerbation had completelydisappeared.

Fourteen of the patients were on neuroleptic medication, corresponding to 66-231 mgper day of chlorpromazine equivalent units (Bernstein, 1988), and 3 were drug-free.

As normal control subjects, 17 volunteers were tested. They were free from history ofpsychiatric and neurological symptoms and alcohol and drug abuse. They were matched forage to the schizophrenic group.

There was no significant age difference between patients and controls (patients = 29.4years, range 20-42; controls = 27.5 years, range 21-38; t = 1.158, d.f. = 32, p > 0.25).However, there was a significant difference between the two groups in years of schooling(12.2 years for the patients and 15.9 years for the controls; t = 6.382, d.f. = 32, p < 0.0001).

All subjects and controls were right-handed, had normal or corrected vision and wereunaware of the purpose of the experiment. Informed consent to administer the tests wasobtained from all subjects.

Apparatus and Stimuli

The apparatus and stimuli were largely based on those of the study of Castiello andUmiltà (1990), but the experimental situation was rendered easier by using only centrally

Attentional focus in schizophrenia 265

presented stimuli. Because eye movements can be abnormal and/or more difficult tosuppress in schizophrenics (e.g., Holzman, Proctor and Hughes, 1973; Kojima, Potkin,Kharazmi et al., 1989), the pre-cue and the stimulus were shown in central vision, thusreducing to a minimum the tendency to shift gaze upon pre-cue presentation (also, see Usaiet al., 1995).

The experiment consisted of two sessions. In each, the subjects were asked to sit infront of a CRT screen driven by an Apple Macintosh LC computer. The head was positionedin a head-and-chin rest, at a distance of 55 cm from the screen. In the experimental session,the visual display (see Figure 1) comprised the pre-cue, that is a square box, the side ofwhich could be 1, 3, or 5 deg, and the imperative stimulus (a black circle of 0.4 deg indiameter). The box was shown in the center of the screen and the circle was shown in thecenter of the box. No masking was presented.

After this session, a second session was conducted to obtain non-cued reaction times(non-cued RTs). In the visual display, only the imperative stimulus (the circle that wasused in the previous session) was shown in the center of the screen. In either session, theresponse to the imperative stimulus was executed by pressing the “space” key on thecomputer keyboard using the right index finger.

Procedure

Each trial in the experimental session started with the presentation of the box, whichremained on the screen until the end of the trial. Then, after an interval of 500 msec, theimperative stimulus appeared in the center of the box. On about 20% of the trials (catchtrials) no imperative stimulus was presented. The subject was asked to keep the eyes on thescreen steadily and was instructed to press the key as fast as possible in response to theimperative stimulus. Reaction time (RT) was measured from the imperative stimulus onsetto response emission. The subject had to refrain from responding on catch trials. Trials forwhich RT was shorter than l50 msec or longer than 1000 msec were considered errors.Each subject was run in 2 experimental blocks of 198 trials each. Therefore, for everysubject there were 396 trials overall: 318 regular trials and 78 catch trials. Before thebeginning of the first experimental block, the subject performed in a practice block of 50trials.

After completing the experimental session, each subject performed in the non-cued RTsession. In it, only the imperative stimulus (the black circle) was shown in the center of thescreen. The intertrial interval varied at random from 500 msec to 1000 msec. Each subjectcontributed first 20 practice trials and then 180 experimental trials.

RESULTS

Errors, including responses on catch trials, were very rare (about 2% in thepatient group and 1% in the control group) and the corresponding RTs werediscarded.

A preliminary analysis showed that there was no significant correlationbetween the dosage of neuroleptics in chlorpromazine equivalent mg and RTs inschizophrenic patients (r = 0.156, d.f. = 17, p > 0.50).

RTs were entered into a two-way analysis of covariance (ANCOVA), inwhich the between-subjects factor was Group (normal controls vs schizophrenicpatients), the within-subjects factor was box Size (1, 3, 5 deg), and the covariatewas years of schooling. The two main effects and the interaction weresignificant: F (1, 31) = 37.561, p < 0.0001, for Group; F (2, 64) = 26.843, p < 0.0001, for Size; and F (2, 64) = 11.937, p < 0.001, for the interaction. Anidentical ANCOVA was conducted on logarithmic transformations of RT data. It

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confirmed the significance of the two main effects and the interaction: F (1, 31)= 79.148, p < 0.00001, F (2, 64) = 35.664, p < 0.00001, and F (2, 64) = 27.856,p < 0.00001, respectively. Schizophrenics were slower than controls (399 msecvs 299 msec), and RT was inversely related to the size of the box (344 msec forthe l-deg box, 346 msec for the 3-deg box, and 356 msec for the 5-deg box).However, the interaction indicated that the size of the box had a different effecton RT depending on the group of subjects.

Therefore, RTs of normal controls for the three different box sizes (1, 3, 5deg) were entered into a one-way analysis of variance (ANOVA), which showeda significant main effect, F (2, 32) = 57.187, p < 0.00001. A Fisher’s posthocanalysis showed significant differences between 1 deg and 5 deg (1 deg: mean =289 msec, S.D. = 14; 5-deg: mean = 309 msec, S.D. = 20; p < 0.001), between3-deg and 5-deg (3-deg: mean = 298 msec, S.D. = 18; p < 0.002), and between1-deg and 3-deg (p < 0.005). Inspection of individual data showed that mostsubjects manifested the effect of box size: 15 out of 17 for the l-deg vs 3-degcomparison, 16/17 for the 3-deg vs 5-deg comparison, and 17/17 for the l-deg vs5-deg comparison.

In contrast, an identical one-way ANOVA did not show any significantdifferences for schizophrenic patients, F (2, 32) = 1.196, p > 0.25. Few patientsmanifested the effect of box size: 5 out of 17 for the l-deg vs 3-deg comparison,11/17 for the 3-deg vs 5-deg comparison, and 10/17 for the l-deg vs 5-degcomparison. RT was 399, 394, and 403 ms for the l-deg, 3-deg, and 5-deg box,respectively. With the Fisher’s analysis, only the 3-deg vs 5-deg comparisonapproached significance (p < 0.1).

Non-cued RTs were entered into an ANOVA along with cued RTs. Thebetween-subjects factor was Group (controls vs schizophrenics) and the within-subjects factor was Cue (present vs absent). The two main effects and theinteraction were significant: F (1, 32) = 41.62, p < 0.00001, F (1, 32) = 24.39,p < 0.00001, and F (1, 32) = 13.48, p < 0.0001, respectively. Schizophrenicswere slower than controls (366 msec vs 289 msec) and cued trials were slowerthan non-cued trials (349 msec vs 308 msec). However, the difference betweencued and non-cued trials was greater for schizophrenics than for controls (399msec vs 336 msec, and 299 msec vs 279 msec, respectively).

DISCUSSION

Performance of normal control subjects replicated the pattern found inprevious experiments (Castiello and Umiltà, 1990, 1992). They responded mostrapidly to the imperative stimuli within the small box, and most slowly when itappeared within the large box. This confirms that the extent of the attentionalfocus can vary and there is an inverse relation between size of the attentionalfocus and efficiency of processing.

In sharp contrast, RTs produced by schizophrenic patients were similar andclearly did not depend on box size (399, 394, 403 msec for box sizes 1, 3, and5). That is, schizophrenics did not show the inverse relation between size of thebox and speed of response. Thus, the present results suggest that the ability to

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control the attentional focus in accord with task demands is impaired inschizophrenics.

Castiello and Umiltà (1990, 1992) found the inverse relation only when theinterval between the pre-cue (i.e., the box) and the imperative stimulus wascomparatively long (500 msec; that is the interval that was used in the presentstudy). The inverse relation was instead absent with a much shorter interval (40-50 msec). That was taken to suggest that, in normals, the operation of varyingthe size of the attentional focus requires less than 500 msec and more than 50msec. Perhaps, in schizophrenics this operation requires a longer time and wasnot yet completed after 500 msec. Of course, it is also possible thatschizophrenics are unable to change the size of the attentional focus, regardlessof the time at their disposal.

For either group of subjects, cued RT was slower than non-cued RT. It isknown that, even between non-overlapping stimuli, paracontrast, which isequivalent to forward masking between overlapping stimuli, occurs (e.g.,Humphreys and Bruce, 1989). That is, a stimulus can mask another stimulus thatis presented after a short time interval, even though the two stimuli do notoverlap. As was demonstrated by Usai et al. (1995), with the type of cueing thatwas used in the present study, detection of the imperative stimulus is negativelyaffected by lateral masking (of the paracontrast type) from the borders of thebox. The difference between cued and non-cued trials was greater inschizophrenics than in controls. This findings might indicate that schizophrenicswere more susceptible than controls to paracontrast. One should consider,however, that on cued trials the cue-stimulus interval was fixed (500 ms),whereas on non-cued trials the intertrial interval varied between 500 and 1000ms. A variable time interval likely rendered it more difficult for the subject toprepare for the forthcoming stimulus, and thus increased RT. Even though thelengthening of RT might have been partially counteracted by the absence ofcatch trials, it is possible that schizophrenics were more affected than controlsby time uncertainty rather than by paracontrast.

Disorders of attention in schizophrenia have interested psychiatrists for along time (e.g., Bleuler, 1911). Several studies have reported that inschizophrenics disorders of sustained and spatial attention can be observed (e.g.,Liotti et al., 1993; Nuechterline and Dawson, 1984; Posner et al., 1988). In thepresent study, we have shown also a specific impairment in controlling theattentional focus. Such an impairment can cause a number of different problemsin visuospatial tasks, such as detection, localization, and discriminations and,thus, can affect schizophrenics’ cognitive efficiency.

Focusing attention is important not only in spatial processing but also inimage analysis (e.g., Kosslyn, 1987). For example, when a subject is askedwhether Rome is in the center of Italy, he/she has to generate a visual image andfocus attention on a certain part of the image. We have not studied focusingattention in the absence of externally driven stimulation, but it may well be thata similar pattern can be observed in imagery tasks.

Generally speaking, modulating the focus of attention is required in a numberof different basic abilities such as perception, visual search, visual imagery,speeded response to visual stimuli, and so on. An impairment of this operation

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can therefore have several side-effects in visuospatial tasks and can be related tomany negative symptoms of schizophrenia.

Deficits in focal attention can be related to some positive symptoms as well.For example hallucinations are explained in a cognitive framework as a self-monitoring disorder (e.g., Frith, 1992), which causes the inability of the patientto identify the source of the stimulus. Hoffman and Rappaport (1994) were ableto induce “hallucinated” reports in their hallucinated patients by using ashadowing task. If there is a disorder in focusing attention on the source ofstimulation, there is an increased possibility of misattributing its source.

Acknowledgement. This study was supported by grants from CNR and MURST to C.U.and G.S.

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(Received 15 February 1997; accepted 28 August 1997)

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