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Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19

Sustained attention following mild closed-head injury a

a

Raja Parasuraman , Sharon A. Mutter & Robert Molloy a a

The Catholic University of America , Published online: 04 Jan 2008.

To cite this article: Raja Parasuraman , Sharon A. Mutter & Robert Molloy (1991) Sustained attention following mild closed-head injury, Journal of Clinical and Experimental Neuropsychology, 13:5, 789-811, DOI: 10.1080/01688639108401090 To link to this article: http://dx.doi.org/10.1080/01688639108401090

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Journal of Clinical and Experimental Neuropsychology 1991, Vol. 13, NO. 5, pp. 789-811

0168-8634/9111305-0789$3.OO 0 Swets C Zeitlinger

Sustained Attention Following Mild Closed-Head Injury*

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Raja Parasuraman, Sharon A. Mutter, and Robert Molloy The Catholic University of America

ABSTRACT The sustained-attention performance of patients with mild closed-head injury (CHI) was examined within one month of injury using a high-event rate, digit-discrimination vigilance task with two levels of stimulus degradation (undegraded, highly degraded). Under undegraded stimulus conditions, vigilance performance for mild CHI subjects, uninjured case-matched control subjects, and college students was highly accurate and remained so across the entire task period. When stimuli were presented in degraded fashion, however, all three groups showed a similar decline over time (i.e., vigilance decrement) in hit rates and d’ scores. Although mild CHI did not lead to a greater rate of deterioration in vigilance performance in the degraded stimulus condition, it did produce lower overall levels of sensitivity ( 8 )in target detection. These results suggest that, during the first month after mild CHI, vigilance performance is unimpaired under normal task conditions, but may fall short under task conditions that require sustained effortful processing. These findings join a growing body of evidence showing that mild CHI can lead to measurable deficits in cognitive functioning.

The impact o f closed-head injury (CHI) on cognitive functioning can be extensive and wide-ranging. For example, disorders of memory (Levin, Papanicolaou, & Eisenberg, 1984; Mutter, Howard, Howard, & Wiggs, 1990; Schacter & Crovitz 1977), difficulties with language (Levin, Benton, & Grossman, 1982), and disturbances of intellectual function are often observed after CHI. Another consequence o f head trauma, noted more than 50 years ago b y Conkey (1938), is an impairment i n attention. Disorders i n attention are reported frequently after CHI

* This research was supported by Grant R49 CCR302583-0 from the Centers for Disease Control to The Catholic University of America. The authors are grateful to James Howard and Darlene Howard for their substantive suggestions concerning this research, and to Cheri Wiggs and Amy Ebner for their help in testing subjects. We would also like to thank Howard Champion. Wayne Copes, and the Trauma Research staff of the Washington Hospital Center MedSTAR unit for their important contributions to this research. Requests for reprints should be sent to Raja Parasuraman, Department of Psychology, The Catholic University of America, Washington, DC 20064, USA. Accepted for publication: January 4, 1991.

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(Rimel, Giordani, Barth, Boll, & Jane, 1981; Rimel, Giordani, Barth, & Jane, 1982) and recent research has confirmed the existence of problems in this area (e.g., see Van Zomeren, Brouwer, & Deelman, 1984, for a review). Moreover, attentional problems may persist long after apparent recovery from injury (Stuss et al., 1985). It is generally accepted that “attention” is not a unitary aspect of cognition, but rather comprises a variety of interacting processes (Parasuraman & Davies, 1984; Posner & Marin, 1985). One variety of attention - selective/divided attention - involves the selection of a stimulus source(s) in the presence of competing information; a second variety - sustained attentiodvigilance - involves the ability to maintain attention for infrequent critical events for sustained periods of time; and a third variety - attentional capacity allocation - involves the ability to vary the amount of attention in response to information processing demands. Although there is a fairly large literature on “attention” after CHI, researchers in this area have only recently begun to use these varieties of attention as a framework for the study of attentional disorders (e.g., Gentilini, Nichelli, & Schoenhuber, 1989; Gronwall, 1987, 1989; Levin, Goldstein, High, & Williams, 1988; Van Zomeren & Brouwer, 1987; Van Zomeren, Brouwer, & Deelman, 1984). In the present research, we investigate the effect of mild CHI on two varieties of attention. Specifically, we address the issue of whether mild CHI leads to impaired performance in a sustained attentiodvigilance task and whether the degree of impairment varies as a function of the amount of attentional capacity required by the task. Vigilance tasks, in which one must monitor a series of stimuli in order to detect an infrequent, critical target, are designed to assess a decline in performance efficiency over time. Normal performance on these tests is typified by high levels of accuracy in detecting critical targets at the beginning of the test. Thereafter, however, there is a decline in the detection rate with time on task, a phenomenon known as the vigilance decrement (Davies & Parasuraman, 1982). The magnitude of the vigilance decrement depends to a large extent on the type of vigilance task (Parasuraman & Davies, 1977; Warm & Jerison, 1984). For example, the decrement is more pronounced when the rate of stimulus presentation or the event rate is high (generally greater than about 24 events/min) and when the stimulus presentation mode is visual rather than auditory (Davies & Parasuraman, 1982; Jerison & Pickett, 1964; Parasuraman, 1979). Moreover, when observers are alerted to the Occurrence of targets, as for instance with a warning cue, detection performance is generally accurate and fast. Thus, greater decline in vigilance performance results from a requirement to watch for unpredictable, low-probability targets among a set of high-event-rate stimuli. Buchtel(l987) has suggested that a vigilance task may be “ideal for determining the degree of attentional deficit in patients after head trauma, even with minor damage” (p. 373-374). At present, however, there has been little empirical research on head injury-related deficits in vigilance performance and the evidence from the few existing studies is mixed. In an early study, Dencker and Lofving (19581,

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tested CHI patients several years after their head injury using a 15-min visual choice-reaction time task. The control group consisted of the non-injured twin siblings of the CHI group. The investigators stated that their intention was to measure performance decrement over time; however, a key feature of the standard vigilance task - that the target event be infrequent - was absent. Since all alternatives in the task occurred with equal frequency, one would not necessarily predict a performance decrement over time in this study. Indeed, neither group displayed a vigilance decrement, although the injured subjects did produce fewer correct reactions than controls. More recently, Ewing, McCarthy, Gronwall, and Wrightson (1980) used an auditory vigilance task with low-probability targets to assess the performance of a mild CHI group who had sustained injuries two years earlier and a matched control group. Since the CHI subjects had shown substantial recovery by the time of testing, all subjects were tested under conditions of mild hypoxia to augment any residual group differences. The CHI group was found to be significantly less accurate in detecting auditory targets than was the control group, but neither group exhibited a vigilance decrement over the course of the 30-min session. This is, perhaps, due to the fact that for half the subjects the vigilance task was interrupted by a memory task. Thus, again, the implications of the results for effects of CHI on vigilance are unclear. Van Zomeren and his colleagues (Van Zomeren & Brouwer, 1987; Van Zomeren et al., 1984) have reported the results of a study of auditory vigilance performance for CHI subjects with “severe” (unspecified) head injuries. Subjects were instructed to keep their eyes closed for the entire 30-min duration of the task (presumably to facilitate artifact-free recording of EEG, which was also measured). Not surprisingly, some subjects became drowsy, and the relationship between drowsiness and Performance was the major finding reported. That is, subjects who became drowsy, whether CHI or normal, showed a vigilance decrement, whereas subjects who remained alert did not. Again, however, the CHI group detected fewer targets than did controls. Brouwer and Van Wolffelair (1985) used this same auditory vigilance task in a study of eight CHI subjects with injuries of wide-ranging severity (Glasgow Coma Scale Scores in the range 615). As in the earlier study (Van Zomeren et al., 1984), subjects were tested with their eyes closed. CHI subjects had lower hit rates and slower reaction times than did controls, but both groups showed a similar vigilance decrement. The method the authors used to measure this decrement was unusual: They compared performance on the latter 20 mins of a 30-min vigilance test with the average level of performance in the first 10 mins of this task and a posttest separated from the main test by a 15-min rest break. This procedure departs from the examination of differences in detection rate as a function of time on task that is typical in vigilance research (e.g., Davies & Parasuraman, 1982; Warm, 1984). Moreover, although the procedure was designed to minimize possible confounds due to learning and changed expectancies, it does so at the expense of the information that is lost by collapsing a 20-min block of time into a single period.

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While these studies offer some evidence that CHI influences sustained attention, certain methodological problems tend to limit their usefulness. First, only one study (Brouwer & Van Wolffelaar, 1985) found the effect that defines vigilance - performance decrement over time, and in this study the method used to measure the decrement was somewhat atypical. Second, all of the studies used low-event-rate tasks. As pointed out earlier, vigilance decrement is h o w n to be reduced in such tasks (Jerison & Pickett, 1964). Third, auditory tasks were used in three of the four studies. This is also somewhat atypical of the vigilance literature, in which predominantly visual tasks are used. Furthermore, as mentioned previously there is evidence that auditory tasks may show less decrement over time than do visual tasks (Davies & Parasuraman, 1982). Hence, previous studies used two task features that made it less likely that a vigilance decrement would be observed. Rather remarkably, therefore, the available literature provides almost no evidence on the effects of head injury on visual sustained attention. Another characteristic of previous studies on vigilance and CHI is that they were concerned, for the most part, with moderately severe to severe levels of head injury. However, even mild head injury can affect cognitive functioning adversely (e.g., Hugenholtz, Stuss, Stethem, &Richard, 1988; Levin et al., 1987; Mutter et al., 1990; Ruff et al., 1989; Stuss et al., 1989). With the exception of the study by Ewing et al. (1980), only two other studies have specifically investigated the effects of mild head injury on sustained attention. Gronwall & Wrightson (1974) compared the performance of mild CHI patients (PTA ranging from less than 1 hour to 24 hours) with and without postconcussion symptoms (e.g., poor concentration, fatigue, irritability, headache) using the Paced Auditory Serial Addition Test (PASAT). Subjects were tested several times over a period ranging from 24 hours to 70 days after injury. PASAT scores were initially reduced for all groups of mild CHI subjects, but improved over testing occasions. In addition, improvements in these scores were related to reductions in postinjury symptoms (Gronwall & Wrightson, 1974). In the Gentilini et al. (1989) study, patients with mild CHI (GCS 13-15, loss of consciousness less than 20 mins, negative neurological exam, hospitalization less than 3 days) were tested 1 month and 3 months following injury on a “sustained attention” task involving the performance of a simple manual RT response to a stimulus appearing in the lateral visual fields. As in the Gronwall and Wrightson (1974) study, performance was impaired on the initial tests. Scores for CHI patients were lower than for controls on later tests as well; however, due to lack of statistical power resulting from loss of subjects, these results were inconclusive. According to Gronwall and her colleagues (Gronwall, 1987; Gronwall & Wrightson, 1981), while the PASAT is primarily an index of information processing rate, it also reflects aspects of attention such as concentration and sustained attention. Gentilini et al. (1989) were also concerned with studying changes in the rate of information processing, but they indicate very clearly that their simple reaction task was designed to measure sustained attention. Both the PASAT and simple RT may play a useful role in the assessment of early deficits and recovery

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of function in general attentional processes following mild CHI (Gronwall & Wrightson, 1974). Indeed, these tests reveal substantial recovery in RT and attentional processes within the first three months after injury (see also Hugenholtz et al., 1988). However, the hallmark of failure in sustained attention - a decline in performance efficiency with time on task -is not revealed by these tests. Thus, as before, little information concerning the effect of mild CHI on vigilance performance can be gleaned from the existing literature. In the present study, we compared the sustained attention performance of mild CHI patients and uninjured control subjects during the first month after injury using a high-event-rate, visual vigilance task, combined with stimulus degradation to induce the need for effortful or controlled processing. Since the vigilance decrement is most pronounced and rapid in high-event-rate tasks (e.g., Davies & Parasuraman, 1982), we felt that such a task would be especially suitable for use with a mildly head-injured population. When a high-event-rate is combined with targets that impose a load on working memory (Parasuraman, 1979) or with targets that are degraded perceptually (Nuechterlein, Parasuraman, & Jiang, 1983; Parasuraman & Mouloua, 1987; Warm, Chin, Dittmar, & Dember, 1987), the vigilance decrement in detection rate is associated with a decrement in sensitivity (d’) as opposed to a pure change in the response criterion (6) (Parasuraman, 1979). For example, Nuechterlein et al. (1983) found that sensitivity in detecting a target digit among nontarget digits presented at a high-event-rate (60 events/min) declined markedly over a period of 8 mins when the stimuli were degraded but not when stimuli were undegraded. Converging evidence from dual-task (Parasuraman, 1985) and psychophysiological (Rohrbaugh et al., 1988) studies indicates that the sensitivity decrement in high-event-rate, degraded stimulus vigilance tasks is attributable to the need for sustained, effortful allocation of processing capacity (or controlled processing) to display monitoring (high-eventrate) and target discrimination (degraded stimuli). In contrast, when stimuli are highly discriminable or are presented within a low event rate, targets may be detected automatically and sensitivity does not decline over time, particularly if familiar stimuli such as digits and letters are used. Fisk and Schneider (1981) have also reported a relation between effortful or controlled processing and sensitivity decrement. In their study, sensitivity decrement was limited to a highevent-rate task in which stimuli (letters) were variably mapped to responses, a condition that requires controlled, capacity-limited processing (Schneider & Shiffrin, 1977). When stimuli and responses were consistently mapped to each other, allowing for detection on the basis of automatic processing after extensive practice, the sensitivity decrement was minimal. A distinction between automatic and controlled processing has frequently been used to explain patterns of intact and impaired cognitive functioning in clinical and other special populations. For example, it has been reported that impaired functioning in normal aging, depression, and Parkinson’s disease is restricted largely to tasks that require controlled processing (Hasher & Zacks, 1979; Roy-Byme, Weingartner, Bierer, Thompson, & Post, 1986; Weingartner,

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Bums, Diebel, & Lewitt, 1984). whereas cognitive impairments in Alzheimer’s disease, Korsakoff Syndrome, and severe CHI occur in tasks that require controlled processing as well as in those that involve primarily automatic processing (Levin, Goldstein, High, & Williams, 1988; Nestor, Parasuraman, & Haxby, 1991; Weingartner et al., 1981). This suggests two possible outcomes for the present study. If mild CHI disrupts both automatic and controlled processing in sustained attention, we would expect to see differences in vigilance performance between persons with mild head injuries and matched controls under both undegraded and degraded stimulus conditions. In contrast, if primarily controlled processing is affected, group differences in vigilance performance should be observed when stimuli are degraded, but not otherwise. Moreover, the basis for this p u p difference should be a reduction in sensitivity, but not in response criterion, for the CHI group.

METHOD

Subjects The experimental group consisted of 10 persons (8 males, 2 females) admitted to the Washington Hospital Center Shock-Trauma Acute Resuscitation (MedSTAR) Unit for mild closed-head injuries sustained during a motor vehicle accident. Pertinent medical and demographic data for these subjects are contained in Table 1. “Mild” closed-head injury was defined on the basis of the following criteria outlined by Rimel et al. (1981): Glasgow Coma Scale score on admission of 13-15 (maximum is 15). loss of consciousness of 20 mins or less, duration of hospital stay (for treatment of head injury) not exceeding 48 hours, and a normal neurological exam at the time of admission. Subjects who were under 15 or over 55 years of age were excluded, as were those with a previous history of head injury (within 6 months of the current injury). Also excluded were persons with a history of chronic alcohol or drug use and/or neuropsychiatric disorder. Subjects in the closed-head injury group (CHI) were tested on the sustained attention task an average of 10.4 days postinjury (range 0 - 32 days). The mean age of subjects in this group was 29.7 years (range 18-55 years) and they had an average of 14.0 years (range 12-20 years) of formal education. The CHI subjects obtained mean WAIS-R Block Design, Vocabulary, and Information scores of 31.1 (range 23 - 39). 41.8 (range 17 - 68), and 17.6 (range 7 27). respectively. The matched control (MAT) group consisted of 10 subjects (6 males, 4 females) who were matched to individual CHI subjects on the basis of age, education, and WAIS-R subtest scores. These subjects were either relatives or friends of the CHI subjects or were recruited through advertisement in local newspapers. The subjects in the MAT group had a mean age of 28.6 years (range 19 - 52 years), an average of 13.6 years of formal education (range 12 - 20 years), and mean WAIS-R Block Design, Vocabulary, and Information, scores of 37.2 (range 25 - 55). 51.2 (range 20 - 67). and 20.2 (range 5 - 28), respectively. There were no significant differences between the head-injured and control subjects on any of these subject variables (age: t (18) < 1; education: t (18) < 1; block

’

One subject (see Table 1) was found later to have moderate diffuse cerebral edema with subarachnoid hemorrhage; however, the vigilance data for this subject were not atypical of the remaining CHI group data. In fact, this subject achieved the second highest overall d’ score in the group.

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Table 1 . Demographic, Intelligence, and Medical Data for CHI Patients. SN

Age

Educ(yrs)

Block

Vocab.

1 2 3 4 5 6 7 8 9 10

28 33 23 55 20 27 29 18 42 22

14 14 14 20 16 12 12 12 14 12

23 29 34 23 28 39 37 28 36 34

34 40 36 68 37 62 45 21 58 17

Info. 13 14 17 27 14 22 20 16 26 7

GCS

CT

15 15 15 15 15 15 14 15 15 15

Normal None done Normal Normal Normal Diffuse edema w/SAH Normal None done Normal Normal

Abbreviations: SN = Subject Number; Educ. = Education; Block = WAIS-R Block Design score; Vocab. = WAIS-R Vocabulary score; Info. = WAIS-R Information score; GCS = Glasgow Coma Scale; CT = Computed Tomography; SAH = Subarachnoid Hemorrhage

design: t (18) = 1.7; vocabulary: t (18) = 1.40; information: t (18) c 1). The vocabulary scores of the MAT subjects were somewhat higher than those of the CHI subjects; however, we are unaware of any evidence linking WAIS-R vocabulary scores with sustained attention performance; and except for the mentally retarded (Warm & Berch, 1987), psychometric intelligence test performance has been found to be unrelated to performance on sustained attention tasks (Davies & Parasuraman, 1982). The college control (COL) group consisted of 15 students (8 males, 7 females) from the Catholic University of America. The COL group had a mean age of 21.1 years (range 18 - 33 years), an average of 13.5 years of formal education (range 12-16 years), a mean WAIS-R Vocabulary score of 54.7 (range 41 - 65), a mean Information score of 19.7 (range 13 - 22) and a mean Block Design score of 39.2 (range 23 - 46). All subjects were paid for their participation in the study.

Vigilance Task The vigilance task was a digit-discrimination task used in previous studies of vigilance in normal young adults (Nuechterlein et al., 1983; Parasuraman, 1985). older adults (Parasuraman, Nestor, & Greenwood, 1989), and in subjects under alcohol intoxication (Rohrbaugh et al., 1988). Single digits (0 through 9) were presented for 1 0 0 msec at a rate of 1 per second using a Kodak Carousel E-2 slide projector (focal length = 6 inches) fitted with a Gerbrandts electronic shutter. The projector and shutter were controlled though the game port of an Apple IIe microcomputer. At a viewing distance of 1 meter, the digits subtended 2.7 degrees horizontally and 3.6 degrees vertically. The digits were degraded by blurring or defocusing the projected image. (This was equivalent to decreasing the slide-to-lens or object distance while keeping the slide-to-screen or image distance constant). The power of a correcting lens, P c (diopters), required to restore the image to the focused level was used to quantify the degree of image degradation, For a Pc value of 2.0, the digits appeared clear and focused, whereas for a Pc value of 3.00, they appeared highly blurred. In the present study, stimuli were presented either virtually undegraded at Pc = 2.0, moderately degraded at Pc = 2.75, or highly degraded at Pc = 3.00. The digit 0 was the designated target ; all other digits were nontargets. Digit stimuli

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were presented in a pseudo-random sequence, with the restriction that identical digits never followed one another. Targets were presented at irregular time intervals with a probability of 0.25, and were preceded by each nontarget an equal number of times. Subjects indicated target presence by depressing a response key (Apple IIe game paddle) held in their preferred hand. No response was required for nontargets. In each condition (normal and degraded), a total of 486 trials (120 targets and 366 nontargets) were presented over a period of 8.1 mins. Although the stimuli were presented continuously, trials were divided into six, 1.35-min blocks of 81 trials each for the purposes of assessing performance changes over time.

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Procedure Subjects were tested individually in a single, 3-hour session during which a number of other cognitive tasks were administered. The sustained attention task was completed after a 30-min rest break in the last hour of the session . The complete sustained attention task consisted of three parts, an initial test of visual acuity, a practice period, and the main vigilance task. Since accurate performance in the vigilance task required good visual acuity, subjects with uncorrected vision below 20/40 as measured by the Snellen test were excluded from the experiment. One subject from the MAT group and no subjects from either the CHI or COL groups were eliminated by this restriction,. In the practice period, subjects received short blocks of trials under both normal and degraded stimulus conditions. The experimenter was present in the testing room throughout this period, and feedback and rest breaks were provided so that performance could be assessed under “alerted” detection conditions. Practice blocks were administered in the following order: (Block la) 40 trials with focused stimuli, (Block Ib) 41 trials with stimuli slightly defocused (Pc = 2.00). and (Block 2) 81 trials with highly degraded ( P ~ ~ 3 . 0 0 ) stimuli. Feedback on hits and false alarm rates was provided at the end of each block. Subjects were required to achieve a criterion performance level of at least a 75% hit rate and no more than a 10%false alarm rate or a d’ criterion of 2.0 in the degraded stimulus condition. This criterion level was set on the basis of previous studies with normal young and old subjects using the same task (Parasuraman et al.. 1989). To ensure that performance in the degraded stimulus condition reached a stable level, an additional three practice blocks were given (81 trials each, with 2-min intervening rest breaks). Stimuli in these three practice blocks were presented at a highly degraded level if the subject was able to reach criterion with this level of image degradation in Block 2. If the subject was unable to reach criterion, stimuli in Block 3 were presented at a moderately degraded level (Pc = 2.75) and if the subject’s performance was very accurate (i.e.. 90100% hits and 510% false alarms), stimuli in Blocks 4 and 5 were presented at a high level of image degradation (Pc = 3.00). Otherwise stimuli remained at the moderate level of degradation for the last two blocks. Overall, subjects received a total of 405 trials of practice prior to performing the main vigilance part of the task. This relatively large amount of practice ensured that potential differences in sustained attention between head-injured and conaol subjects would not be contaminated with the effects of familiarity, learning. or other factors. Fatigue was not a major factor because the individual practice blocks lasted only 1.35 min each, and frequent rest breaks were provided. All subjects reached criterion at the highest level of image degradation within 160 trials. The main vigilance task period followed the practice period after a short break. Subjects were tested, without feedback, in both normal stimulus and degraded stimulus conditions. For the degraded stimulus condition, Pc = 3.00 was used since all subjects were able to achieve criterion at this level of image degradation in the practice trials. Each condition lasted for a continuous period of 8.1 min and there was a 20-min rest break between the two conditions. The order of administration for the two conditions was counterbalanced across subjects.

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RESULTS The hit (correct identification of a target) and false alarm rates (incorrect identification of a nontarget as a target) were computed for the six, 81-trial blocks in each condition. The hit and false alarm rates were then used to obtain measures of sensitivity and response criterion. The signal detection theory (SDT) measure of sensitivity, d',is very robust to violations of the assumptions of the theory in vigilance and recognition memory tasks (Craig, 1987; Davies & Parasuraman, 1982; Swets, 1986). However, the SDT criterion measure,@, is much less robust and its use has been criticized (Dusoir, 1975). Snodgrass and Corwin (1988) compared the robustness of different criterion measures and concluded that the criterion cutoff measure, C, which is defined as half the sum of the normalized hit and false alarm rates, is superior to@ because C is orthogonal to d' whereas@ is not. We therefore used d' as our sensitivity measure and C as our criterion measure. All results reported as statistically significant are associated with p values of .05 or less.

Practice Trials To ascertain whether detection performance for the three groups differed under short-term, "alerted" conditions, scores obtained in the final practice block were compared. No significant group differences were found for hit rates (mean scores: CHI - .93, MAT - .94, COL - .915), F(2,27) < 1, MSe = .004), false alarm rates (mean scores: CHI - .02, MAT - .019, COL - .019), F(2,27) < 1, MSe =.0002), d' (mean scores: CHI - 3.52, MAT - 3.58, COL - 3.44), F(2.27) < 1, MSe =.219), or C (mean scores: CHI - .285, MAT - .272, COL - .333), F(2,27) < 1, MSe =.02). Thus, initial detection performance was similar for the three groups. Vigilance Trials Preliminary analyses of hit and false alarm rates indicated that there were no significant main effects due to the order in which the normal stimulus and degraded stimulus conditions were administered. This factor did not enter into any significant two-way interactions with group (all Fs < 1); however, there was a Group x Order x Block interaction for the false alarm rates in the degraded stimulus condition, F(10, 120) = 3.285, MSe = .001. This interaction was due to the fact that differences among the three groups were somewhat greater in the last three blocks for testing order 2 (normal - degraded) than for testing order l(degraded normal). However, since false alarm rates for both testing orders were consistently higher for CHI subjects than for control subjects in each of the six blocks, all subsequent analyses were based on data collapsed across the two orders. To examine performance changes over time in the normal stimulus condition, hit and false alarm rates for the CHI, MAT, and COL groups were computed for each of the six consecutive blocks of the task. Mean hit rates by block in this condition are displayed by group in the upper portion of Figure 1; mean false

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alarm rates by block are displayed in the lower portion of the figure. Mean hit and false alarm rates collapsed across the six blacks of trials for the three groups are presented in Table 2. As Figure 1 shows, detection performance for the three groups in this condition was comparable (all Fs < 1) and virtually error-free in each of the six blocks of trials. The overall hit rates for the CHI, MAT, and COL groups represent performance levels in which an average of about 1, 5 , and 3 targets, respectively, were not correctly identified over the 8.1 min period of the vigilance task. False alarm rates for the CHI, MAT, and COL groups were also low, representing an average of about 4, 4, and 3 nontargets incorrectly identi-

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fied as targets, respectively. Because error rates in this condition were so low, the SDT measures, d' and C , were not computed. It is clear, nonetheless, that under the normal stimulus condition there was no vigilance decrement over the six blocks. Moreover, the detection performance of the CHI group did not differ from that of the two control groups. The distributions of hit and false alarm rates collapsed across the six blocks of trials for the CHI, MAT, and COL groups in the degraded stimulus condition are shown in Figure 2; group means for these data are presented in Table 2. These

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distributions show that within-group variability was slightly higher for the head injured group than for the other two groups and that group differences appear to be present in false alarm rates, but not in hit rates. Closer examination of individual scores within the distributions indicated that 4 CHI subjects had hit rates equal to or above the mean for the MAT group, whereas only 2 CHI subjects had false alarm rates equal to or below the mean for the MAT group. Mean hit and false alarm rates for the three groups in each of the six consecutive blocks of the degraded stimulus condition are presented in Figure 3. These scores were submitted to separate 3 (group) x 6 (block) mixed-factorial analyses of variance. As the upper portion of Figure 2 indicates, the CHI subjects had slightly lower hit rates in the degraded condition than did the MAT and COL controls, but the effect of group was not significant, F(2,27) = 1.169, MSe = .062. There was, however, a steady decline in hit rates over block, indicative of a vigilance decrement, F(5.135) = 4.459, MSe = .006, and the absence of a Group x Block interaction, F(10,135) < 1, showed that hit rate trends over time were similar for the three groups. False alarm rates across blocks for the three groups are displayed in the lower portion of Figure 3. There was a main effect of group, F(2,27) = 8.468, MSe = .004, showing that false alarm rates differed among the three groups. However, false alarm rates remained stable over the six blocks, F(5,135) < 1, MSe=.001, and the absence of a Group x Block interaction, F(10,135) < 1, indicated that all three groups showed this pattern. Pairwise comparisons (Tukey HSD) of group means collapsed over blocks (see Table 1) indicated that the CHI group had a significantly higher false alarm rate than did either the MAT group or the COL group, who did not differ significantly from each other (dt = .041). The CHI subjects demonstrated an approximately three-fold increase in false alarm rate as compared to the matched control group (6.5% versus 2.1%).

Table 2. CHI and Control Group Scores for the Normal and Degraded Image Conditions Collapsed Over Six Blocks of Trials. CHI

MAT

COL

Normal Image Condition: Hits False Alarms

989 (.012) .011 (.017)

959 (.083) .011 (.016)

.976 (.051) .009 (.012)

Degraded Image Condition: Hits False Alarms d' C

.844(.118) .065 (.035) 2.73 (.823) .217 (.226)

.899 (.109) .021 (.022) 3.707 (.977) .325 (.252)

.907 (.072) .023 (.022) 3.606 (.726) .341 (262)

Abbreviations: CHI = Closed-Head Injury Group; MAT = Matched Control Group; COL = College Control Group. Standard deviations are in parentheses.

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1.00

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Fig. 3. Mean hit and false alarm rates by block for the CHI, MAT, and COL groups in the degraded image condition.

To determine whether variations in detection accuracy for the three groups in the degraded stimulus condition were due to differences in sensitivity or response criterion, overall d' and C scores were computed for each group*. Distributions of overall d' and C scores for the CHI, MAT, and COL groups are presented in Figure 4; mean values for these measures are shown in Table 1. Within-

'

The SDT measures of d' and C are non-linear functions of hit and false alarm rates. Hence the overall d' and C scores for the entire vigilance task (all six blocks) are not equivalent to the average of these scores computed for each block. Therefore, a separate analysis was conducted for overall d' and C scores.

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group variability was similar for the three groups for both measures and group differences appear to be present for d' scores, but not for C scores. Only 1 CHI subject achieved a d score equal to or above the mean for the MAT group, whereas 4 CHI subjects achieved C scores equal to or above the mean for the MAT group. Separate one-way analyses of variance for d' and C scores revealed a significant group effect for d', F(2,27)= 4.012, MSe = .72,but not for C,F(2,27)< 1, MSe = .061. Pairwise comparisons (Tukey HSD) of d' scores revealed that the

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CHI group had significantly lower sensitivity than did the MAT and COL control groups, whereas the d scores for these latter two groups were not significantly different (d, = 3 6 ) . Compared to the MAT group, the CHI group had a reduction in sensitivity of 26%. To examine changes in d' and C over time, these scores were computed for each block and submitted to separate 3 (group) x 6 (block) mixed-factorial analyses of variance. The upper portion of Figure 5 shows mean d' scores across the six blocks. Analysis of these scores revealed significant main effects of block, F(5,135)=2.374,MSe = .193, and, as in the previous overall d analysis, of group,

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F(2,32) = 3.717, MSe = 2.284. However, the interaction between group and block was not significant, F(10,160) < 1. Thus, despite overall group differences in d' scores, the three groups showed a similar decline in these scores over blocks. The trends over time in the criterion measure, C, are shown in the lower portion of Figure 5. The effect of block on C was significant, F(5,135) = 4.147, MSe = .039, indicating that this measure increased over the six blocks of trials. As in the prior analysis of overall C scores, there was no effect of group, F(2,27) < 1,MSe = .172, and the absence of a Group x Block interaction, F(10.135) c 1, indicated that the three groups showed an increasingly conservative bias in response criterion over time. DISCUSSION This study of vigilance performance after mild CHI has produced three major findings. First, when digit stimuli were presented under normal viewing conditions, vigilance performance for both mild CHI patients and uninjured controls was highly accurate and remained so across the entire task period. In contrast, when stimuli were presented in degraded fashion, the three groups' vigilance performance deteriorated over time. This decline in performance was reflected in both decreased sensitivity (d') and increased conservative response bias ( C ) over blocks. Second, there was no evidence that mild CHI magnified the vigilance decrement observed under the degraded image condition. Thirdly, despite the absence of differential effects of CHI on the vigilance decrement, head-injured subjects demonstrated substantially lower sensitivity in the detection of degraded stimuli throughout the task period. Together these findings show that vigilance performance after mild CHI is comparatively normal under conditions that encourage automatic processing of stimuli. IJnder conditions that require effortful processing of stimuli, however, the vigilance performance of both CHI patients and uninjured controls deteriorates over time . Although mild CHI does not lead to a greater rate of deterioration in performance, it does seem to produce less sensitivity in target detection and this may, in turn, lead to significant deficits in vigilance. These findings are consistent with those of other recent studies (e.g., Gentilini et al., 1989; Hugenholtz et al., 1988; Levin et al., 1987; Mutter et al., 1990; Rime1 et al., 1981) in showing that mild CHI results in measurable deficits in cognitive functioning. We emphasize at the outset, however, that because we tested our mild CHI subjects within the first month of their injury, our results do not address the issue of whether, and to what extent, the vigilance performance of individuals with mild CHI recovers over time. We therefore preface the following discussion with the qualifier that the results may apply only to the period of time immediately following mild CHI. Recovery periods ranging from 1 to 3 months have been reported for other attentional skills (Gronwall & Wrightson, 1974; Hugenholtz et al., 1988). but there are no comparable studies of recovery of vigilance following mild head injury.

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Certain aspects of the present results for mild CHI subjects parallel earlier findings on vigilance for more severely injured subjects, whereas other aspects do not. Vigilance decrements have not been observed in a number of prior studies (e.g., Dencker & Lofving, 1958; Ewing et al., 1980; Van Zomeren & Brouwer, 1987) and, using undegraded digit stimuli, we likewise failed to find a performance decrement over time for our mild CHI and uninjured groups. On the other hand, vigilance performance for all groups clearly declined over time when digit stimuli were presented in degraded fashion. Nuechterlein et al. (1983) have suggested that under normal conditions, encoding of stimuli may occur automatically, with very little demand for processing capacity. Under these conditions, a vigilance decrement may not be observed. However, recognition of highly degraded images requires considerable effort and the demand for effortful processing remains high over the entire task. Rapid vigilance decrements have been observed under these conditions (Neuchterlein et al., 1983). In prior studies, task characteristics such as low event rate and auditory presentation may have played a role in eliminating the vigilance decrement. The present results suggest that another factor may be important, namely, the vigilance tasks in earlier studies could be accomplished without effortful or capacity-limited processing. When the vigilance task did not involve high demand for effort, our mild CHI patients, like uninjured controls, did not exhibit poor vigilance performance. In contrast, when continued effortful processing was required for the recognition of degraded digit stimuli, both CHI patients and uninjured controls exhibited a marked decline in target detection rate. This decline was a function of both a decreasing ability to detect targets (i.e., decreased perceptual sensitivity) and an increasing reluctance to respond positively to stimuli (i.e., increased conservative bias). Even under high effort demands, however, mild CHI did not lead to a more rapid rate of decline in vigilance performance. The evidence from this study therefore supports the recent conclusion of Van Zomeren and Brouwer (1987) that the vigilance performance of CHI patients is as stable over time as that of uninjured controls (see also Brouwer & Van Wolffelaar, 1985). In a vigilance task, changes in performance over time - the vigilance decrement - can be distinguished from the overall level of performance or the level of vigilance (Parasuraman, 1984). Although differential effects of CHI on the vigilance decrement were not observed in the present experiment, the level of vigilance was consistently lower for mild CHI patients than for controls under degraded stimulus conditions. Low accuracy scores for brain-damaged patients are frequently observed in vigilance tasks (e.g., Brouwer & Van Wolffelaar, 1985; Dencker & Lofving, 1958; Ewing et al., 1980; McDonald & Burns, 1964; Van Zomeren & Brouwer, 1987; Van Zomeren, Brouwer, & Deelman, 1984). Unfortunately, signal detection measures have not been employed in all of these studies and the evidence from those studies that do use these measures is mixed. For example, Ewing et al. (1980) reported that a lax response criterion was responsible for the greater number of errors observed for CHI patients on an auditory vigilance task; however, Brouwer and Van Wolffelaar (1985) found no criterion differences for

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their CHI and control groups on a similar auditory task, but did observe group differences in sensitivity in the pretest and posttest of their main vigilance task. The results of the present study are generally in line with those of Brouwer and Van Wolffelaar (1985): The low level of vigilance for CHI patients relative to controls was due to lower perceptual sensitivity (d‘) and not to differences in response criterion (C) alone. Interestingly, the reduction in perceptual sensitivity associated with mild CHI (26%) is comparable to that observed with the same vigilance task under high doses of alcohol (22%; Rohrbaugh et al., 1988) and greater than that associated with increasing adult age (12%; Parasuraman et al., 1989). The observation that differences in perceptual sensitivity for the CHI and uninjured groups occurred only under the degraded stimulus condition provides some support for the second of the two predictions made earlier: That is, mild CHI has a detrimental effect on vigilance performance when controlled or effortful processing is required. What is not clear, however, is whether group differences in perceptual sensitivity under degraded stimulus conditions were due to the failure of CHI patients to mobilize the eflorr required to process high-event-rate, briefly presented, degraded digit stimuli or simply to the fact that CHI produces ageneral eZevulbn in perceptual threshold (e.g., Dencker & Lofving, 1958;Hannay, Levin, & Kay, 1982; Reusch, 1944a, 1944b). CHI patients’ detection accuracy for degraded digits may be especially low because encoding these digits places additional demands upon a perceptual system that is already impaired. From this viewpoint, one might expect that detection accuracy for CHI patients would be lower than that for uninjured controls regardless of the effort demands of the detection task. This was not the case, however. Detection accuracy for CHI patients was not impaired under normal stimulus conditions, nor was it impaired with degraded stimuli under “alerted” conditions in the practice trials. This latter finding suggests that a simple “effort” explanation also will not suffice. Rather it seems that the combined effects of the high processing effort required by the vigilance task and some other factor led to the lower sensitivity scores for our CHI patients. One possibility for this unknown factor may be that the neuropathological changes that accompany mild CHI lead to changes in arousal mechanisms. Gronwall and Wrightson (1974) have suggested, for example, that attentional deficits after CHI may be due to lowered arousal resulting from reduced brainstem reticular formation activation. The neural systems mediating performance on vigilance tasks are not well specified, but intact performance seems to depend on the functional integrity of the ascending reticulo-thalamic pathways as well as on the prefrontal and posterior parietal cortices (Aston-Jones, 1985; Mesulam, 1981; Parasuraman, 1984; Parasuraman & Nestor, 1986). Except in severe cases, however, head trauma may result in damage to only limited regions within these widely distributed neural systems. Indeed, Ommaya and Gennarelli (1974) have suggested that mesencephalic and caudal diencephalic areas of the brain are far less vulnerable to injury than

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are fronto-temporal cortices. On the other hand, brainstem functions regulated by higher level cortical and diencephalic control systems may be disrupted indirectly by damage to these areas (Ommaya,l979). Animal models of human acceleration/ deceleration injury provide evidence that “mild” concussion can result in brainstem changes. For example, Povlishock and colleagues (Povlishock, Becker, Miller, Jenkins, & Dietrich, 1979; Povlishock, Becker, Sullivan, & Miller, 1978) have observed transient neuronal permeability alterations in some brainstem areas as well as damage in the endothelium and blood-brain barrier of blood cells in the brainstem. Moreover, there is evidence of brainstem axonal degeneration after minor head injury (Jane, Steward, & Gennarelli, 1985; Povlishock & Coburn, 1989). Thus it seems possible that brainstem dysfunction after mild CHI, whether due to insult to the brainstem itself or to cortical and diencephalic structures, could lead to transient changes in arousal level. Prior research has shown that the level of vigilance is affected more directly than the vigilance decrement by changes in tonic arousal (see Davies & Parasuraman, 1982, for a review). For example, stressors that lower arousal, such as heat and alcohol-induced drowsiness, lead to lower overall levels of vigilance, but have little effect on the vigilance decrement (e.g., Erwin, Wiener, Linnoila, & Truscott, 1978; Poulton, 1977). Thus, one possibility is that our CHI patients were suffering from lower tonic arousal and were unable to expend the greater effort required to encode degraded stimuli. Previous studies using the same vigilance task as the present study have shown that normal subjects with low arousal levels as assessed by self-report (Matthews, Davies, & Lees, 1990) or autonomic measures (Munro, Dawson, Schell, & Sakai, 1987) show reduced sensitivity towards the end of the task under degraded-stimulus conditions. However, this idea is incompatible with findings from studies of EEG and heart rate activity during vigilance indicating that even individuals with severe head injuries do not show comparatively lower levels of tonic arousal (e.g., Brouwer & Van Wolffelaar, 1985; Van Zomeren et al., 1984). Moreover, we did not observe a sensitivity deficit for our CHI subjects under the alerted conditions of the practice trials when feedback and encouragement were provided. In combination, these two findings suggest that mild CHI may disrupt mechanisms of phasic rather than tonic arousal: That is, individuals with mild CHI can not sustain accurate detection performance under capacity-demanding conditions unless adequate motivation is provided. This attentional deficit may best be characterized by what Stuss and Benson (1984) have described as “wandering attention” in head-injured patients who are fully alert and cooperative, but who are easily distracted by external stimuli. Before concluding, we would like to emphasize the practical implications of these findings. “Real world” vigilance tasks may vary in the absolute level of performance required. For example, suppose a detection rate of 75% is adequate for one job, whereas a rate of 95% is necessary for another. In both cases, a vigilance decrement will only be problematic if performance falls below the required criterion. Although it is clear that mild CHI did not lead to a faster rate

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of decline in vigilance over time, it is also clear that during the first few weeks following their injury, our CHI patients’ performance was functionally lower than that of controls, even in the early stages of our capacity-demanding vigilance task. Thus, for certain tasks, especially those requiring substantial amounts of effort or those involving suboptimal encoding conditions, individuals with mild CHI may fall below some necessary level of perfoxmance sooner than do individuals without injuries. The perception of this deficiency may be partially responsible for the numerous clinical and anecdotal reports of disorders in attention and concentration after mild CHI (e.g., Rimel et al., 1981). It will be important in future research to determine when, and if, after mild CHI, the level of vigilance for capacity-demanding tasks returns to normal.

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